Handbook of Zoology: Volume 2 Pleistoannelida, Sedentaria II 9783110291681, 9783110291476

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Handbook of Zoology Annelida Volume 2: Pleistoannelida, Sedentaria II

Handbook of Zoology Founded by Willy Kükenthal continued by M. Beier, M. Fischer, J.-G. Helmcke, D. Starck, H. Wermuth Editor-in-chief Andreas Schmidt-Rhaesa

Annelida Edited by Günter Purschke, Markus Böggemann and Wilfried Westheide

DE GRUYTER

Annelida

Volume 2: Pleistoannelida, Sedentaria II Edited by Günter Purschke, Markus Böggemann and Wilfried Westheide

DE GRUYTER

Scientific Editors Prof. Dr. rer. nat. Günter Purschke Universität Osnabrück FB 5 - Biologie/Chemie Barbarastr. 11 49076 Osnabrück [email protected] Prof. Dr. Markus Böggemann Universität Vechta - Fakultät II Natur- und Sozialwissenschaften/Biologie Driverstr. 22 49377 Vechta [email protected] Herrn Prof. Dr. em. Wilfried Westheide Gerhart-Hauptmann-Str. 3 49134 Wallenhorst [email protected]

ISBN 978-3-11-029147-6 e-ISBN (PDF) 978-3-11-029168-1 e-ISBN (EPUB) 978-3-11-038884-8 ISSN 2193-4231 Library of Congress Control Number: 9783110291476 Bibliografic information published by the Deutsche Nationalbibliothek The Deutsche Nationalbibliothek lists this publication in the Deutsche Nationalbibliografie; detailed bibliographic data are available in the Internet at http://dnb.dnb.de. © 2019 Walter de Gruyter GmbH & Co. KG, Berlin/Boston Typesetting: XXX Printing and Binding: CPI books GmbH, Leck www.degruyter.com

Preface Annelida, the segmented worms, comprise one of the most important taxa of invertebrates. The majority of annelid species occur in marine environments but they can also be found in freshwater and terrestrial realms. In particular, the marine forms are one of the most widespread, abundant, and diverse elements of the world’s benthic fauna. Although comprising just approximately 21,000 described species, annelids show a remarkable diversity comparable, for instance, with that observed in crustaceans. This diversity could only be achieved by the plasticity of their bauplan constituting the prostomium, followed by a number of primarily identical modules, the segments, and the pygidium. Species are usually of median size and do not exceed a few centimeters in length. However, their range is much wider; some interstitial annelids of the smallest adult metazoans are known with body lengths of 300 to 400 µm such as certain Nerillidae, as well as species exceeding body lengths of more than 3 m such as Eunice aphroditois. The number of segments varies accordingly from less than ten to several hundred. The marine forms often show broadcast spawning and their life cycle is primarily comprised of a planktonic larval stage, the trochophore, and a benthic adult stage. However, there are many deviations from this pattern that, inter alia, are correlated with life style and body size. Thus, their reproductive biology is highly diverse as well. The traditional classification and subdivision of Annelida into Polychaeta and Clitellata comprising Oligochaeta and Hirudinea does not reflect their phylogenetic systematization, but the names polychaetes and oligochaetes are still in use for practical reasons. Recent phylogenetic analyses have confirmed that polychaetes constitute nothing else but a paraphyletic assemblage of the more or less plesiomorphic Annelida. The same applies for the oligochaetes representing a basal grade of Clitellata. Therefore, polychaetes are those annelids that do not possess a clitellum, a view that is followed in the ­Handbook of Zoology. Annelid phylogeny now sees a so-called basal grade only comprising a few taxa but the majority of Annelida, termed Pleistoannelida, are now classified into two large monophyletic groups: Errantia and Sedentaria. In a highly derived position, the latter also comprise Clitellata, earthworms and leeches. Thus, phylogenomic analyses led to the resurrection of two traditional taxa albeit with somewhat different taxon compositions that, for a long time, were not thought to represent monophyletic groups. In addition, some taxa that were once regarded to represent separate phyla turned out to be https://doi.org/10.1515/9783110291681-202

nothing else but true Annelida, although being morphologically highly derived especially with respect to one of the so-called key characters, segmentation. These taxa are Sipuncula, Myzostoma, Pogonophora, and Echiura, which are now placed in different positions in the phylogenetic tree of Annelida. This fact impressively demonstrates the adaptive capacity and potential of the annelid bauplan. It is hoped that these former phyla will be reduced in rank to the family level; this already happened to Pogonophora, which are now known as Siboglinidae, and the next candidate may be Echiura, which in the future may be known simply as Echiuridae, or for priority reasons, Thalassematidae. The vast majority of polychaete species is marine; here, they are dominant members of the epi- and endobenthos but there are also a few holopelagic species. Polychaetes comprise one of the most important groups of invertebrates in the marine food web, where they can be found in almost every habitat, often in high abundance. In addition, a few polychaete species managed to colonize even freshwater and terrestrial realms. ­Moreover, certain polychaetes occur in comparatively extreme environments—from hydrothermal vents at the ocean floor spreading centers to terrestrial ground water. Most polychaete species are microphagous or predatory but a number of species are symbionts or commensals. In contrast, the mainly terrestrial forms or clitellate oligochaetes are structurally more uniform but also have representatives in limnetic and marine habitats. Nevertheless, oligochaete Clitellata is a comparatively speciose taxon and many species are extraordinarily important members in terrestrial decomposer communities often occurring in high abundances. Surprisingly enough, one group of these oligochaetes is closely related to parasitic or carnivorous forms, the leeches. With global human activities and climate change, the distribution patterns of many species have been subjected to dramatic changes; as a consequence, certain introduced species turned out to become pests with often fatal effects for the original ecosystems. The Annelid volume of the first edition of the ­Handbook of Zoology appeared in the years between 1928 and 1934, edited by W. Kükenthal and T. Krumbach. In particular, the anatomical part still serves as a valuable resource of knowledge. However, since then, our knowledge on annelids has broadly increased. The amount of information on annelids has not only expanded in the number of investigated and described as well as revised taxa but the details of observations, quality of data, and numbers

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 Preface

of different approaches have increased. Moreover, in morphological and taxonomic research, new methods have become available such as electron microscopy and ­confocal laser scanning microscopy as well as molecular tools that currently allow us to sequence and analyze whole genomes. Although several reviews on annelids have been published, they usually cover only special topics in this group of invertebrates. Therefore, around the year 2010, the idea was born that a new edition of this very successful work would be urgently needed. Very soon thereafter, it turned out to be impossible to write a ­handbook in its strict sense treating morphology, anatomy, reproduction, development, ecology, phylogeny, and taxonomy on this group of animals in a single volume. Now, more than ever, such a task could not be achieved by a single person or by just a few authorities, and so we began looking for authors who could contribute to such a big effort. Unfortunately, we had to learn that for many annelid groups, specialists did not exist in the scientific zoological community or were not available for various reasons. Therefore, it took much longer than originally planned to compile the manuscripts and despite our efforts, there will remain a few gaps of missing chapters. This is the reason why currently only the polychaetes will be treated in the handbook. Because all the authors have many other duties and the writing of handbook chapters is rather time-consuming, it took some time to compile the manuscripts from our authors. It was a great advantage that each chapter ready for publication was published electronically in Zoology Online so that the c­ hapters were available for the scientific community quite soon after acceptance. All contributions were peer-reviewed and revised prior to publication. We were very happy and proud that it was possible to publish the first volume on annelids at the beginning of 2019 and now, within a comparatively short time after this date, the second volume appears in the same year. In the meantime, the Annelida series in the Handbook of Zoology will comprise four volumes. Because we try to keep as up-to-date as possible with scientific progress, we roughly follow the new phylogeny in the arrangement of the taxa treated in the various chapters, each of which is generally devoted to a single family. We are well aware of the fact that such a phylogeny is nothing else but a

hypothesis which, with our current knowledge, best explains the phylogeny or evolution of a certain group. Therefore, it cannot be excluded that this system would need to be revised somehow in the future resulting in a different order of taxa. Moreover, there are more than 100 families of annelids and the systematic position has not been solved for every taxon and there are still many open questions in their relationships. Therefore, some taxa may now seem to be in a position that is predisposed to changes; however, this does not interfere with the information contained in those chapters. Furthermore, because there are still several aspects of annelid phylogeny under discussion, not all of our colleagues and authors who contributed to this handbook accept this new phylogeny completely. This second volume covers the second part of Sedentaria comprising the clades Sabellida/Spionida and Opheliida/Capitellida. The latter also includes Echiura, a taxon that was among the first of the former annelidlike phyla to group constantly within the sedentary polychaetes in molecular phylogenetic analyses. Unfortunately, we still have a few gaps, which means a few families are missing, and it is hoped that we can add them in the forthcoming volume. Accordingly, the third volume will be devoted to the remaining Sedentaria with the exception of Clitellata and the first part of Errantia, whereas the final volume will treat the rest of Errantia. At this point, we would like to thank all the authors that contributed to this volume of the Handbook of Zoology; they have done an excellent job. The work of the various reviewers is gratefully acknowledged; reviewing scientific manuscripts always takes a considerable amount of working time, especially because some chapters on larger groups are voluminous. Nonetheless, their helpful suggestions for improvements helped in keeping the scientific standards as high as possible. Last but not least, we thank the lectors and employees of our publisher, De Gruyter, for their endless help and fruitful discussions during the publishing process. Günter Purschke, Wilfried Westheide, and Markus Böggemann Osnabrück, Wallenhorst, and Vechta, Germany, June 2019

Contents Preface

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List of contributing authors

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James A. Blake, Nancy J. Maciolek and Karin Meißner 7.4 Sedentaria: Sabellida/Spionida 1 Spionidae Grube, 1850 7.4.1 1 Introduction 1 Morphology 1 Reproduction and development 19 Biology and ecology 30 Phylogeny and taxonomy 38 References 90 James A. Blake and Nancy J. Maciolek 7.4.2 Poecilochaetidae Hannerz, 1956 Introduction 103 Morphology 103 Reproduction and development Biology and ecology 112 Phylogeny and taxonomy 113 References 118 James A. Blake and Nancy J. Maciolek 7.4.3 Trochochaetidae Pettibone, 1963 Introduction 120 Morphology 120 Reproduction and development Biology and ecology 131 Phylogeny and taxonomy 132 References 134

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120

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James A. Blake and Nancy J. Maciolek 7.4.4 Uncispionidae Green, 1982 136 Introduction 136 Morphology 136 Biology and ecology 139 Reproduction and development 140 Phylogeny and taxonomy 141 References 144 María Capa and Pat Hutchings 7.4.5 Sabellariidae Johnston, 1865 144 Introduction 144 Morphology 145 Reproduction and development 149 Biology and ecology 150 Phylogeny and taxonomy 153 Acknowledgments 158 References 158

María Capa, Adriana Giangrande, João M. de M. Nogueira and María Ana Tovar-Hernández Sabellidae Latreille, 1825 7.4.6 164 Introduction 164 Morphology 164 Reproduction and development 178 Biology and ecology 185 Phylogeny and taxonomy 189 Acknowledgments 203 References 203 Elena K. Kupriyanova, Alexander V. Rzhavsky and Harry A. ten Hove 7.4.7 Serpulidae Rafinesque, 1815 213 213 Introduction Morphology 213 224 Reproduction and development Biology and ecology 230 Acknowledgments 266 References 266 Günter Purschke Sedentaria: Opheliida/Terebellida/ 7.5 Clitellata: incertae sedis 275 Hrabeiellidae Christoffersen, 7.5.1 2012 275 275 Introduction Morphology 275 Reproduction and development 280 Biology and ecology 282 Phylogeny and taxonomy 282 References 283 James A. Blake & Nancy J. Maciolek 7.6 Opheliida/Capitellida 285 7.6.1 Opheliidae Malmgren, 1867 285 285 Introduction Morphology 285 Biology and ecology 288 Phylogeny and taxonomy 291 References 299 James A. Blake and Nancy J. Maciolek 7.6.2 Travisiidae Hartmann-Schröder, 1971, new family status 302 Introduction 302 302 Morphology Reproduction and development Biology and ecology 306

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Phylogeny and taxonomy References 310

307

James A. Blake Scalibregmatidae Malmgren, 1867 7.6.3 312 312 Introduction Morphology 312 Reproduction and development 323 Biology and ecology 326 Phylogeny and taxonomy 327 References 346 Wagner F. Magalhães and James A. Blake Capitellidae Grube, 1862 7.6.4 349 349 Introduction Morphology 350



Reproduction and development Biology and ecology 365 Taxonomy and phylogeny 370 References 394

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Jörn von Döhren 7.6.5 Echiura Stephen, 1965 (= Thalassematidae, Forbes & Goodsir, 1841) 404 404 Introduction Morphology 405 Reproduction and development 424 Biology and ecology 431 Phylogeny and taxonomy 434 References 438 Index

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Annelida will be continued in: Volume 3: Annelida, Sedentaria III and Errantia I, ISBN 978-3-11-029148-3 Volume 4: Annelida, Errantia II, ISBN 978-3-11-064531-6

List of contributing authors James A. Blake Aquatic Research & Consulting 24 Hitty Tom Road, Duxbury, MA 02332-4112, USA [email protected] María Capa University of the Balearic Islands Department of Biology Cra. de Valldemossa, km 7.5, Palma, Illes Balears, Spain E-07122 [email protected] Jörn von Döhren University of Bonn Institute of Evolutionary Biology and Ecology An der Immenburg 1, D-53121 Bonn, Germany [email protected] Adriana Giangrande University of Salento Piazzetta Arco di Trionfo, 1, 73100 Lecce, Italy [email protected] Harry A. ten Hove Naturalis Biodiversity Center PO Box 9517, 2300 RA Leiden, The Netherlands [email protected] Pat Hutchings Australian Museum Research Institute 1 William Street, Sydney, NSW 2010, Australia [email protected] Elena K. Kupriyanova Australian Museum Research Institute 1 William Street, Sydney, NSW 2010, Australia [email protected] Nancy J. Maciolek Aquatic Research & Consulting 24 Hitty Tom Road, Duxbury, MA 02332-4112 USA [email protected]

Wagner Magalhães Universidade Federal da Bahia Instituto de Biologia Labimar Rua Barao de Jeremoabo, 668, Campus de Ondina 40170-115 Salvador, Bahia, Brazil [email protected] João M. de Matos Nogueira Universidade de Sao Paulo Av. Prof. Almeida Prado nº1280, 05508-070 (Butantã), São Paulo, Brazil [email protected] Karin Meißner Senckenberg Forschungsinstitute und Naturmuseen (SFN) Deutsches Zentrum für Marine Biodiversitätsforschung Biozentrum Grindel, Martin-Luther-King-Platz 3, D-20146 Hamburg, Germany [email protected] Günter Purschke Osnabrück University Faculty of Biology/Chemistry – Zoology Barbarastraße 11, D-49076 Osnabrück, Germany [email protected] Alexander V. Rzhavsky† A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences Leninskij Prospekt 33, Moscow, 119071, Russia María Ana Tovar-Hernández Geomare & El Colegio de Sinaloa Av. Miguel Alemán 616-4B, 82040 Mazatlán, Sinaloa, Mexico [email protected]

James A. Blake, Nancy J. Maciolek and Karin Meißner

7.4 Sedentaria: Sabellida/Spionida 7.4.1 Spionidae Grube, 1850 Introduction The Spionidae represent one of the largest and most common polychaete families in marine benthic invertebrate communities; it currently includes approximately 590 species grouped into 38 genera. They are readily recognized by their general body shape, especially the anterior end, which carries a pair of long ­prehensile palps; the posterior extension of the prostomium, which is termed the caruncle; the form of the parapodia, which often have foliose postchaetal lamellae; dorsally flattened branchiae; and the presence of specialized chaetae including neuropodial and sometimes notopodial hooks, which are typically hooded. However, there is no single synapomorphy that distinguishes the ­Spionidae; instead, a suite of characters, some homoplasic, are used together to define the family. The Spionidae and five other morphologically similar family-level taxa have typically been grouped into the order Spionida (Blake 1996; Rouse and Fauchald 1997; Rouse and Pleijel 2001, 2006). Currently, these additional families include the Poecilochaetidae, Trochochaetidae, Uncispionidae, Apistobranchidae, and Longo­somatidae (genus Heterospio). The Poecilochaetidae, Trochochaetidae, and Uncispionidae are sister taxa to Spionidae and are treated in separate chapters in this handbook (Blake and Maciolek 2019a,b,c). Despite the presence of paired palps or tentacles, the last two families are not closely allied with the Spionidae (Fauchald and Rouse 1997) and are also treated separately (see Blake and Petti 2019 for Apistobranchidae). The genus Heterospio (Longosomatidae) is treated with the cirratuliform polychaetes (Blake and Maciolek 2019d). Spionids occur in a wide variety of habitats from the intertidal to the deep sea, sometimes forming dense benthic assemblages. Individuals may extend their palps from burrows or tubes to filter particles from the water; in other situations, the worms are surface deposit feeders and use their palps to sweep the sediment surface. Some spionids, such as Polydora and related genera, bore into calcareous substrates and are sometimes considered pests by the shellfish industry. Other polydorids are known to form tubes within or on sponges. A few species are opportunistic, occupying environments that are disturbed or organically enriched; such species have life history https://doi.org/10.1515/9783110291681-001

patterns that allow them to populate available areas rapidly. Details and references to these activities are provided in the Biology sections. Because so many spionids occur in shallow waters and are readily accessible for collection and study, the literature concerning their morphology, biology, ecology, and systematics is extensive. Several articles have treated the reproduction and larval development of multiple species (Hannerz 1956; Blake 1969, 2006; Blake and Arnofsky 1999) and elucidated the different types of gametes, spawning patterns, larval life, and larval morphology found in this family. Reproductive and larval data have recently been incorporated into phylogenetic ­analyses (Blake and Arnofsky 1999). In the sections that follow, we describe the morphology of adult and larval spionids, their biology and behavior, phylogenetic relationships, taxonomy, and current classification. The majority of illustrations have been taken from the works of three of the chapter authors and, where possible, our original plates or photographs have been used and reimaged, modified, or updated to better illustrate the topics in a manner different from that originally intended. Numerous new, original figures have also been incorporated. Every effort has been made to include abbreviations on the figures to identify key morphology. We expect that this chapter will serve to introduce new students of polychaetes to this large and interesting family. ZooBank Registration Number: urn:lsid:zoobank.org:pub:C49CF9A8-E94C-4AE8-B042-F7089CE6A9C3.

Morphology External morphology Body shape. The bodies of spionids are elongate and subcylindrical in cross-section. Although lacking any distinctive division into abdomen and thorax, they are divided as in other types of polychaetes into (1) a presegmental region consisting of the prostomium and peristomium, (2) a long segmental region, and (3) a postsegmental region consisting of the pygidium and a growth zone that produces new segments. Anterior segments are usually widest, with the body tapering posteriorly to a pygidium that consists of lobes, cirri, or discs (Figs. 7.4.1.1 B; 7.4.1.2 B). The anterior end bears a pair of long prehensile palps (Figs. 7.4.1.1 A–C, F–H; 7.4.1.2  A, B). Segments are numerous, short, and similar; the fifth segment is modified in some genera (e.g., Dipolydora and Polydora; Fig.  7.4.1.2  B). Branchiae are present on all genera (Fig.  7.4.1.1  B, F, G) except Amphi­ polydora, Glyphochaeta, and Spiophanes (Fig.  7.4.1.1  A)

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 7.4 Sedentaria: Sabellida/Spionida



and, when present, are limited to a few anterior chaetigers (Fig.  7.4.1.1  G), middle segments (Fig.  7.4.1.1  F), or continues for numerous segments (Figs. 7.4.1.1 B; 7.4.1.2 A, B) but are usually absent from far posterior segments. Dorsal membranous transverse crests are present on some species (Fig.  7.4.1.2  F). Transverse and/or longitudinal ciliary bands are usually present on some body segments and often form distinctive patterns (Fig. 7.4.1.3 C, G, I, J). Some genera have rows of pits or glands, usually on the venter (Fig. 7.4.1.3 H). Spionids generally have relatively narrow, elongate bodies ranging from 8 to 20 mm long and 0.5 to 1.0 mm wide, with 50 to 150 chaetigers; however, as noted subsequently, size differences can be extreme. Polydorella kamakamai is only 1.3 mm long and 0.3 mm wide with 14 chaetigers (Williams 2004), whereas the largest spionid recorded seems to be Lindaspio southwardorum from hydrothermal vents on the Juan de Fuca Ridge with the holotype 15.9 cm long, and 7 mm wide for 304 chaetigers; fragments of an even larger specimen were observed in the same collection (Blake and Maciolek 1992). Spio aequalis from New Zealand is reported to be approximately 15 cm long and 7 mm wide, only slightly smaller than L. south­ wardorum (Read 1999). Some species of Scolelepis such as S. foliosus can also be in the 14 to 15 cm range. Dipolydora concharum is also large, up to 14.0 cm long with 300 chaetigers (Blake 1971); however, this species is a shell borer and its burrows are curved and twisted, making extraction of complete specimens and measurements difficult. Spionid bodies are typically widest anteriorly due to well-developed parapodia, branchiae, and long capillary chaetae; posteriorly the parapodia are reduced, branchiae are shorter or absent, and capillaries are often replaced at least in part by hooks and short spines. Color. The larvae and postlarvae of some spionids are often characterized by distinct melanophores or bands and spots of black pigment and these are sometimes retained or carried over to the adults. The pigment pattern of adult Dipolydora socialis is a good example of this, having distinct bands of melanin on the dorsal and ventral surfaces of adults that are similar to the larval pigment pattern (Blake 1969, 1971). The bodies of adult spionids are generally tan or light brown in color when alive, with red blood visible especially in the branchiae and palps (Figs.  7.4.1.1  B, F;

7.4.1 Spionidae Grube, 1850 

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7.4.1.2 A, B); preserved specimens are often tan to opaque white. Adults are generally not heavily pigmented but some species have reflective yellow or white pigment or various colors that may be in bands or patterns on the body and along the palps (Fig. 7.4.1.3 G, I); such patterns are best observed when the worm is alive because, after preservation, this pigment either disappears or appears brown or black. External details of the integument. A general classification of annelid epidermal glands distinguishes between secretory cells loosely spread in the epidermis (“unicellular glands” sensu Storch 1988), and the condensed occurrence of secretory cells forming glandular fields and multicellular glands (Hausen 2005; Rößger et al. 2015). This classification is also applicable to secretory cells present in Spionidae. As in many polychaetes, isolated secretory cells are present in the epidermis of Spionidae (Söderström 1920; Radashevsky 2012). They are of different shapes, open externally and are present in different parts of the body, in particular on the prostomium, pygidium, parapodia, branchiae, and the venter. The function of these cells has not been demonstrated, but is usually suggested to be involved in mucus production. The occurrence of multicellular glands has been reported repeatedly. Claparède (1870) observed “poches glanduleuses” or glandular pouches in Polydora. Later, the presence of large multicellular glands was also confirmed for other genera, for example, Spio, Microspio, Pygospio, and the Polydora complex (Mesnil 1896; Söderström 1920; Fauvel 1927). Glandular organs discovered more recently are those associated with grooved neuropodial spines in Glyphochaeta (Bick 2005a) and the large glandular organs present in some anterior segments of Glandulospio that open in the region of neuropodial chaetae (Meißner et al. 2014). Today, it is accepted that complex multicellular glands are rather common and diverse among Spionidae, and in particular among the Spioninae, and their comparison requires the consideration of all available information (Meißner et al. 2012; Rößger et al. 2015). However, except for the parapodial glandular organs of Spiophanes (Meißner et al. 2012) and the ventral epidermal glands of Spio and Microspio (Rößger et al. 2015), multicellular glands of Spionidae have not been studied using the techniques of modern histology and complementary anatomical data are lacking. Based on current knowledge, the

◂ Fig. 7.4.1.1: Examples of Spionidae, entire worms and prechaetiger morphology. A, Spiophanes bombyx, entire worm, dorsal view; B, Malacoceros vulgaris, entire worm, dorsal view; C, same, anterior end, dorsal view; D. Malacoceros fuliginosus, anterior, dorsal view; E, Aonides oxycephala, anterior end, dorsal view; F, Pygospio elegans, entire worm, dorsal view; G, Streblospio shrubsolii, entire worm, right lateral view; H, Scolelepis squamata, anterior end, dorsal view; I, Spio sp. (as S. filicornis), anterior end, dorsal view. A–F, H, I, after McIntosh (1915); G, after Buchanan (1890). Abbreviations: anC, anal cirrus; br, branchiae; car, caruncle; pa, palp; per, peristomium; pr, prostomium.

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 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.2: Examples of Spionidae, entire worms and parapodia. A, Scolelepis squamata; B, Polydora ciliata; C, Laonice antarcticae, chaetiger 5, anterior view; D, Prionospio fauchaldi, chaetiger 21, anterior view; E–F, Prionospio orensanzi: E, chaetiger 5, anterior view; F, chaetiger 7, anterior view. A, B, after McIntosh (1915); C, E, F, after Blake (1983); D, after Maciolek (1985). Abbreviations: br, branchiae; dCr, dorsal crest; neL, neuropodial lamella; noL, notopodial lamella; pa, palp; per, peristomium; pr, prostomium; pyg, pygidium.



ventral epidermal glands of Spio and Microspio stand out by being intraepidermal, meaning they are strictly limited to the epidermal layer and by their position away from the parapodia, whereas other multicellular epidermal glands of Spionidae are located subepidermally, and are usually associated with the parapodia. Glandular pouches are comprised of epidermal glandular cells grouped together in a single envelope, and hence are multicellular epidermal glands. Individual cells are grouped into an array of cells with large and rounded expanded ends that then taper to a thin point where several arise (Fig.  7.4.1.6  C). The entire structure containing the individual cells is the glandular pouch. The term “glandular pouch” or segmental mucus gland is commonly but not exclusively used for glands present in the Polydora complex (e.g., Dorsett 1961a,b). These glands secrete acid mucopolysaccharides that are believed to play a role in tube building and boring into calcareous structures. Much of the early literature associated with boring was reviewed by Blake and Evans (1973). Details of the potential role of these glands in boring are presented in the tube-building section later in this chapter. The parapodial glandular organs (PGO) present in all Spiophanes are an excellent example of highly derived compound multicellular glands. They were first described by Claparède (1870) as “organes trop exceptionnels” in his original description of Spiophanes bombyx. These organs are of conspicuous size, and they bulge deeply below the epidermis invading the coelomic sac. The PGOs are directly associated with the parapodia of the middle body region, comprising chaetigers 5 to 14 or 5 to 15. Large PGOs, usually present in chaetigers 5 to 7 (rarely 5–8), display different species-specific types of openings termed “chaetal spreaders” (Fig.  7.4.1.4  C, D) whereas small PGOs, present from chaetiger 9, always open in a simple vertical slit (Meißner and Hutchings 2003; Meißner 2005; Radashevsky 2012). Meißner et al. (2012) conducted a detailed study regarding the functional anatomy and ultrastructure of PGOs in Spiophanes together with a three-dimensional reconstruction based on semi-thin section series. The authors distinguished three main complexes: (1) a glandular sac with several distinct epithelia of secretory cells and secretory cell complexes and a reservoir filled with fibrous material, (2) a gland-associated chaetal complex, and (3) a bilayered musculature surrounding the gland. It was determined that both large and small PGOs have the same general composition, but that small PGOs lack the “chaetal spreader”, which is part of the gland-associated chaetal complex in large PGOs. Very fine gland-associated chaetae (called “bacillary chaetae”

7.4.1 Spionidae Grube, 1850 

 5

in the taxonomic literature) emerge from inside the PGOs guided by the “chaetal spreader”. It was documented that these chaetae are typical annelid chaetae formed by chaetoblasts and follicle cells (Meißner et al. 2012). Among the different cell types involved in secretory activity, guidance of the gland-associated chaetae, and final expulsion of the fibrous secretion in PGOs, the secretory cells with cup-shaped microvilli located in the proximal glandular complex are the most interesting from a phylogenetic perspective (for additional information and an extended discussion on this subject, see, e.g., Southward et al. 2005; Meißner et al. 2012; Guggolz et al. 2015; Müller et al. 2015). It has been shown that b-chitin is produced by the secretory cells with cup-shaped microvilli in both the pyriform glands of Siboglinidae and the PGOs of Spiophanes, and is used for tube-building (Shillito et al. 1995; Guggolz et al. 2015). The term “ventral pores”, sometimes used in the literature, refers to the presence of small openings on the venter on several anterior and middle segments in Spio and Microspio. They are easily detected in well-preserved specimens using scanning electron microscope (SEM) or in live specimens, and also become apparent after methyl green staining as white dots against the surrounding blue-stained tissue or in a blue ring-shaped pattern (Fig. 7.4.1.3 H). The ventral pores are openings of ventral epidermal glands, which are supposedly involved in tube construction. The ventral epidermal glands were studied in detail and three-dimensionally reconstructed based on semi-thin section series by Rößger et al. (2015). Acinar and tubular ventral epidermal glands were found and the authors suggested that the acinar type stains in a ringshaped pattern, whereas the tubular type becomes apparent as a white dot. This hypothesis still needs support from additional data. Nonetheless, information on the types and distribution patterns of the ventral epidermal glands along the body is of taxonomic significance at the species level (see Maciolek 1990; Bick and Meißner 2011; Meißner et al. 2011; Meißner and Götting 2015). Rows of dorsal holes or openings have been observed on the branchiate region of Aonidella cf. dayi (Meißner et al. 2014). These are only observed with SEM and their function is unknown. Some, however, are observed with cilia protruding from their openings, suggesting a sensory function (see Fig. 7.4.1.13 C, D in the taxonomic section). Bacillary glands are elongate striated cells that occur on the dorsum and on the pygidium of some spionid larvae (Hannerz 1956) and adults. The tips of these cells protrude through the cuticle and are collectively called bacillary glands. Groups of bacillary glands occur on the dorsal surface of some segments in species of Amphipolydora

6 

 7.4 Sedentaria: Sabellida/Spionida



(see Fig.  7.4.1.31  A in the taxonomic section; Blake 1983; Paterson and Gibson 2003). Head. The prostomium is longer than wide and overlies the peristomium; it is narrow and more or less wedge-shaped, with an anterior end that may be entire (Figs.  7.4.1.1  E, I; 7.4.1.3  D), incised, or bilobed (Fig.  7.4.1.2  B); rounded (Figs.  7.4.1.1  I; 7.4.1.3  J), pointed (Figs.  7.4.1.1  H; 7.4.1.2  A), or expanded laterally into prominent frontal horns (Figs. 7.4.1.1 A, B; 7.4.1.3 A–D). It is typically widest in the middle where eyespots are present and narrows as it continues posteriorly as a caruncle over one or more anterior chaetigers (Fig. 7.4.1.3 D). The caruncle may bear an occipital antenna (sometimes called a nuchal tentacle), which is usually a single short digitiform projection that appears at about the level of the palps. The presence or absence of an occipital antenna is an important taxonomic character. Polydora bioccipitalis has two such antennae on the caruncle (Blake and Woodwick 1972). In Streblospio, a similar structure is separate from the prostomium but it is uncertain whether this is homologous to the antenna found in other spionids (Dauer 1984; Dauer et al. 2003). Prostomial eyes may be present (Fig. 7.4.1.1 E, F, H, I) or absent. These may be black or red. Comparatively small they are usually refered to as eyespots. In spionid larvae, there are typically one or two pairs of larger lateral eyespots and a single pair of medial eyespots. These usually persist in adults in more or less the same arrangement, but are dependent on the final form of the prostomium. In some instances, larval eyespots merge into a single one in adults; in other cases, additional eyespots develop in adults. Fixation may alter the color of eyespots from black to red as they fade in preservative. The eyespots have been described in Scolelepis squamata as consisting of only two cells each, a pigment cell and rhabdomeric receptor cell (Rhode 1991). Prostomial papillae have been described in species of Paraprionospio (Ehlers 1901; Dauer 1985), Marenzelle­ ria (Verrill 1873; Dauer 1997), Prionospio (Maciolek 1985, as prostomial “peaks”), and Streblospio (Dauer et al. 2003). These papillae are eversible and may be sensory in nature with a role in selecting or rejecting sediment

7.4.1 Spionidae Grube, 1850 

 7

particles (Dauer 1997; Dauer et al. 2003). They may be randomly scattered over the prostomial surface or confined to certain locations, and they may be smooth or irregular in appearance. Although considered to be of taxonomic value, the eversible nature of the structure results in some difficulty in ascertaining patterns after fixation. Nuchal cilia are developed to varying degrees lateral to the caruncle. These first appear in larval stages as rounded to oval-shaped ciliary patches. In adults, they appear as paired longitudinal bands of cilia on either side of the caruncle, but also appear in spionids such as Spiophanes that lack a caruncle (Fig.  7.4.1.3  B). Nuchal organs vary considerably in size and appearance. They may be short, extending only as far as the end of the caruncle, or may continue posteriorly along the body for many segments. These elongate nuchal organs may occur as a continuous pair along the dorsum or may be interrupted segmentally; they may be straight, curved, or diagonal. Their ultrastructure has been investigated in Pygospio elegans by Schlötzer-Schrehardt (1986, 1987) and in a number of additional species by Jelsing (2002, 2003) and Jelsing and Eibye-Jacobsen (2010). The segmental continuation of the nuchal ciliation is often accompanied by transverse ciliary bands (Fig.  7.4.1.3  C, G, I, J), which are likely derived from the larval nototrochs. In addition, other ciliary bands may form longitudinal groups along the body (Fig. 7.4.1.3 C, G, I). These various types of segmental or metameric ciliary bands were termed “dorsale Sinnesorgane” by Söderström (1920). The arrangement and organization of these dorsal sense organs with or without accompanying nuchal cilia are highly diagnostic and important taxonomic characters. The peristomium is achaetous and surrounds the mouth ventrally and the prostomium dorsally, and often forms a pair of lateral lobes that in some species of Priono­ spio, Paraprionospio, and Streblospio are enlarged to form erect, membranous wings. In Streblospio, the peristomium extends anteroventrally to encompass the mouth and laterally forms a transverse hood that surrounds the bases of the palps dorsally (Dauer 1984; Dauer et al. 2003); in Paraprionospio, this hood continues dorsally, forming wings that encompass and cover part of the prostomium.

◂ Fig. 7.4.1.3: Spionidae parapodia and chaetae. A, Paraprionospio sp. (Gulf of Mexico), chaetiger 4, parapodium, anterior view; B, Spiophanes cf. bombyx (Massachusetts Bay), chaetiger 7, right lateral view; C, Spiophanes duplex, chaetal spreader; D, Spiophanes berkeleyorum, chaetal spreader; E, Paraprionospio sp. (Gulf of Mexico), midbody neuropodial hooded hooks and capillaries; F, Spiophanes cf. bombyx (Massachusetts Bay), neuropodial hooded hooks; G, H, Streblospio benedicti (California), neuropodial hooded hooks; I, Dipolydora commensalis, major spines from chaetiger 5; J, Polydora cornuta, major spine and companion chaeta from chaetiger 5; K, Dipolydora blakei, major spine from chaetiger 5; L, Dipolydora commensalis, neuropodial hooded hook; M, Tripolydora spinosa, neuropodial hooded hook; N, Dipolydora giardi, major spines and companion chaetae from chaetiger 5; O, Boccardia berkeleyorum, major spines from chaetiger 5; P, Dipolydora quadrilobata, major spines from chaetiger 5. A, B, E–J, L, O, P, originals; C, D, after Meißner and Hutchings (2003); K, after Maciolek (1984a); M, after Blake and Woodwick (1981); N, after Blake (1981). Abbreviations: neP, neuropodium; noP, notopodium.

8 

 7.4 Sedentaria: Sabellida/Spionida

In both Paraprionospio and Streblospio, the peristomium and first segment are entirely fused ventrolaterally. This segment has chaetae that are lost during metamorphosis from the larval form to the adult. In contrast, adults of Pri­ onospio retain chaetae on segment 1, which is not fused or only partially fused to the peristomium. The paired palps arise dorsolaterally at the posterior end of the peristomium in all spionids (Figs. 7.4.1.1 A–C, F, G, H; 7.4.1.2 A, B; 7.4.1.3 G, I). The palps are elongate prehensile organs that are actively used to collect particles from either the water column or sediment surface; they are used in tube construction and/or feeding (Dorsett 1961a). A ciliated ventral groove acts as a channel to carry particles to the mouth where they are either ingested or manipulated and placed on tubes. Species of Scolelepis lack grooves on their palps and captured particles are carried to the everted proboscis by contraction of the palp into a coil (Dauer 1983). Polydora commensalis lives in shells occupied by hermit crabs and its palps appear unusually short compared with other spionids. The worms extend their palps to retrieve food particles brought in by the crab. Dualan and Williams (2011) determined that palp length was negatively influenced by the hermit crab host, which can cut or damage them during its movements. Worms experimentally removed from the shells developed palps that were of a length typical for other species of Polydora. Lindsay and Woodin (1992) investigated the effect of palp loss on feeding behavior and exposure to predation for two infaunal species: Rhynchospio glutaea and Pseu­ dopolydora kempi, both of which extend their palps from tubes to feed. Additionally, R. glutaea extends several anterior segments during feeding whereas P. kempi does not. Therefore, loss of feeding palps resulted in a greater exposure to predation for R. glutaea than P. kempi. Palp loss also reduces the potential area that the worms can access during feeding because the feeding area is a circle around the tube opening. Without palps, this area was reduced by 90% for R. glutaea and by nearly 100% in P. kempi (Lindsay and Woodin 1992). Worsaae (2001, 2003) and Williams (2007) suggested that palp morphology was of taxonomic significance within the genera Dipolydora, Polydora, Prionospio, and Scolelepis. The morphology of palp cilia and their arrangement are complex and differ among spionid genera, but are generally similar among species of individual genera (Dauer 1987; Worsaae 2001). According to Worsaae (2003: 259), 13 palp characters are present in 10 genera of Spionidae: (1) motile frontal cilia, (2) nonmotile cilia, (3) basal transverse cilia, (4) lateral cilia, (5) latero-frontal cirri, (6) randomly scattered motile cirri, (7) randomly scattered nonmotile cilia, (8) nonmotile cirri on papillae, (9) ciliary

sensory organs, (10) mucus glands, (11) glandular holes, (12) single transverse ciliary bandlets, and (13) transverse ciliary bands. The two latter characters were identified by Worsaae (2003) for two species of Prionospio that, unlike related species, exhibit considerable morphological differences in palp morphology. Williams (2007) identified four distinct palp ciliation patterns in species of Scolelepis where palp morphology has been reported. Meißner and Götting (2015) found a notably elevated number of mucus-secreting cells compared to accompanying cilia on palps of Scolelepis inversa. To date, however, these diverse ciliary patterns have not been applied to phylogenetic analyses or used widely as taxonomic characters. In Paraprionospio, a basal sheath surrounds the base of the paired palps (Dauer 1985). A similar sheath is present in Scolelepis but it is typically fused with the palp and is difficult to discern. The edge of this sheath may be papillated in some species of Scolelepis (Blake 1996). Segmentation and parapodia. The parapodia of spionids are biramous and lack aciculae. Podial lobes are generally reduced but prechaetal and postchaetal lamellae may be developed to varying degrees (Figs.  7.4.1.2  C–F; 7.4.1.4  A, B); these decrease in size and complexity posteriorly. In some genera, such as Prionospio, transverse dorsal crests sometimes connect the parapodia (Fig. 7.4.1.2 F). Interramal membranes or pouches, also called genital pouches, may be present between successive parapodia in genera such as Laonice, Prionospio, and Spiophanes. Dorsal and ventral cirri are absent. Prechaetal lamellae are rare in spionids, whereas postchaetal lamellae occur in all genera. These lamellae are usually best developed in anterior segments (Fig. 7.4.1.2 C, D), becoming reduced and inconspicuous posteriorly. Prechaetal notopodial lamellae in some species of Pri­ onospio are merged with postchaetal lamellae to form a kind of hood from which the notochaetae emerge (Blake 1996). The shape or form of postchaetal lamellae varies, but is highly diagnostic in some genera and species. For example, in species of Laonice and Prionospio, the postchaetal lamellae are often large and foliaceous (Figs.  7.4.1.2  C–E; 7.4.1.4  A) and sometimes merge with dorsal crests to form a continuous membrane from one side to the other (Fig. 7.4.1.2 F). Dorsal crests extend across the dorsum of some species of Prionospio and Laonice and connect with the postchaetal notopodial lamellae (Fig.  7.4.1.2  F). These crests may be large and high, appearing membranous, or may be simple low elevations. Typically, dorsal crests are highest on the segment where they first appear, becoming lower and less prominent on following segments. Ventral crests are known only for Laubierellus and extend from the



ventral postchaetal lamellae (Maciolek 1981b; Erickson and Wilson 2018). The presence and form of these crests are of taxonomic significance. Membranous transverse dorsal ridges occur on chaetiger 1 in Paraprionospio, on chaetiger 2 in Streblospio, and on middle body chaetigers in some species of Spiophanes (Blake 1996). Ventrolateral interparapodial pouches are thin membranes that occur between adjacent neuropodia on either side of the body; these form pockets that open dorsally. They are best known in species of Laonice, but also occur in certain species of Prionospio (e.g., P. ehlersi), Aonidella, and Spiophanes. The first presence of these pouches and their extent along the body are taxonomic c­haracters. There are reports that these pouches, often called “genital pouches”, have a role in reproduction. Much of the information regarding this subject is anecdotal and not well supported; further study is needed to clarify their role. Similarly, dorsal interparapodial membranes that form pockets that open ventrally have been reported for Prio­ nospio steenstrupi (Sigvaldadóttir and Mackie 1993) and are known to occur in at least one other undescribed species of Prionospio (Maciolek unpublished). Sigvaldadóttir and Mackie (1993) note that the dorsal folds in P. steenstrupi are not as well developed as the ventrolateral pouches of other species; their function is also unknown. Chaetae. Spionid chaetae are all simple and include smooth and winged (limbate) capillaries, hooded and nonhooded hooks with one to several teeth, and curved inferior sabre chaetae in some neuropodia. Modified spines of various types, some with a bristled apex, occur in the fifth chaetiger of Polydora and related genera (Fig. 7.4.1.4 I–K, N–P). A recurved crooklike chaeta occurs in the first chaetiger of Spiophanes species; modified posterior notopodial spines, needles, or recurved spines occur in species of Microspio, Polydora, and Boccardia. Unusual spoonlike neurochaetae occur in some chaetigers instead of hooded hooks in species of Pygospio. The distribution and morphology of these numerous chaetal types are of major taxonomic significance for genera and species of Spionidae and will be discussed in the taxonomic section. The arrangement of noto- and neurochaetae in spionid parapodia was originally described by Mesnil (1896) and updated and refined by Radashevsky and Fauchald (2000) and Radashevsky (2012). The basic patterns are (1) anterior notochaetae include two rows of capillaries and a dorsal superior tuft; (2) anterior neurochaetae include two rows of capillaries and a ventral tuft; (3) posterior notochaetae are reduced in number, with rows or groups becoming indistinct; and (4) posterior neurochaetae include the replacement of capillaries by hooded hooks and the presence or absence of an inferior sabre chaeta.

7.4.1 Spionidae Grube, 1850 

 9

Within these basic patterns are many modifications, additions, and subtractions. For example, (1) Spiophanes species have long, thin capillaries in anterior notopodia and crooklike spines in the neuropodia of chaetiger 1; (2) species of Lindaspio have groups of up to 10 large heavy spines in the notopodia of chaetigers 2 to 4; (3) acicular spines of different types occur in the posterior notopodia of several of the polydorid species and other genera; these may be rosettes of awl-shaped spines, bundles of needles, or strongly curved boat hooks; (4) all of the polydorids have a modified chaetiger 5 typically with one or two rows of modified chaetae of different types; a dorsal tuft of capillaries is usually present as well as a tuft of ventral neurochaetae. The modified spines of polydorids include curved falcate spines with or without apical teeth or flanges (Fig.  7.4.1.4  I, J, N). Some spines have an expanded apex covered with a cloak of fine bristles (Fig. 7.4.1.4 K, O, P). Hooded hooks or crotchets. The presence of hooded hooks in the neuropodia is a characteristic feature of Spionidae. Rarely, hooks are also present in the notopodia, but never in notopodia only. The number of teeth or dentition of the hooks is an important taxonomic character. There is typically a large main fang surmounted by one, two, three, or more apical teeth (Fig. 7.4.1.4 E–H, L, M). Apical teeth are typically in sequential pairs that, when numerous, are difficult to count, as in the multidentate hooks of species of Prionospio. Hooks of Spiophanes are usually quadridentate with one single apical tooth surmounted by two smaller teeth (Fig. 7.4.1.4 F). Unhooded neuropodial hooks of Pygospiopsis species are curved spines with or without a subapical tooth or cusp on the concave side and may have a bristled apex and no hood (Blake 1983, 1996; Blake and Maciolek 2018). The hood that covers most spionid hooks is thin and transparent in light microscopy and is termed an outer hood; the dentition of the teeth is readily visible. With SEM, apart from a narrow opening in the hood from which the main fang projects, the smaller apical teeth are often not fully visible (Fig. 7.4.1.4 E, L). Species of Priono­ spio and Paraprionospio have a separate secondary hood that covers the subdistal part of the hook. Secondary hoods also occur in some species of Spiophanes; many species of Spiophanes have half-hoods that extend from the tip of the main fang to the shaft (Fig. 7.4.1.4 F), but do not cover the apex of the chaeta and some species lack a hood entirely. P. elegans has a unique hooded hook with a spoonlike distal end in addition to more typical bidentate hooks (Light 1978). Branchiae. Dorsal paired branchiae occur along the body of most spionids (Fig. 7.4.1.1 B, F); these are either entirely

10 

 7.4 Sedentaria: Sabellida/Spionida



separate from the postchaetal lamellae (Figs. 7.4.1.2 C, E; 7.4.1.3 D, J), or fused with them to varying degrees. Ventral branchiae that originate below the neuropodia as well as dorsal branchiae have been reported for Lindaspio (Blake and Maciolek 1992). A separate kind of branchia, often called a lateral or accessory branchia, is palmately branched and arises directly from the body wall posterior to the dorsal lamellae in species of Dispio. Dorsal branchiae of most spionids are typically smooth, ciliated, and either flat and straplike or thin and tapered. Those without lateral appendages are considered to be simple branchiae and are termed apinnate (Figs.  7.4.1.2  C; 7.4.1.3  A, J). When lateral pinnules are present, the branchiae are termed pinnate; the pinnules may be either digitiform, which are cylindrical (Figs.  7.4.1.2  E; 7.4.1.3  D, E), or platelike, which are flattened and stacked (Fig.  7.4.1.3  F). Pinnate branchiae are characteristic of some species of Prionospio; platelike branchiae occur in species of Apoprionospio and Para­ prionospio. In some species of Prionospio, both apinnate and pinnate branchiae occur together in various combinations that are of taxonomic significance. In Apopriono­ spio, anterior apinnate branchiae are followed by a pair of platelike branchiae, whereas Paraprionospio species have only platelike branchiae. An additional form of branchia was described by Maciolek (1985) for two species of deepsea Prionospio. These branchiae were neither smooth nor pinnate, so were best described as “wrinkled;” however, the taxonomic value of this form is unclear. Dorsal branchiae are relatively flat structures typically oriented parallel with the dorsal surface and directed at the branchia on the opposite side (Figs. 7.4.1.1 B, F; 7.4.1.2 A, B; 7.4.1.3  A, I, J). In some instances where branchiae are long, a pair will meet or overlap at the dorsal midline. In several genera, such as Malacoceros and Scolelepis, the branchiae are fused to the dorsal postchaetal lamellae to varying degrees. The two small pairs of branchiae on Aurospio dibranchiata are fused basally to the dorsal lamellae of chaetigers 3 to 4 (Maciolek 1981a). In contrast, the branchiae of Prionospio species are generally free from the dorsal lamellae. This distinction has not been recognized by recent authors and a few species of Prionospio may have been erroneously referred to Aurospio (Sigvaldadóttir 2002; Mincks et al. 2009; Patterson et al. 2016).

7.4.1 Spionidae Grube, 1850 

 11

On most spionids, branchiae are added continuously along the body with growth and with the addition of new segments. In species with a fixed number of branchiae as in some species of Prionospio, Laonice, Aurospio, Aonides, and some polydorids, branchiae will be added as juveniles develop up to the point where the adult arrangement is attained. In these instances, branchiae are limited to a few anterior segments. In late planktic larvae of the polydorid genera Boccardia and Boccardiella, branchiae develop on chaetiger 7 and subsequent segments; the development of branchiae on anterior chaetigers 2 to 4 and 6 is delayed until postlarval development (Rullier 1960; Dean and Blake 1966; Woodwick 1977; Blake and Kudenov 1981). However, as part of a recent study on the development of Boccardia berkeleyorum, branchiae both anterior and posterior to chaetiger 5 were already developed in late planktic larvae (Blake 2017). Branchiae of P. dubia occur on chaetigers 2 to 3 and 7 to about chaetiger 16; branchiae of chaetigers 2 to 3 are free from the dorsal lamellae, whereas those from chaetiger 7 are basally fused to the notopodial lamellae (Blake 1983). In species of Pygospio, branchiae are fused to the notopodial lamellae and occur from chaetiger 10 or posterior (Fig.  7.4.1.1  F). However, males may have a separate pair of branchiae on chaetiger 2 that is not fused to dorsal lamellae (Fig. 7.4.1.1 F). Pygidium. The pygidial segment takes on several distinctive forms in spionids, including the presence of additional accessory lobes, cirri, cushions, discs, collars, and combinations of these forms. The number and length of anal cirri are of taxonomic significance, but they are often lost or damaged in preservation. In Prionospio species, there are typically three anal cirri, one long and dorsal, two short and ventral. Spiophanes species have a pair of cirri arising from a small ventral lobe, or up to 11 cirri in dorsal or lateral position. Four anal cirri, two dorsal and two ventral, are typical for Microspio, Pygos­ pio, and Spio. Species of Aonides, Malacoceros, Marenzel­ leria, and Rhynchospio may have anywhere from 5 to 15 or more anal cirri (Fig. 7.4.1.1 B). However, these numbers are likely age dependent, with fewer cirri in juveniles. Species of Scolelepis have a cushionlike pygidium with thick, fleshy, and rounded pads surrounding the anal opening.

◂ Fig. 7.4.1.4: Spionidae external morphology. A, Malacoceros jennicus, anterior end, dorsal view; B, C, Spiophanes bombyx (SEM): B, anterior end, dorsal view; C, middle body segments, dorsal view; D, E, Prionospio cf. steenstrupi: D, anterior end, dorsal view; E, pinnate branchia; F, Apoprionospio pygmaea, platelike branchia; G, Spio filicornis, anterior end, dorsal view; H, Spio arndti, anterior end, ventral view; I, J, Spio blakei: I, anterior end, dorsal view from life; J, anterior end, SEM. A, after Graff et al. (2008); B, C, after Meißner and Blank (2009); D–F, originals; G, H, after Meißner et al. (2011); I, J, after Meißner and Götting (2015). Abbreviations: br, branchiae; car, caruncle; dcb, dorsal ciliary band; nuO, nuchal organ; pa, palp; per, peristomium; pr, prostomium; tcb, transverse ciliary band.

12 

 7.4 Sedentaria: Sabellida/Spionida

The polydorids exhibit a wide range of pygidial morphologies. Boccardiella species have a pair of rounded lobes bearing short cirri. Some Boccardia species have the anus surrounded by multiple lobes. Species of Dipolydora and Polydora often have the anal opening surrounded by a thin disclike structure that is either entire with a dorsal gap (Fig. 7.4.1.2 B) or divided into three or four partitions. The shape and size of these pygidia are of taxonomic significance. Pygidial lobes may also contain large reflective bacillary glands. Anatomy Musculature. The musculature of Spionids as described by Buchanan (1890) for Streblospio shrubsolii consists of a thin circular layer that is best developed in the ventral region just over the nerve cord and can be seen in transverse thin sections (Fig.  7.4.1.5  C). Longitudinal muscles are well developed with one dorsal and two ventral bands. A delicate layer of coelomic epithelium, forming the outer wall of the coelom and consisting of a few nuclei on the extremities of the muscle fibers, occurs below and above the dorsal and ventral longitudinal muscles, respectively. Dorsoventral muscles divide the dorsal longitudinal muscles on either side, and vertically become attached close to the thickened portion of the ventral epidermis. Dorsoventral muscles divide the cavity of each of these segments more or less completely into three longitudinal chambers. In addition, there are segmental muscles along the ventral body wall on each side to the corresponding two chaetal bundles. Digestive system. The digestive system of spionids consists of a pharynx and a simple intestinal track consisting of a short foregut or esophagus followed by a hindgut (Fig.  7.4.1.5  A). The pharynx is unarmed, and is either a soft, ciliated, or slightly eversible axial proboscis as in Streblospio and Scolelepis (Buchanan 1890; Dales 1962) or a muscular ventral pharyngeal organ with a mouth that opens into a pharynx with dorsolateral folds and muscular ventral pharyngeal organ as in Prionospio cirrifera (Purschke and Tzetlin 1996). Orrhage (1964) had earlier reported a simple ventral buccal organ in Prionospio and Spiophanes. The intestine is lined by ciliated columnar cells and may have lobes or folds that presumably increase surface area (Figs.  7.4.1.5  A; 7.4.1.6  B). In some species, the intestine has been found to be infested with gregarine parasites that are attached to the cellular lining (Fig. 7.4.1.6 B). As part of a study of five spionid species, Penry and Jumars (1990) determined that they all belonged to a group of deposit feeders having simple ciliated tubular

guts consisting of a short foregut and a longer hindgut. In some species of Carazziella, Dipolydora, and Spio­ phanes, there is a muscular gizzardlike structure on the posterior part of the foregut (Blake 1969, 1971, 1979a; Radashevsky 1993; Meißner 2005). In Carazziella species where a gizzard occurs, there are four symmetrically arranged muscles that encircle the gizzard and presumably crush or otherwise treat the incoming food particles (Fig. 7.4.1.6 E) (Blake 1979a). In D. socialis, there are four embedded chitinous plates, teeth, or inclusions that are associated with the muscles (Fig. 7.4.1.6 A, D) (Blake 1969, 1971) and that presumably assist in the same function. Gizzardlike structures are also present in other spionids such as Paraprionospio and Spiophanes, but these are entirely muscular (Radashevsky 2012). Excretory system and nephridia. Both protonephridia and metanephridia are described for Spionidae (Bartolomaeus and Quast 2005). Protonephridia generally develop first and are found in the anterior chaetigers of larvae. In adults, paired metanephridia or segmental organs occur throughout the body (Figs. 7.4.1.5 A; 7.4.1.7  A–C). The metanephridial system functions both for filtration by special cells termed podocytes and in reproduction with gonoducts. A nephrostome or ciliated funnel serves as an entrance to a ciliated nephridial canal (Fig.  7.4.1.7  A) through which gametes are transported to a nephridiopore from which they are released or spawned (Söderström 1920; Rice and Reish 1976). Details of the role of nephridia in the reproduction of spionids in presented in the following section. Blood vascular system. A closed circulatory system with dorsal and ventral vessels connected by lateral vessels with capillaries is present in most spionids. Buchanan (1890) described the anatomy and function of the circulation in Streblospio shrubsolii. Blood flows anteriorly in the dorsal vessel and posteriorly in the ventral vessel. The dorsal and ventral vessels connect to blood loops in the palps and branchiae where blood is oxygenated; the ventral vessel connects to sinuses that run along most of the intestine (Fig.  7.4.1.5  A). Buchanan (1890) also identified a heart body as being present in Streblospio; this has been confirmed by Radashevsky (2012) in the closely related Prionospio, but not in other genera. Blood is red in color due to the respiratory pigment erythrocruorin; however, there are no erythrocytes. Nervous system and sensory organs. The nervous system of several spionids was well described by Orrhage (1964) and more recently reviewed by Orrhage and Müller (2005).



7.4.1 Spionidae Grube, 1850 

 13

Fig. 7.4.1.5: Spionidae internal morphology. A, Streblospio shrubsolii, circulatory system, nephridium, intestine; B, Scolelepis spp., diagram of nervous system; C, Boccardiella hamata (California), cross-section of middle body segment with muscles, intestine, ventral nerve cord, and glandular pouch. A, after Buchanan (1890); B, modified after Orrhage (1964); C, original. Abbreviations: A, an, anus; blSin, blood sinus; br, branchia; coel, coelom; dBrv, dorsal branchial vessel; dBv, dorsal blood vessel; int, intestine; neph, nephridium; pa, palp; ph, pharynx; vBrv, ventral branchial vessel; vBv, ventral blood vessel. B, dcvr, dorsal commissure of the ventral root; dcdr, dorsal commissure of the dorsal root; dG, dorsal ganglion of dorsal nerves; dn, dorsal nerves; drcc, posterior (dorsal) root (drcc); neN, neuropodial nerves; noN, notopodial nerves; nuN, nuchal nerves; Oen, esophageal nerve; Palp nerves (numbered: 1, 2, 4, 5, 6, 7); prN, prostomial; vcdr, ventral commissure of the dorsal root; vcvr, ventral commissure of the ventral root; vnc, ventral nerve cords; vrcc, anterior (ventral) circumesophageal root. C, gP, glandular pouch; lMus, longitudinal muscles; int, intestine; vnC, ventral nerve cord.

14 

 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.6: Spionidae internal morphology. A, Dipolydora socialis, juvenile, digestive tract with gizzard; B, Boccardiella hamata, crosssection of middle body with intestine infested with gregarine parasites; C, Polydora cornuta, sagittal section showing large glandular pouch; D, Dipolydora socialis, gizzard of adult; E, Carazziella hobsonae, gizzard. A–C, originals; D, after Blake (1971); E, after Blake (1979). Abbreviations: eso, esophagus; gP, glandular pouch; giz, gizzard; mus, muscle; int, intestine.

The example shown in Fig.  7.4.1.5  B for S. squamata (as Nerine cirratulus) is modified and updated from Orrhage (1964). The brain or supraesophageal ganglion of spionids, like that of many polychaetes, consists of four transverse commissures: dorsal commissure of the ventral root (dcvr); ventral commissure of the ventral root (vcvr); dorsal commissure of the dorsal root (dcdr); and ventral commissure of the dorsal root (vcdr) (Fig. 7.4.1.5 B). Two of these

(dorsal and ventral) connect with an anterior (ventral) circumesophageal root (vrcc); the other two connect to a posterior (dorsal) root (drcc). Prostomial nerves arise directly from the dcvr; esophageal nerves arise from vcvr. Palp nerves (1, 2, 4, 5, 6, 7) arise from both the vrcc and drcc (Fig. 7.4.1.5 B). Dorsal nerves arise from the dcdr whereas the nuchal nerves arise from both the dcdr and vcdr or the posterior brain. The drcc and vrcc on each side form

▸ Fig. 7.4.1.7: Spionidae reproductive morphology. A, B, Polydora cornuta (California), sagittal section of female with ovaries and nephridia; C, D, Boccardiella hamata (California): C, cross-section of female with ovary and nephridia; D, detail of nephridiopore; E, F, P. cornuta (California), female with seminal receptacle and spermatophores; G, B. hamata (California), cross-section of male with sperm masses; H, Spio setosa (Maine), mature sperm with spiral nucleus; I, Dipolydora concharum (Maine), egg capsules in burrows in shells of Placopecten magellanicus; J, Boccardia proboscidea (California), egg capsules with larvae and nurse eggs; K, Polydora quadrilobata (Maine), detail of egg capsule with nurse eggs and larvae. All originals. Abbreviations: gP, glandular pouch; neph, nephridium.



7.4.1 Spionidae Grube, 1850 

 15

16 

 7.4 Sedentaria: Sabellida/Spionida

the circumeophageal connectives which continue as the ventral nerve cord (Fig. 7.4.1.5 B, C) that extends along the body, giving off branches to each segment with additional branches to the noto- and neuropodia. The overall morphology of the spionid nervous system is most similar to that of Trochochaeta and Poecilochae­ tus (Orrhage 1964). Among spionids, Orrhage (1964) provided descriptions of six species of Scolelepis (as Nerine and Nerinides), Spio, Laonice, Spiophanes, and Prionospio. The overall arrangement of the nerves as described for the example in Fig. 7.4.1.5 B is nearly identical with that of the other spionids described by Orrhage (1964). Reproductive organs and gametes. All spionids have paired ovaries. However, there are two patterns of ovary structure and oogenesis: intraovarian and extraovarian (Eckelbarger 1983, 1988, 1992). In species with intraovarian oogenesis, a single pair of ovaries is located in each segment, associated with nephridial blood vessels and covered by a thin layer of peritoneal cells. Oocytes are retained in the ovary and derive nutrition from associated blood vessels. Intraovarian oogenesis has been described for Streblospio benedicti, Marenzellaria viridis and Spi­ ophanes uschakowi (Eckelbarger 1980, Bochert 1996a, Radashevsky et al. 2018). In species with extraovarian oogenesis, the paired ovaries are attached to muscles near the ventral midline (Fig. 7.4.1.7 A, B); oocytes are released into the coelom where they continue to develop in association with coelomocytes (Fig.  7.4.1.7  B). This pattern of gamete production and spawning was described by Dorsett (1961a) for Polydora ciliata and by Blake (2006) for Polydora cornuta. The gonads of P. ciliata and P. cornuta arise from the medial border of the ventral longitudinal muscle in a few anterior chaetigers. The ovaries appear as pairs of club-shaped sacs that project into the coelom (Fig.  7.4.1.7  A–C). In P. ciliata, the oocytes remain in the ovaries until they reach a diameter of 25 to 30 µm, at which time they are released into the coelomic cavity; this pattern seems to be the same for P. cornuta (Fig. 7.4.1.7 B). After release from the ovaries, oocytes move toward middle body segments where they accumulate in the parapodia and continue to grow and mature to a maximal size of approximately 130  µm (Dorsett 1961a). At the time of spawning, mature eggs are transported through nephridial canals to the nephridiopores where they are released into egg capsules as they are formed. At the same time, sperm that are stored in seminal receptacles are also released into the capsules. The same pattern was observed for Boccardia proboscidea by Woodwick (1977). Two different types of vitellogenesis have been reported in spionids (Eckelbarger 1992). S. benedicti has intraovarian oogenesis and accumulates yolk outside the

oocyte by a process termed heterosynthesis. In P. cornuta, which has extraovarian oogenesis, yolk is produced by the oocyte, a process called autosynthesis (Eckelbarger 1992). Three different types of eggs have been reported in spionids (Blake and Arnofsky 1999; Blake 2006): (1) eggs with thick, highly ornamented egg envelopes (= membranes) that are honeycombed externally (Fig. 7.4.1.8 J) and may contain prominent and numerous cortical alveoli (= ­membrane vesicles) (Fig. 7.4.1.8 I); (2) eggs with thick egg envelopes formed of several layers that have a reticulated, but not honeycombed surface and lack cortical alveoli; and (3) eggs with thin envelopes consisting of a single layer that is never ornamented and lacks cortical alveoli (Fig.  7.4.1.8  K). The first type of egg occurs in the genera Aonidella, Aonides, Dispio, Laonice, Lindaspio, Malaco­ ceros, Marenzelleria, Parascolelepis, Rhynchospio (in part), Scolelepis, Scolecolepides, and Spiophanes (Fig.  7.4.1.8  I,  J). The second egg type occurs in the Prionospio complex, including Streblospio, which has a three-layered egg envelope and seems to be intermediate between the highly ornamented types and those with thin, single-layered egg envelopes (Blake 2006). The third egg type occurs in Microspio, the Polydora complex, Pygospio, Pygospiopsis, Rhynchospio (in part), and Spio (Figs. 7.4.1.7 B; 7.4.1.8 K). Detailed observations of the ultrastructure of spionid eggs and oogenesis are available for five species: P. cornuta, Spio setosa, S. benedicti, M. viridis, and (Eckelbarger 1980, 1984, 1992, 1994; Bochert 1996a, Radashevsky et al. 2018). In optical sections using light microscopy, the honeycombed envelope of type 1 eggs appears to be perforated by pores that connect cytoplasmically to the cortical alveoli (George 1966; Blake 2006). The number of pores and alveoli varies among genera. The alveoli of eggs of Aonides and Dispio are few but large and arranged in two rows. In spionids having this type of egg, the cytoplasm concentrates in the center after fertilization (Hannerz 1956; George 1966; Blake and Arnofsky 1999; Blake 2006). Hannerz (1956) speculated that pores in the envelope allow water to enter and exert a constant pressure on the cytoplasm. As development of the embryo continues, the original egg envelope becomes incorporated into the larval cuticle. Cilia and chaetae protrude, probably through the pores. This process was demonstrated for M. viridis by George (1966). Bochert (1996a) described the ultrastructure of the thick honeycombed egg envelopes and large cortical alveoli of M. viridis. Ten to 18 large cortical alveoli or vesicles occur just below the surface and are connected cytoplasmically to pores in the envelope. The surficial honeycomb appearance is due to furrows that extend 4 µm below the surface of the egg envelope. Individual microvilli are single structures that become elongate and branch irregularly as oocyte development proceeds. The tips of the microvilli extend



7.4.1 Spionidae Grube, 1850 

 17

Fig. 7.4.1.8: Spionidae eggs and sperm. A, Malacoceros jennicus, mature sperm; B–E, Dipolydora concharum spermiogenesis: B, tetrad of four spermatids, C, early spermatid, D, late spermatid; E, mature sperm; F, Prionospio sp., ect-aquasperm; G, Marenzelleria viridis, ect-aquasperm; H, Tripolydora sp., introsperm; I, M. jennicus, mature egg with membrane vesicles; J, Scolelepis sp., mature egg with honeycombed membrane; K, Pygospio elegans, nurse eggs and oocyte. A, I, after Graff et al. (2008); B–E, after Blake (1996); F, H, after Rouse (1988) and Blake (2006); G, after Bochert (1996b); J, original; K, after Rasmussen (1973). Abbreviations: acr, acrosome; mC, mitochondria; mP, middle piece; nu, nucleus.

through the egg envelope where they terminate in spherical granules. According to Bochert (1996a), the high density of the microvillar tips (50–60 per µm2) increases the available surface area of the oocytes, suggesting that increased

surface area might facilitate movement of molecules across the membrane during development. Radashevsky (2018) described the newly released oocytes of Spiophanes uscha­ kowi as being flattened or lentiform.

18 

 7.4 Sedentaria: Sabellida/Spionida

The egg envelope (type 2) of S. benedicti consists of three layers having digitiform microvilli that bifurcate basally and lie nearly parallel to the surface (Eckelbarger 1980). The microvilli produce glycocalyx strands that form the outer layer of the egg envelope. The inner and middle layers of the egg envelope consist of filamentous, electron-dense material; cortical alveoli are absent. S. setosa and P. cornuta have thin, single-layered egg envelopes (type 3) with no cortical alveoli (Eckelbarger 1984, 1992, 1994). In S. setosa, the microvilli are elongate, thin, double V-shaped structures; whereas in P. cornuta, the individual microvilli are shorter, solitary, and bulbous structures. The tips of the microvilli project through the egg envelope and therefore are in direct contact with fluid in the coelomic cavity or fluid within egg capsules. The male reproductive system in spionids is best described for species of Polydora, Dipolydora, and Streblospio (Rice 1978, 1980, 1981). In Polydora, paired spermatogonia are suspended in the coelom between individual intersegmental septa and a nephridium. Each gonad is associated with an efferent parapodial blood vessel and surrounded by simple cuboidal cells (Rice 1981). Each gonad contains approximately 1000 spermatogonial cells. For the three polydorids studied by Rice (1981), gonads were first present in middle body segments. Spermatogonial cells of polydorids are released into the coelom in pairs connected by a cytoplasmic bridge (Rice 1981). The first meiotic division results in four secondary spermatocytes attached by cytoplasmic bridges. Following the second meiotic division, eight spermatids are formed, also connected by cytoplasmic bridges. Dense masses of sperm accumulate in the coelom (Fig. 7.4.1.7 G). Using light microscopy, Blake (1969) diagrammed spermiogenesis for several polydorids. An example for D. concharum is shown in Fig.  7.4.1.8  B–E where individual spermatogonia develop into mature introsperm. The morphological changes in the maturation of spermatids into mature sperm including the elaboration of the acrosome, nucleus, and middle piece are described by Rice (1981). In addition to the spermatogonia, sperm production, and maturation, the male reproductive system consists of a nephridium with a ciliated nephrostome or funnel that is located on the anterior border of intersegmental septa. In polydorids and some other genera, this leads through the septa to the nephridium and an elongated nephridial canal that terminates in a nephridiopore that opens on the dorsal surface (Rice 1978, 1981). In some spionids, sperm are concentrated into distinct spermatophores within the nephridial canal and these are in turn released from the nephridiopores where they are transferred in various manners to females. The biology of fertilization in spionids is further discussed in subsequent sections.

Retzius (1904) and Franzén (1956) defined two types of sperm: (1) primitive, referring to short-headed sperm (e.g., Fig. 7.4.1.8 A) that were spawned into seawater and (2) aberrant, referring to sperm that were modified and asso­ ciated with copulation or a modified form of sperm transfer. Primitive sperm were subsequently referred to as aquatic sperm (Baccetti 1979) and aquasperm (Jamieson 1986a,b). Rouse and Jamieson (1987) and Jamieson and Rouse (1989) refined these definitions and introduced the terms ect-aquasperm and ent-aquasperm for the primitive types. Ect-aquasperm are freely spawned into seawater where eggs are fertilized. Ent-aquasperm are released and swim in seawater but are drawn into the tube or burrow of the female by inhalant feeding currents. For the aberrant sperm, Rouse and Jamieson (1987) introduced the term introsperm. Both ect-aquasperm and introsperm are found among spionids. The morphology of spionid sperm has now been documented for more than 30 species (see table 2 in Blake and Arnofsky 1999). The ultrastructure of ect-aquasperm has been described for Prionospio cf. queenslandica (Fig.  7.4.1.8  F) by Rouse (1988), P.  japon­ ica by Radashevsky et al. (2010), Aonides oxycephala by Radashevsky et al. (2011), Marenzelleria neglecta (as M.  viridis) (Fig.  7.4.1.8  G) by Bochert (1996b), and Spio­ phanes uschakowi by Radashevsky (2018). The structure of spionid ect-aquasperm includes a spherical or ovoid nucleus, a midpiece consisting of four large, rounded mitochondria that surround two centrioles, and a free flagellum or tail (Rouse 1988; Bochert 1996b). The acrosome is typically a small, cylindrical structure that rests in a depression on the anterior end of the nucleus (see Fig.  7.4.1.8  F, G). Radashevsky et al. (2018) described the acrosome of S. uschakowi as being flattened and platelike. The reproductive biology and light microscopy investigations of the sperm of species of the genera Scolelepis, Aonides, Laonice, Malacoceros, Parascolelepis, and Spiophanes suggest that they also have ect-aquasperm. Introsperm are found in Microspio, Polydora, Dipo­ lydora, Pygospio, Spio, Streblospio, and some species of Rhynchospio. The morphology of introsperm includes modifications of the nucleus and midpiece. Mature sperm of polydorids have elongate heads (Fig. 7.4.1.8 H) and typically range from 59 to 74.5 µm long (Blake 1969, 2006). Sperm break away from aggregates of sperm plates when mature and lie free in the coelom. Ultrastructure details concerning spermatogenesis in Polydora and Tripolydora may be found in Rice (1981) and Rouse (1988). In Streblospio, the nucleus is long and the midpiece is short; the acrosome is long and spiral (Rice 1981). Membrane-bound electron-dense bodies are present throughout the nucleus and midpiece of polydorid sperm and the nucleus of Streblospio sperm (Rice 1981; Rouse



1988). Other modifications include a spiral or coiled nucleus (Fig. 7.4.1.7 H) in Spio setosa (Simon 1967; Eckelbarger and Hodgson 2014) and an unusually long nucleus and midpiece with an unusually short flagellum or tail in Boccardiella hamata (Blake 1965; Rice 1992). The introsperm of dwarf males of Scolelepis laonicola have an elongated nucleus and middle pieces (Vortsepneva et al. 2006, as Asetocalamyzas laonicola). Rice (1981) suggested that females of polydorids and S. benedicti should be able to store sperm for prolonged periods without loss of viability. Such an adaptation would be ecologically important for species that produce multiple broods within a single season (= polytelic).

Reproduction and development Reproduction Sexual reproduction. Spionid polychaetes either spawn their gametes directly into seawater or males transfer sperm, usually in spermatophores, to females, which store the sperm in seminal receptacles until fertilization and spawning, usually into egg capsules. This topic was reviewed by Blake (2006). Broadcast spawning is believed to occur in most of the genera referred to the subfamily Nerininae. These include the genera Paraprionospio, Prionospio, Dispio, Aonides, Aonidella, Lindaspio, Spiophanes, Rhynchospio, Scolecolepides, Malacoceros, Marenzelleria, Scolelepis, and Laonice. Unfortunately, there is little direct evidence that fertilization actually occurs in the water column. Available data were presented in Appendix 1 in Blake and Arnofsky (1999), but the authors noted that the absence of observations on spawning behavior in these genera is a major gap in an otherwise large and elaborate literature on reproduction and development. Based on that summary and more recent observations by Radashevsky (2007) and Radashevsky et al. (2014) on Rhynchospio, it would seem that three patterns of broadcast spawning occur: (1) dissemination of eggs and sperm into the water column where fertilized eggs develop freely into larvae; (2) discharge of eggs and sperm by paired males and females that result in an egg mass or cocoon within which fertilized eggs develop to a stage where they leave as planktic larvae; and (3) discharge of eggs and sperm into a dorsal posterior area on the abdomen, termed a “hatchery” by Radashevsky (2007) where gametes are discharged and held in place by long chaetae and where developing embryos and larvae are retained. Observations of eggs and larvae taken from the plankton in Northern California strongly suggest that ­Spiophanes bombyx, S. duplex, and Dispio uncinata spawn

7.4.1 Spionidae Grube, 1850 

 19

their gametes directly into seawater where development proceeds in its entirety (Blake 2006). This was confirmed by observing that early planktic stages for these species ranged from fertilized eggs through pretrochophores. Radashevsky et al. (2006) reported that for Prionospio patagonica, small oocytes of 82 to 92 µm were spawned directly into seawater. Planktic larvae of the same species from small two-chaetiger stages to five- to six-chaetiger larvae settled and underwent metamorphosis in the laboratory. George (1966) observed broadcast spawning in Marenzelleria viridis (as Scolecolepides) and suggested that spawning was stimulated by changes in salinity. Bochert and Bick (1995), however, concluded that spawning of M. viridis in the Baltic Sea was related to decreasing water temperature because high densities of fertilized eggs were observed when the temperature decreased to 15°C. Blake (2006) supported George’s (1966) observations based on high densities of M. viridis larvae in ­Penobscot Bay, Maine, USA where larvae were taken in plankton tows through lenses of low-salinity surface water. Larvae were rare or absent in deeper high-saline water. Simple postspawning cocoons or egg masses are formed by some species of Scolelepis (subgenus Paras­ colelepis). For example, Imajima (1959) observed simple external cocoons for Scolelepis yamaguchii (as Nerinides). Blake and Arnofsky (1999) and Blake (2006) reported the same structures for Scolelepis cf. tridentata in California. Both species produce elongate, club-shaped cocoons that are anchored to the sediment by an elongate ribbon of mucous. Larvae are retained in the cocoons until three chaetigers have developed, after which they enter the plankton where they develop into large fusiform-shaped planktotrophic larvae. Larvae settle and metamorphose after approximately 18 chaetigers have developed. See Blake (2006) for details. The formation of mucous egg masses after fertilization has also been reported. Guérin and Kerambrun (1984) identified such an egg mass in Malacoceros fuliginosus. The formation of any postspawning egg mass or cocoon would logically require pair formation among adults, but there are no observations to confirm this. Due to the lack of data on pair formation and spawning in species believed to be broadcast spawners, the number of species producing egg masses or cocoons may be underestimated. Radashevsky (2007) described an unusual type of external brooding in Rhynchospio nhatrangi in which gametes, embryos, and larvae up to the four-chaetiger stage are held in place by long chaetae on the posterior dorsal surface of the abdomen prior to release of the larvae into the water column. In a later article, Radashevsky et al. (2014) reported a similar mode of brooding for Rhyncho­ spio asiatica. These brooding species are hermaphroditic,

20 

 7.4 Sedentaria: Sabellida/Spionida

have thin-membraned eggs, and long-headed sperm. In contrast, Rhynchospio cf. foliosa reported by Radashevsky et al. (2016a) from Oregon, USA had thick-membraned eggs and short-headed sperm. These authors speculated that R. cf. foliosa, unlike other species of Rhynchospio, spawned gametes directly into the water column. The brooding of eggs and larvae on the surface of abdominal segments in some species of Rhynchospio is somewhat similar to that of Streblospio gynobranchiata, where eggs and larvae are held in place by branchiae-like structures. In contrast to spionids that broadcast their gametes directly into the water column, a cocoon, or “hatchery”, other spionids have been reported that package sperm into packets or spermatophores and variously discharge these in a manner that allows transmission to females. Spermatophores have been described for Microspio me­cznikowianus, Polydora cornuta, P. websteri, Tripolydora sp., Scolelepis sp. (as S. squamata), Spio filicornis, Streblo­ spio benedicti, S. gynobranchiata, and Pygospio elegans (Söderström 1920; Franzén 1956; Richards 1970; Greve 1974; Rice 1978, 1980; Rouse 1988; Rice and Levin 1998). The nephridia become highly modified in segments where gametes mature and eventually serve as gonoducts for the passage of eggs and sperm out of the body (Fig.  7.4.1.7  D). Depending on the species, a pair of nephridia may join and have a common nephridiopore (Fig. 7.4.1.7 D), or there may be two separate nephridiopores. In species where spermatophores are formed, sperm are concentrated and enclosed in discrete packets that are discharged from the male nephridia. Rice (1980) investigated the formation of spermatophores in the nephridia of mature male Polydora cornuta (as Polydora ligni). The nephridia of this species are enlarged paired urogenital organs located in several segments; Rice divided the structure into seven morphological regions: (1) nephrostome, (2) descending nephridial canal, (3) dorsal curvature, (4) U-shaped depressions, (5) large urn-shaped depressions with long, thin microvilli, (6) U-shaped depressions as in region 4, and (7) ascending nephridial canal that terminates in the nephridiopore. Rice found that the spermatophores are composed of a central sperm mass surrounded by tubules that form a capsule. Rice noticed that the tubules were identical to the microvilli found in areas 4, 5, and 6 of the nephridia and postulated that spermatophores were produced in the nephridia and derived from the same microvilli. The shape and size of spermatophores vary among species. Rice (1978) demonstrated that spermatophores of Polydora cornuta were released from the male and deposited outside the tube. These were then picked up by the female using ciliary currents generated by the palps and carried into her tube. Sperm were then stored in seminal

receptacles until egg spawning and capsule formation. This type of sperm transfer is a form of pseudocopulation because the male and female do not actually form pairs. In dense populations, this is a convenient manner in which males can disperse their gametes. Richards (1970) observed spermatophores attached directly to the body of specimens of Scolelepis from Barbados. They were large, white-colored, and granular in appearance with a leaflike shape approximately the size of a parapodium. The sperm were bound together in a matrix and became active and were released when the spermatophores were manipulated in seawater. The author, however, was not able to observe how the spermatophores were produced or how the sperm were transferred to females. The occurrence and morphology of seminal receptacles on female spionids has not been well documented. McEuen (1979) described seminal receptacle structures for several species including Pseudopolydora pauci­ branchiata and Pygospio californica. Similar appearing seminal receptacles are also found in Polydora cornuta (Fig. 7.4.1.7 E–F). These three species have dorsal seminal receptacles that are relatively small, but are found in all epitokous segments, whereas in S. benedicti, these same structures extend completely across the dorsum only of chaetigers 14 to 16 (McEuen 1979). The unusual reproductive biology of Scolelepis laon­ icola was revealed by Vortsepneva et al. (2008), who discovered that a parasitic polychaete, Asetocalamyzas laonicola, previously described by Tzetlin (1985) from the White Sea, was actually a dwarf male of its host spionid polychaete, Scolelepis sp., a female. This type of sexual dimorphism is not known elsewhere in the Spionidae. The taxonomy required that both the host and parasitic male would be referred to the same species, which became S. laonicola (Tzetlin, 1985). The host had been previously described as Scolelepis matsugae Sikorski, 1994, which was officially recognized as a junior synonym of S. laon­ icola by Sikorski and Pavlova (2015). Although the mode of fertilization and larval development of S. laonicola remain unknown, spermiogenesis, sperm ultrastructure, musculature, nervous system, and mode of attachment of the dwarf males have been described in detail (Vortsepneva et al. 2006, 2009a,b). All females observed by these authors had one to four attached males. The modified anterior end of the dwarf male is reduced, penetrates the female tissues and opens into its body cavity. The four main longitudinal muscle strands enter the female. These muscles are twisted 90° along the body of the male resulting in its dorsal side facing the dorsal side of the female with its ventral side turned up; the male is further oriented such that its posterior end faces the posterior end of



the female (Vortsepneva et al. 2009a). The septae of the host forms a chamber around the anterior region of the male (Vortsepneva et al. 2008). The males have a well-developed digestive track with the mouth opening inside the body cavity of the female where the male presumably derives nutrition (Vortsepneva et al. 2008). Early and late spermatids are joined by cytoplasmic bridges into tetrads. Mature sperm have an elongated nucleus and middle piece (Vortsepneva et al. 2006), characteristic of spionids that have a modified type of fertilization sensu Franzén (1956) and an introsperm sensu Jamieson and Rouse (1989). Because no copulatory organs have been identified, Vortsepneva et al. (2008) suggest that sperm are transferred by pseudocopulation within the tube of the females. The formation of egg capsules by spionids was first described by Söderström (1920) for Pygospio elegans and Polydora and later confirmed by Rice and Reish (1976) for P.  cornuta (as P. ligni). Mucus is extruded from each nephridiopore and contacts the wall of the tube. Eggs are then squeezed through the same nephridiopores. The two adjacent streams of mucous and their eggs coalesce into a single chamber that fills with additional eggs. At the same time, sperm that are stored in seminal receptacles near the nephridiopores are discharged into the capsules. Capsules produced on adjacent segments merge with one another, forming a beadlike string. In some species, the individual capsules are so tightly joined to one another (Fig. 7.4.1.7 I) that the entire string appears to be one unit. Capsules of P. cornuta are attached to the tube by two thin extensions representing the paired nephridiopores. Species having only a single nephridiopore have a single attachment for the capsules. In P. cornuta, the individual capsules are loosely joined to one another, but sometimes individual capsules are separate. In Dipolydora commensalis, the individual capsules are tightly joined to one another. In Boccardia proboscidea and Boccardia columbiana, the individual capsules are not fused with adjacent ones and remain separate in a line attached to the wall of the tube (Figs. 7.4.1.7 J; 7.4.1.11 A). In D. quadrilobata, adjacent capsules fuse and form a single elongate cylinder (Blake 1969; Fig.  7.4.1.7  K). Gibson and Paterson (2003) reported that the egg capsules of Amphipolydora vestalis were smooth cylinders formed from seven fused capsules that lacked stalks and were attached to the tube wall by mucous. Asexual reproduction. In a few species such as Pygospio elegans and several polydorids, asexual reproduction occurs as an additional form of reproduction. Two types of asexual reproduction occur in spionids: architomy and paratomy. Architomy is the simplest form and includes fragmentation of the body into individual segments or groups of segments,

7.4.1 Spionidae Grube, 1850 

 21

which then regenerate into new individuals (Fig.  7.4.1.9  G). Paratomy involves the division of the body into two distinct halves, with the reconstitution of missing parts by regeneration. Sometimes, the second half (stolon) remains attached to first half (stock) while regenerating. Additional divisions may also occur, resulting in chains of stolons being proliferated from the original stock parent. Spionids having paratomy tend to be very small, usually with a reduced and defined number of segments, whereas species having architomy are larger and have numerous segments. To date, architomic asexual reproduction in Spio­ nidae seems restricted to several species of the subfamily Spioninae. Architomy has been reported in the l­aboratory for Dipolydora caulleryi and D. socialis by Stock (1965), but has not been observed in the field. P. elegans has been widely reported as architomic (Rasmussen 1953, 1973; Bregenballe 1961; Muus 1967; Hobson and Green 1968; Armitage 1979; Wilson 1985; Anger 1984; Gibson and Harvey 2000; Thonig et al. 2016). Architomy also occurs in the closely related species Pygospio ­californica (Blake ­ mphipolydora 2006). Blake (1983) reported architomy for A abranchiata, from off Argentina in 100 m. Gibson and Paterson (2003) reported architomy for A. vestalis from New Zealand. Radashevsky and Nogueira (2003) described architomic fragmentation in Dipolydora armata. David and Williams (2012b) report architomy for Polydora colonia from Long Island, New York, USA. The best studied architomic species is P. elegans, in which the parent body divides into fragments through transverse fission. Each fragment regenerates into a separate individual (Fig. 7.4.1.9 G). Gibson and Harvey (2000) provided a defined sequence of events for regeneration following fragmentation: wound healing (day 1), development of a blastema to regenerate lost tissues and body regions (days 2–3), segmentation (days 3–6), and differentiation of regenerated segments into specific structures such as palps and pygidial cirri (days 4–8). This sequence was the same regardless of where on the body fission took place. Fragments having the original head had a higher survivorship than fragments containing the original posterior end. In most populations of P. elegans that have been studied, both sexual and asexual reproduction occurs. This strategy ensures that once colonized by settling larvae, populations could be expanded and maintained asexually. Armitage (1979), working with populations from two different localities in Tomales Bay, California, USA, found that both sexual and asexual phases of P. elegans were controlled primarily by seawater temperature with both forms of reproduction accelerated with increasing temperatures. These results support earlier observations by Rasmussen (1953) from Denmark that asexual reproduction in P. elegans increased during spring.

22 

 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.9: Spionidae asexual reproduction. A–E, diagram of paratomic asexual reproduction in Polydorella kamakamai; F, stolonization in Polydorella stolonifera; G, architomic asexual fragmentation and anterior regeneration in Pygospio elegans. A–F, after Williams (2004); G, after Rasmussen (1953).

Recent observations on architomy in Polydora colonia by David and Williams (2012b) evaluated the effect of temperature on regeneration. These authors determined that temperature played an important role in the rate of regeneration after fragmentation, with regeneration being twice as fast at higher temperatures (24°C) than at low temperatures (14°C). Paratomy has been reported for Polydora tetrabranchia and five closely related species of Polydorella: P. prolifera, P. stolonifera, P. smurovi, P. dawydoffi, and P. kamakamai (Campbell 1955; Blake and Kudenov 1978; Tzetlin and Britayev 1985; Radashevsky 1996; Williams 2004). Polydora tetrabranchia is a shell borer whereas the five Polydorella species construct tubes on the surfaces of sponges. According to Campbell (1955), asexual reproduction in P. tetrabranchia occurs by transverse fission of the stock animal. Regeneration of new posterior and anterior ends proceeds while the separate stolons are still connected, providing the appearance of two joined individuals. A chain of three individuals was found in a laboratory experiment, but no more than two joined individuals were ever observed in the field. Asexual reproduction proceeded year-round and approximately one-third of all specimens collected were regenerating anterior or posterior ends.

Radashevsky (1996) and Williams (2004) reviewed the pattern of paratomy in Polydorella species. In P. pro­ lifera, P. stolonifera, P. kamakamai, and P. smurovi, the fission and growth zone occurs between segments 10 and 11 (Fig.  7.4.1.9  A–F), whereas in P. dawydoffi, the growth zone appears between segments 11 and 12. The first three species have 15 segments; the latter two species have 16. Radashevsky (1996) has reported chains of five to six stolons for P. dawydoffi. In P. stolonifera, regeneration of a stolon begins with the development of a new anterior end with small palp buds that appear in the growth zone (Fig.  7.4.1.9  F). Eventually, the section of the worm anterior to the growth zone breaks away and regenerates a new posterior end, whereas the stolon differentiates into a fully functional and normal-appearing individual (Blake and Kudenov 1978). A similar pattern occurs in the other species (see Williams 2004). Sexual reproduction has been reported for P. smurovi and P. kamakamai but is likely to occur in all five species because a dispersive larval stage would be needed to colonize new sponges. Williams (2004), however, speculated that in lieu of sexually produced larval stages, adults of Polydorella species might leave their burrows and move to adjacent sponges, presumably by swimming or drifting.



Regeneration The ability to regenerate lost or damaged body parts is widespread in marine invertebrates including annelids (Bely 2010; Bely and Nyberg 2010; Lindsay 2010). In spionid polychaetes, observations of anterior and/or posterior regeneration have been made on more than 25  species (Stock 1965; Lindsay et al. 2007; 2008; Whitford and Williams 2016). The process of regeneration of the anterior ends was reviewed by Whitford and Williams (2016). After ablation of the anterior end, initial wound healing is followed by the formation of a blastema; this is followed by anterior extension of the blastema and differentiation of the pros­ tomium. In addition, Whitford and Williams (2016) observed that in Marenzelleria viridis, intersegmental furrows representing the development of lost segments were formed at the posterior end of the regenerating section and progressed anteriorly as regeneration continued. This process had earlier been observed by Paterson and Gibson (2003) for Amphipolydora vestalis except that, for this species, the reappearance of missing segments was simultaneous rather than sequential. Whitford and Williams (2016), however, suggest that the sequential development of lost segments may occur in all spionids, but is too rapid and difficult to follow in light microscopy. The number of segments that can be regenerated following ablation is somewhat limited by the number of segments that are lost. Whitford and Williams (2016) observed that for M. viridis, the number of segments replaced was equal to those lost by up to 10 segments; when 20 to 30 anterior segments were lost, regeneration replaced only 13 to 17 segments. These authors noted that other species replaced fewer segments. There have been observations of spionids replacing both anterior and posterior ends from fragments (Stock 1965), but such extensive regeneration has not been well studied. It is similar, however, to asexual reproduction by fragmentation and regeneration that has been observed in species such as Pygospio elegans. Life cycles Spawning. In general, most species of Spionidae that have been studied to date seem to reproduce during periods when water temperature is highest (Blake 1969, 2017; Levin 1984a; Levin and Creed 1986; Sato-Okoshi et al. 1990). Typically, such species are polytelic, and capable of reproducing more than once during that interval. Many of these species are capable of establishing dense populations during the times they reproduce because sequential sets of gametes and spawnings can be produced by a single female. Blake (1969) found that at least two species of Polydora in Maine, Dipolydora concharum

7.4.1 Spionidae Grube, 1850 

 23

and D. quadrilobata type II, were species that likely reproduced during the winter months. Both species were found with egg capsules and larvae in the early spring months, suggesting that gametogenesis and spawning occurred during months when the water temperature was lower. Larval development. An extensive literature exists on the larval development of spionids, largely because of their various types of development, elegant pelagic larvae, and the fact that so many species are available and accessible for study in nearshore habitats. Comprehensive accounts of spionid larval development that treat multiple species include those of Wilson (1928), Thorson (1946), Hannerz (1956), Blake (1969, 2006, 2017), Blake and Arnofsky (1999), and Blake and Woodwick (1975). Spionid larvae are characterized by having long provisional serrated chaetae, and prominent ciliary bands including a prototroch, telotroch, neurotroch, nototroch, and gastrotroch. The degree of development, organization, and number of prototroch and gastrotroch bands are critical in the identification of larvae encountered in the plankton. Additionally, distinctive body shapes, as well as pigment patterns and colors are usually species-specific. Because of these characters, keys and pictorial guides to planktic spionid larvae have been produced that allow users to identify individual species after collection and removal from the samples (Hannerz 1956; Larink and Westheide 2011). In the following sections, examples are provided for the main types of larval development in spionids. Details of all species known as of 1999 were presented in Blake and Arnofsky (1999), followed by some updates in Blake (2006, 2017). A few additional references are noted subsequently. Genera of Spionidae with species that spawn their eggs and sperm directly into the water column resulting in embryos that develop in the plankton include Laonice, Malacoceros, Marenzelleria, Paraprionospio, Prionospio, Scolelepis, and Spiophanes (Hannerz 1956; George 1966; Yokoyama 1981, 1996; Blake and Arnofsky 1999; Radashevsky et al. 2006). A complete list of studies through 1999 is included in Blake and Arnofsky (1999: appendix 1). Radashevsky et al. (2006) reported that for Prionos­ pio pata­gonica from Chile, small oocytes of 82 to 92 µm diameter were spawned directly into seawater. Planktic larvae of the same species were described from a small two-chaetiger stage to five- to six-chaetiger larvae, which settled and underwent metamorphosis in the laboratory; the presence of so few chaetigers in the planktic larvae of this species is unusual for the genus. The larvae of Prion­ ospio orensanzi were described by Diaz-Jaramillo (2004). This species has eggs of approximately 110 µm diameter

24 

 7.4 Sedentaria: Sabellida/Spionida

and produces elongate, thin planktic larvae that settle and undergo metamorphosis at the 28-chaetiger stage. The larvae of three species of Paraprionospio have been described from plankton: Paraprionospio patiens by Yokoyama (1981) (as P. pinnata) from Japan, Paraprionos­ pio cordifolia (as P. sp. B) by Yokoyama (1996) from Japan, and Paraprionospio alata (as P. pinnata) by Blake and Arnofsky (1999) from Northern California. All reported larvae of Paraprionospio have elongate, narrow bodies. The species names and synonyms are based on Yokoyama (2007). Examples of other well-described accounts of larval development of spionids that broadcast their gametes

directly into seawater or in egg masses include the following: M. viridis from off Nova Scotia by George (1966 as Scolecolepides viridis); Scolelepis (Scolelepis) foliosa from Sweden by Hannerz (1956 as Nerine foliosa); S. (Para­ scolelepis) cf. tridentata from Northern California by Blake and Arnofsky (1999) and Blake (2006) as Parascolelepis cf. tridentata; and Spiophanes duplex from Northern California by Blake (2006). Examples of the larvae of these kinds of ­spionids are presented for S. (Parascolelepis) cf. tridentata (Fig. 7.4.1.10 A, B); S. duplex (Fig. 7.4.1.10 C, D), and Laonice sp. (Fig. 7.4.1.10 E, F). The development of species of Streblospio includes brooding of larvae in dorsal pouches (S. benedicti) or

Fig. 7.4.1.10: Larvae of Nerininae. A, B, Scolelepis cf. tridentata: A, dorsal view; B, ventral view; C, D, Spiophanes duplex: C, dorsal view; D, ventral view, anterior end; E, F, Laonice sp.: E, dorsal view; F, ventral view. All after Blake (2006). Abbreviations: cilP, ciliated pit; gsT, gastrotroch; m, mouth; noT, nototroch; nuO, nuchal organ; pa, palp; pr, prostomium; prT, prototroch; teT, telotroch.



under specialized branchiae (S. gynobranchiata) prior to the release of larvae into the plankton. There is extensive literature on the larval development of S. benedicti (Dean 1965; Levin 1984b; Schulze et al. 2000; Pernet and McArthur 2006; Gibson et al. 2010). S. gynobranchiata development was described in detail by Rice and Levin (1998). Larvae of S. shrubsolii develop directly from eggs brooded in dorsal grooves on the body of the female until 14-chaetiger juveniles crawl off and burrow into the sediment (Cazaux 1985; Fonseca-Genevois and Cazaux 1987). Females of S. benedicti brood their young in dorsal pouches (Fig. 7.4.1.11 A–C), with larvae eventually released into the plankton. Collier and Jones (1967) described the dorsal brood pouches as thin-walled, dorsolateral extensions of the coelom and explained how eggs were transported from the ovaries to those pouches. Males of both S. benedicti and S. gynobranchiata produce spermatophores that are transferred to ventral seminal receptacles on the females (Rice and Levin 1998). Blake and Arnofsky (1999) and Blake (2006) provided a summary of the literature on S.  benedicti. Two types of development occur in S. bene­ dicti: lecithotrophic and planktotrophic, providing a classic example of poecilogony. Lecithotrophic larvae with up to 9 to 12 chaetigers (550–650 µm) are retained in brood pouches (Fig.  7.4.1.11  B, C) and then released; they settle within hours or a few days. These larvae lack provisional chaetae, have poorly developed ciliary bands, and are weak swimmers (Fig. 7.4.1.11 D–G). Metamorphosis is relatively rapid, with larvae developing thickened palps and branchiae (Fig.  7.4.1.11  H) and retaining cilia until the first mucous tube is constructed. Thereafter, early juveniles crawl and form tubes (Fig.  7.4.1.11  I). Lecithotrophic populations occur in the Southeastern United States, Gulf of Mexico, and California (Levin 1984b, Blake and Arnofsky 1999). Planktotrophic larvae are released from the brood pouches when they have four to nine chaetigers (200–300 µm long). These larvae have well-developed serrated provisional chaetae, well-developed ciliary bands (Fig. 7.4.1.11 J, K; up to 450 to 550 µm long), and are planktotrophic for up to 45 days. Planktotrophic development occurs along the eastern United States and Gulf of Mexico (Levin 1984b; Blake and Arnofsky 1999; Blake 2006). Planktotrophic populations have also been identified from estuaries on the Atlantic coast of France (Fonseca-Genevois and Cazaux 1987). Gibson et al. (2010) developed a more extensive evaluation of the morphological differences between the planktotrophic and lecithotrophic forms of S. benedicti. Superficially, planktotrophic larvae have well-developed provisional larval chaetae, sensory cilia, and anal cirri with bacillary glands. Lecithotrophic larvae lack larval chaetae and have only poorly developed sensory cilia and

7.4.1 Spionidae Grube, 1850 

 25

anal cirri that lack bacillary glands. Other aspects of morphogenesis were found that are not obvious superficially. For example, whereas notopodial chaetal sacs developed early in both larval forms, development proceeded differently. Planktotrophic larvae developed chaetal sacs that produced both larval chaetae and adult capillaries; in contrast, chaetal sacs of lecithotrophic larvae developed early, but did not produce any chaetae until later in development when adult capillaries were formed. Other differences observed were in the development of anal cirri, sensory cilia, prostomial mucous glands, timing of the development of the coelom and septa, and development and functionality of the gut. Gibson et al. (2010) also confirmed with the cytochrome oxidase I (COI) gene that the two forms of larval development represented the same species. Brooding and larval development of S. gynobranchi­ ata differ from that of S. benedicti in that eggs and larvae are brooded under straplike branchiae that develop on the abdominal segments of females (Rice and Levin 1998). Males produce spermatophores that are incorporated into ventrally located seminal receptacles on the females. There are 100 to 200 larvae produced per female. Larvae are released from the broods after three chaetigers have developed; these are planktotrophic larvae with ­serrated provisional chaetae and settle after 9 to 12 ­chaetigers have developed. Egg capsules containing eggs and embryos are known for genera of the subfamily Spioninae including Amphi­ polydora, Boccardia, Boccardiella, Carazziella, Dipoly­ dora, Microspio, Polydora, Pseudopolydora, Pygospio, and Spio. The literature for these genera is extensive and has been reviewed by Blake and Arnofsky (1999) and Blake (2006). Recent accounts of the development of additional spionids having egg capsules with brooding within adult tubes followed by planktic larvae include Amphipolydora vestalis by Gibson and Paterson (2003), Polydora neocaeca by Williams and Radashevsky (1999), Boccardia knoxi by Handley (2000), Polydora rickettsi by Radashevsky and Cárdenas (2004), Polydora ecuadoriana and Polydora carinhosa by Radashevsky et al. (2006), Pseudopolydora rosebelae by Radashevsky and Migotto (2009), Polydora cf. websteri by Barros et  al. (2017), Pseudopolydora cf. kempi and Ps. cf. reticulata by Kondoh et al. (2017), and ­Boccardia berkeleyorum, Dipolydora cardalia, Polydora pygidialis, and Polydora spongicola by Blake (2017). One example of this type of development is B. colu­ mbiana, a common intertidal species in the Eastern Pacific that bores into hermit crab shells, coralline algae, and tests of barnacles (Woodwick 1963a). The larval development was described by Blake and Arnofsky (1999) and Blake (2006). Egg capsules are deposited in a row within

26 

 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.11: Development of Streblospio benedicti. A–I, lecithotrophic larvae from California: A, five segments of adult female with larvae in brood pouches; B, C, sagittal section of female through brood pouches: B, early encapsulated larva; C, larva ready to hatch; D–F, newly emergent larvae, no provisional chaetae; lateral view; G, planktic larva before metamorphosis; H, juvenile capable of swimming and crawling, prototroch and telotroch still visible; I, crawling juvenile; J, K, planktotrophic larvae (Maine), newly released from brood pouches with long provisional chaetae. A, D, E, H, J, K, after Blake (2006); others original.



burrows excavated by the adult. Each capsule is attached separately to the burrow lining by two thin extensions (Fig.  7.4.1.12  A). Each egg capsule contains 50 to 60 eggs that individually measure 110 to 115 µm in diameter. All eggs are fertilized; this species does not produce nurse eggs. Early embryos are pretrochophores 120 × 100 µm in size that move slowly in the capsule using a pair of large ciliated patches on their ventral side (Fig.  7.4.1.12  B). An oral opening or vestibule is present; the yolk mass is prominent. The trochophore larvae are present after approximately 24 h and retain the ventral patches, but also have a prototroch and telotroch (Fig.  7.4.1.12  C); a large ciliated vestibule or mouth is prominent. By 48 h,

7.4.1 Spionidae Grube, 1850 

 27

the larvae have developed three chaetigers (Fig. 7.4.1.12 D: 130 µm long) and by 72 h, early four-chaetiger larvae are developed (170 µm long). These early chaetigerous larvae are characterized by having two and then six eyespots, serrated provisional chaetae, a well-developed prototroch and telotroch, but no segmental ciliary bands. The ventral ciliated patches are still present and are retained until the larvae leave the capsules, at which time they are shed. The four-chaetiger larvae are released into the plankton where they become planktotrophic and continue to develop. A typical four-chaetiger larva on release is 280 µm long, slender in shape, a strong swimmer, and photopositive (Fig.  7.4.1.12  E). The provisional chaetae are long and held close to the body providing the larva with

Fig. 7.4.1.12: Larvae of Spioninae. A–F, development of Boccardia columbiana: A, egg capsule; B, encapsulated pretrochophore; C, encapsulated trochophore; D, early three-chaetiger larva prior to release from capsule; E, fourchaetiger larva after release from capsule; F, large planktic larva; G, Polydora websteri, 12-chaetiger planktic larva; H, Pseudopolydora paucibranchiata, 13-chaetiger planktic larva; I, Dipolydora concharum, 14-chaetiger larva. A–F, after Blake (2006); G, I, after Blake (1969); H, after Blake and Woodwick (1975). Abbreviations: Cil patch, ciliated patch; gsT, gastrotroch; noT, nototroch; nuO, nuchal organ; pa, palp; prT, prototroch; teT, telotroch.

28 

 7.4 Sedentaria: Sabellida/Spionida

a streamlined rigid shape. The characteristic pigment pattern eventually consisting of a dorsal medial row of large branching chromatophores is first present from chaetiger 2. These larvae feed on phytoplankton and, in the laboratory, will also feed and grow on cells of algae and diatoms if provided. Eventually, the planktic larvae of B. columbiana become large and robust and develop a fusiform shape that characterizes several species of the genus Boccardia. The larva shown in the figure has 11 chaetigers and measures 560 µm long (Fig. 7.4.1.12 F). The body has an overall greenish cast; dorsal medial chromatophores begin on chaetiger 2 and continue posteriorly along the dorsum; additional lateral pigment is also present. Segmental cilia include nototrochs from chaetiger 3 and gastrotrochs on chaetigers 3, 5, 7, and another on chaetiger 10 that develops later. The modifications of chaetiger 5 are already evident. Nuchal organs and palps are beginning to develop. Examples of other species of planktic larvae of polydorids are shown: Polydora websteri (Fig.  7.4.1.12  G), Pseudopolydora paucibranchiata (Fig.  7.4.1.12  H), and Dipolydora concharum (Fig. 7.4.1.12 I). Of note are the different body shapes and pigment patterns that distinguish one species from another. Finer details of the chaetae of chaetiger 5, shape and form of the nuchal organs, eyespot patterns, and segmental ciliary bands also differ between species and genera. Readers are referred to Hannerz (1956), Blake (1969, 2006, 2017), and Blake and Arnofsky (1999) for further information on spionid larvae that produce egg capsules and brood them for variable amounts of time. Although reports of the development of spionid larvae that have either short or long periods in the plankton are numerous in the literature, direct development has rarely been reported or verified. The viviparous development of nonpelagic juveniles of S. shrubsolii by Cazaux (1985) approximates direct development because no free swimming larval stage is produced. Söderström (1920) reported that larvae of Boccardia natrix from Patagonia and sub-Antarctic Islands were brooded in epitokous segments and suggested that development was direct. This mode of development has never been subsequently observed or confirmed, however. The adults of Polydora curiosa from the Kurile Islands deposit only one to four eggs into capsules in their tube; these eggs are large, 240 to 330 µm in diameter. The resulting larvae are retained in the capsules until they are approximately 1400 µm long and have approximately 20 chaetigers, subsisting entirely on their intrinsic yolk reserves (Radashevsky 1994). Although most of the typical cilia develop, these larvae settle and undergo metamorphosis almost immediately on release from the

capsule, with only a very short planktic period or none at all; they do not feed until after settling (Radashevsky 1994). Although this species undergoes encapsulated lecithotrophic development, it can almost be considered as having direct development. Another species reported to have larvae retained in the capsules and tubes to a very late stage is P. carinhosa, as described by Radashevsky et al. (2006) from Brazil; these larvae have only a brief period in the plankton prior to settlement. Early development and size of the eggs is, however, unknown. As part of a cruise to the east Antarctic Peninsula in May 2000, specimens of Pygospiopsis dubia were collected from sediments in the Prince Gustav Channel at a depth of approximately 500 m. In addition to adults, small larval and postlarval specimens that seemed to be within tubes of adults were recovered from the same samples. The morphology of these specimens was described by Blake (2006) and Blake and Maciolek (2018). The smallest specimens had 14 chaetigers and measured 780 × 270 µm; they were short, thick, and did not have sufficient morphology to suggest they were planktic larvae. Although noto- and neurochaetae were present, these were not the serrated provisional chaetae typical of spionid larvae. Nototrochs were absent; a partial telotroch and at least one gastrotroch were observed. A pair of short palps was present. These specimens should be capable of slow swimming or crawling movements within a tube. A 16-chaetiger postlarva or juvenile that had no larval morphology at all was also described by Blake (2006) and Blake and Maciolek (2018). Of particular interest in the study of spionid development is the discovery of variable patterns of larval nutrition among several species belonging to the subfamily Spioninae. The majority of species in this subfamily deposit their eggs into capsules (see previous sections). In some species, all the eggs develop into larvae that initially subsist on yolk reserves derived from their eggs; these larvae are released into the plankton when their yolk reserves are depleted. Once in the plankton, larvae become planktotrophic and subsist on phytoplankton, remaining pelagic for an extended period prior to settlement and metamorphosis. In other species, both fertilized and nonfertilized eggs are present in the capsules. Here, the developing larvae ingest the nonfertilized eggs and subsist on this extrinsic yolk resource until it is fully consumed. At that time, larvae may leave the capsule and become pelagic for a short time until settlement and metamorphosis. The nonfertilized eggs are called nurse cells or nurse eggs; two distinct types have been reported: (1) eggs that are morphologically identical to the fertilized eggs but do not undergo cleavage and (2) eggs that undergo some or unequal cleavage. The first type is well documented in Boccardia



probo­scidea, Dipolydora quadrilobata, Polydora colonia, Polydora hoplura, Polydora nuchalis, and other species. The presence of this type of unfertilized egg suggest their origin is due either to a shortage of sperm or to gamete incompatibility; they are engulfed whole by the developing larvae (Wilson 1928; Woodwick 1960, 1977; Blake 1969, 2006; David and Williams 2012a). The second type occurs in Amphipolydora vestalis, Pygospio elegans, and Pseudo­ polydora kempi; these eggs are fragile and readily break up into small yolk granules (Fig. 7.4.1.8 K) that are devoured by developing larvae (Rasmussen 1973; Blake and Woodwick 1975; Gibson and Paterson 2003; Blake 2006). The type of development that incorporates nurse eggs in the capsules is termed adelphophagia and probably occurs in at least half the species of Spioninae that have been studied to date (Wilson 1928; Simon 1967; Blake 1969, 2006; Blake and Woodwick 1975; Blake and Kudenov 1981; Gibson and Paterson 2003). Adelphophagia has been considered a form of lecithotrophic development because the adult deposits yolk in nurse eggs that are ingested by the developing larvae instead of initially producing larger eggs (Woodwick 1977; Blake and Kudenov 1981). To further complicate these two patterns of development, Blake and Kudenov (1981) observed that Boccardia proboscidea is capable of producing pelagic larvae that are planktotrophic only after variable periods of ­producing lecithotrophic larvae that develop entirely in egg capsules and feed on nurse eggs. Many species probably shift seasonally between intrinsic and extrinsic yolk production; this pattern might be related to available organic inputs. Some species of Spionidae have been found to vary their mode of development throughout their geographic range or from season to season, a phenomenon termed poecilogony. In the species that have been studied, this variability typically includes the length of larval life or presence/absence of nurse eggs in the capsules (Hannerz 1956; Simon 1967, 1968; Blake 1969, 2006; Clark 1977; Blake and Kudenov 1981). Blake and Arnofsky (1999) reviewed the subject of poecilogony in spionids and reported on eight species: Boccardia proboscidea, Dipolydora quad­ rilobata, Pygospio elegans, Pseudopolydora kempi, Spio decoratus, Spio martinensis, Spio setosa, and Streblospio benedicti. Recent studies have identified or confirmed additional examples of poecilogony: Polydora hoplura, Boccardia polybranchia, and Boccardia wellingtonensis (Morgan et al. 1999; Duchêne 2000; David and Simon 2014; David et al. 2014; Oyarzun and Brante 2015). Except for S.  benedicti, all these species have populations that have been reported with one type of development producing larvae with a long planktotrophic larval development and another type with extended brooding in egg

7.4.1 Spionidae Grube, 1850 

 29

capsules using nurse eggs as an extrinsic yolk source. Not all species exhibiting adelphophagia have been reported to also have planktotrophic development. There are some examples in which a species thought to have all of the eggs in the capsules developing into larvae sometimes had individual capsules with unfertilized eggs. Blake (1969) first reported this for Polydora cornuta (as P. ligni). In this example, which was near the end of the breeding season, 2 of 11 capsules in a tube had unfertilized eggs and the developing larvae fed on them. The occurrence of variable modes of development in P. cornuta was explained by Rice and Rice (2009) as being the result of females using up their stored sperm during successive spawnings, resulting in the decline in the percentage of fertilized eggs per capsule and the increase of larval size at release. However, MacKay and Gibson (1999) found considerable variability in a Nova Scotia population of P. cornuta in which females switched between adelphophagia and planktotrophy with the switch not related to sperm availability. Another similar example of poecilogony was reported by Radashevsky and Cárdenas (2004), who observed that P. rickettsi had 10% of the capsules with unfertilized eggs that were consumed by developing larvae. Polydora cornuta is a polytelic species with females capable of rapidly producing multiple broods in a single summer season. During the reproductive season, a depletion of sperm in the seminal receptacles after production of successive strings of egg capsules would naturally result in some eggs not being fertilized and therefore available as an extrinsic yolk source. According to Rice and Rice (2009), such a pattern could be selected if the larvae that are feeding on nurse eggs required less time in the plankton when the required phytoplankton species were less abundant. The shift to permanent adelphophagia and the eventual evolution of a different type of nonviable nurse egg such as found in Pygospio elegans and Pseudopoly­ dora kempi would require a modification of oogenesis. A somewhat different, classic, form of poecilogony occurs in Boccardia proboscidea, in which (1) eggs in capsules are all fertilized and develop into larvae that become planktotrophic or (2) egg capsules contain nurse eggs that the developing larvae ingest and use as an extrinsic yolk source. In the second scenario, the larvae are lecithotrophic while in the capsules and become planktotrophic on release. However, in addition, Blake and Kudenov (1981), Gibson (1997), and Gibson and Gibson (2004) observed that two types of larvae were present in the capsules with nurse eggs. Some adelphophagic larvae remained small, apparently unable to feed on the nurse eggs whereas other larvae in the same capsules fed and grew to a large size. Both the large (type A) and small

30 

 7.4 Sedentaria: Sabellida/Spionida

(type B) larvae were released into the plankton at the same time, but were planktotrophic for different amounts of time. Such capability would allow local populations to be maintained by adelphophagic larval development whereas dispersal of the species over a broad geographic range would be accomplished by planktotrophic larvae (Gibson and Gibson 2004). In contrast to the appearance of unfertilized nurse eggs due to the reduction of stored sperm after successive spawnings as in Polydora cornuta, the production of nurse eggs in Boccardia proboscidea is an active process (Smith and Gibson 1999). Nurse eggs arise as viable oocytes that produce a fertilization envelope and complete meiosis; however, at this point, the nurse egg’s nuclear DNA is lost and the cytoplasm breaks up into small vesicles that contain yolk that is ingested by developing larvae (Smith and Gibson 1999). Oyarzun and Brante (2014) found that both types of larvae in the capsules with nurse eggs were capable of developing normally to metamorphosis. Type B larvae, however, were subject to cannibalism by type A larvae. Smith and Gibson (1999) studied the morphology of planktotrophic larvae that develop without nurse eggs and found that many larval structures were reduced compared with other spionid larvae, suggesting the early development of adult morphology, which facilitated settlement and development into juveniles. Oyarzun et al. (2011) collected Boccardia proboscidea from 12 or more locations along the West Coast of North America from Puget Sound to Southern California and, using two genetic markers, discovered a single species that exhibited a geographic break near Point Conception, CA. Simon et al. (2009) recorded similar genetic comparability between B. proboscidea introduced into South Africa and those from several locations on the West Coasts of North America. B. proboscidea probably originated in the Northeastern Pacific but has since spread to Australia, Hawaii, New Zealand, Argentina, and South Africa. It has most recently been reported from Europe, primarily from the Atlantic coast of Spain (Martínez et al. 2006), the northern coast of Scotland (Hatton and Pearce 2013), and North Sea locations from France to the Netherlands (Kerckhof and Faasse 2014). As an alien species now in many global locations, it is likely that its variable mode of reproduction and larval development has allowed B. proboscidea to successfully colonize new locations. Oyarzun and Brante (2015) recently reported on poecilogony in Boccardia wellingtonensis from Chile. Reproduction in this species is similar to Boccardia pro­ boscidea, with both planktotrophic and lecithotrophic development present in the local population. Similar to B. proboscidea, B. wellingtonensis also has both small nonfeeding larvae and larger feeding larvae in the same

capsules. These authors also documented the cannibalism of the large larvae on the smaller ones. Details on the development of lecithotrophic and planktotrophic larvae of Streblospio benedicti were presented earlier (see previous section). Despite considerable differences in both the superficial and internal morphogenesis of these two types of larval development, molecular analysis has demonstrated that specimens producing these larvae belong to a single species (Gibson et al. 2010).

Biology and ecology Behavior Feeding. An overall review of feeding in spionid polychaetes was recently published by Jumars et al. (2015). This represents a significant update of Fauchald and Jumars’ (1979) work, necessary due to the large body of research on polychaete feeding over the past three decades that has significantly changed earlier concepts regarding this topic. An intermediate review of some of the spionid research was presented by Blake (1996). A brief overview of some key observations is presented here. The ability of spionids to remove particles from the water during times of high particle flux is an active sedimentation process in coastal ecosystems (Frithsen and Doering 1986). In a hypothetical situation, water carrying a heavy suspended sediment load could be significantly cleared when it passes over dense populations of spionid polychaetes. The sediment that is collected by the spionids accumulates as part of their tubes or in interstices between the tubes. Flexibility in feeding behavior, coupled with demonstrated plasticity in reproduction and development for many species, undoubtedly contributes to the evolutionary success of spionids and their dominance in coastal ecosystems including the establishment of the dense tube mats that have been reported for some species (Blake 1971). Taghon et al. (1980) discovered that three species, Boc­ cardia proboscidea, Pseudopolydora kempi, and Pygospio elegans, were capable of switching from deposit feeding to suspension feeding when currents at the sediment/ water interface carried higher amounts of suspended sediments. Subsequently, Dauer et al. (1981) obtained the same result for six species in six different genera. This ability to switch between the water column and sediment surface for a particle source makes it difficult to assign spionids to a single feeding mode category or guild sensu Fauchald and Jumars (1979). Dauer et al. (1981) proposed the category “interface feeding” for species that are able to switch between the sediment surface and water column for



particle collection. Dauer et al. (1981) noted that interface feeders should have broad spatial distributions because of their ability to use a wide variety of food resources. Food particle collection involves different behaviors relative to the use of the palps if the animal is collecting particles from the water column or sediment surface. Dauer et al. (1981) observed differences in palp orientation and palp movement between species. When deposit feeding, both palps are in contact with the sediment, whereas, when suspension feeding, both palps either lash about in regular or irregular patterns, are held rigidly, or a combination of these. Taghon et al. (1980) observed another behavior whereby palps are coiled. Individual species may use one or more of these different palp orientations as part of their feeding activity. Dauer and Ewing (1991), working on the Great Barrier Reef, observed that Malacoceros indicus never extended its palps into the water column; instead, this species limited its particle collection activities to surface deposit feeding. M. indicus was found to have only one group of functional cilia on the palps, thus differing from other spionids with three or more different groups of cilia. This species inhabits coarse sediments that are not easily resuspended. Detailed accounts of palp morphology, particle collection, and waste removal were presented for Scolelepis squamata, Streblospio benedicti, and Paraprionospio pinnata by Dauer (1983, 1984, 1985). Scolelepis differs from other spionids in lacking a ventral ciliated groove on the palps; particles are transported to the mouth by palp contractions or coiling. When currents are present, individuals come to the sediment surface, extend their palps into a coiled orientation, and feed nonselectively on suspended and resuspended particles. The guts of S. squamata were found to contain sand particles, remains of small invertebrates, and fecal pellets (Dauer 1983). S. benedicti has complex food-collection and particle-sorting mechanisms, suggesting that a high degree of food resource partitioning is possible (Dauer 1984). A high degree of particle selection on the palps and at the pharynx was also demonstrated for P. pinnata by Dauer (1985). Particle selection is also known for four species of Polydora, including P. cornuta, P. websteri, P. ciliata, and P. commen­ salis (Dorsett 1961a; Dauer et al. 1981; Dauer 1991). The feeding biology of spionids that bore into calcareous substrates is not well known. The palps of spionids extended above various mollusk shells when placed in aquaria are easy to observe, but studies of their individual feeding habits are harder to detect. It is likely, however, that similar to their sediment-dwelling congeners, they take advantage of suspended particles in the water column and possibly the inhalant and exhalant

7.4.1 Spionidae Grube, 1850 

 31

currents generated by their hosts. P. ecuadoriana bore into a wide variety of calcareous substrates in South America and have been observed to both suspension and deposit feed (Radashevsky et al. 2006). P. bioccipitalis is known from California, Peru, and Chile from shells of intertidal bivalves. In Peru and Chile, the species was observed to concentrate in parts of the shell surrounding the siphons of local surf clams (Riascos et al. 2008). Williams (2002) observed Polydora umangivora and Polydora robi in the Philippines that fed on the eggs and embryos of their hermit crab hosts. The biology of Dipolydora commensalis is especially interesting because it lives in a shallow burrow that is excavated along the columella of a gastropod shell occupied by a hermit crab. This specialized species has short palps with an unusually narrow food groove that seems to be adapted to capturing particles that are stirred up or suspended by the activities of the hermit crab (Dauer 1991). Dualan and Williams (2011) determined that the short palp length, characteristic for this species, was influenced by the hermit crab host, which cuts or damages them. Worms taken out of the shells developed palps of a length typical for other species of Polydora. Levin (1981) studied the feeding biology of two ­spionids, Streblospio benedicti and Pseudopolydora pauci­ branchiata (Okuda) from the standpoint of interspecific and intraspecific competition for resources. Dried particles of Enteromorpha sp. were made available to several individuals of P. paucibranchiata, and this resulted in food fights in 98% of these tests. When the same experiments were tried for S. benedicti, food fights occurred in only 24% of these tests. P. paucibranchiata was thus more aggressive than S. benedicti. For P. paucibranchiata, Levin (1981) observed considerable interaction between the long palps of adjacent individuals and it was common for up to five worms to fight over a single food particle including algae, invertebrate larvae, or other polychaetes. She also observed individuals of P. paucibranchiata biting off a palp of another worm. The palps of S. benedicti were rarely used in such aggressive behavior. These results suggest that intense competition for food and space play a major role in regulating which species of spionids dominate at any one time. Tube building. Particles collected by spionids are used both as food and as building materials for their tubes. Few species have been studied in detail, but particle selection apparently plays an important role in both processes. For Polydora ciliata (Johnston), Dorsett (1961a) found that smaller particles are carried to the gut as food, whereas larger particles are used in tube construction. When

32 

 7.4 Sedentaria: Sabellida/Spionida

adding particles to the tube, P. ciliata uses the lateral lips surrounding the mouth to place them in a precise pattern. The tube is strengthened by mucous secretions from segmental glands or, as for example in Spiophanes, by b-chitin produced by parapodial glandular organs (see previous section, External details of the integument). It is likely that the majority of particles collected by spionids, when they are in the suspension feeding mode, are used in tube building because it is in such situations that the dense tube mats are formed. Within the Polydora complex are many species that are able to bore into calcareous substrates (Blake and Evans 1973; see related comments on the morphology of epidermal glands). Polydorids have been reported from virtually every type of calcareous structure including mollusc shells, living corals, coral rubble, and coralline algae. Many of the associations include commercially important bivalves such as oysters, other bivalves, and abalone (e.g., Moreno et al. 2006; Simon et al. 2006; Sato-Okoshi et al. 2008; Simon 2011; Walker 2011). Other species, such as Polydora armata, bore into different kinds of coral (Radashevsky and Nogueira 2003). Most species are not limited to a single host species or type of calcareous structure (Simon 2011). The burrows have various forms depending on which species is involved (Blake and Evans, 1973). Burrows may be either U-shaped (P. ciliata, P. giardi), pear-shaped (P. websteri), Y-shaped with a single branch (P. websteri), or with multiple branches (Dipolydora  concharum). P.  websteri burrows will differ depending on which bivalve host is involved. Although the structure and form of the burrows has been well documented, the actual mechanism by which the worms initially penetrate the substrate, enlarge, and continue to bore is poorly understood. There have been two conflicting hypotheses, involving either (1) a mechanical process that involves the major spines of chaetiger 5 or (2) a chemical process that includes secretion of an acid to dissolve the calcareous matrix. A third idea is that boring is accomplished by a combination of these two processes. The historical background of this controversy was reviewed by Blake and Evans (1973). These authors favored a chemical mechanism because experiments by Haigler (1969) demonstrated that P. websteri could still bore after the major spines of chaetiger 5 were removed. In addition, Evans (1969) demonstrated that large species with complex burrows, such as P. concharum, are able to enlarge their burrows at various points simultaneously, precluding a dependence on the spines of chaetiger 5. Zottoli and Carriker (1974) assessed burrow morphology, formation of the detrital tube within the burrow, and the ultrastructure of the bored surface in shells of Crassostrea virginica and Mytilus edulis formed by

P. websteri. During initial larval settlement, P. websteri was found to prefer crevices in the shell surface that presumably provide the juvenile with a place to form a simple tube, anchor itself, and then initiate shell dissolution and subsequent burrow enlargement. Juveniles slowly penetrate the shell and form a U- or flask-shaped cavity. Detritus collected by the palps is carried into the burrow forming an internal detrital tube. Evans (1969) had earlier observed that detrital material is absent in those areas where burrows are being enlarged. Zottoli and Carriker (1974) found that P.  websteri secretes a viscous fluid that dissolves the interprismatic organic matrix and then etches the exposed mineral prisms. The ends of the prisms were often noted to be broken off, presumably by chaetal abrasion as the worm moved back and forth. These dissolved and abraded substances were sometimes reincorporated into the detrital tube. Evans (1969) considered this substance to be redeposited. SatoOkoshi and Okoshi (1993) studied shells of scallops and oysters that were infested with four different species of Polydora. Using SEM, these authors discovered numerous concentric-like holes along the inner surfaces of the burrows. Scratches, presumably from chaetae, were also observed. The nature of the holes suggested that some chemical substance that probably dissolves the shell was being secreted by the worms along the length of its body. Sato-Okoshi and Okoshi (1993) support a chemical/physical mechanism to boring and suggest that the scratches they observed in the burrows were due to notoand neurochaetae that may participate in the formation of the concentric holes. Liu and Hsieh (2000), working in Taiwan, studied the burrows of Polydora villosa, which bores into live coral. The worms initially form U-shaped burrows similar to those of species that bore into mollusc shells, but as the coral grows, the worms elongate their burrows, forming multiple straight passages that are lined with mucous and sediments. A mud-lined tube extended from the burrows into the water column where the worms extend their palps and feed. Despite the long history of research on the mechanism of boring by Poly­ dora and its relatives, the source and chemical composition of the acidic secretions have not been identified. Distribution Habitat. A review of the large literature pertaining to benthic ecology and the role of spionids in benthic communities is beyond the scope of this review. The few examples given subsequently serve to demonstrate that spionids are often the most abundant and diverse components of benthic communities. Spionids are found in a wide variety of habitats and range from the intertidal to the deep sea. In bays,



estuaries, and nearshore environments, they build tubes in a full range of sediments from sand to silt. Populations frequently are so large that dense tube-mats form, serving to stabilize sediments and bury or otherwise smother the substrates or other organisms on which they settle (Blake 1971, 1996). Rapid build-up of dense sediment mats of P. cornuta, for example, has been reported to cause extensive mortalities in oysters (Galtsoff 1964). Pygospio elegans and P. californica occupy positions high in the intertidal zone of sand flats in estuaries and are subject to exposure at low tides (Armitage 1979; Blake 1996). In central California embayments, Boccardia pro­ boscidea and Pseudopolydora kempi are found most ­abundantly at the high and middle regions of the intertidal zone, whereas P. paucibranchiata is most abundant at the low intertidal zone (Blake 1996). On more exposed and cleaner sandy beaches, species of the genus Scolelepis are sometimes abundant. In subtidal sediments, species of Prionospio, Spio, and Spiophanes often dominate. Spionid population density has been found to be seasonal and to exhibit patterns of spring/summer abundance in temperate environments (e.g., Holland 1985). A typical season starts with overwintering adults responding to increasing spring temperatures and increased food supply by initiating gametogenesis and producing egg capsules. As polytelic species, individual females are capable of producing several clutches of eggs and strings of egg capsules during a single year. Larvae produced by these adults settle, build their own tubes, mature rapidly, and in turn produce more egg capsules and larvae. Zajac (1991) monitored intertidal populations of P. cornuta for two years in Connecticut, where densities peaked between June and August, and then decreased to low levels by October. Because of the great densities that have sometimes been recorded for species of Spionidae, research has focused on how such populations become established and are maintained. Interest has centered on the ability of spionids to switch between deposit and suspension feeding (see previous section). Taghon (1992) found that deposit-feeding individuals of Boccardia pugettensis and Pseudopolydora kempi maintained a constant distance to their nearest neighbor regardless of density. When suspension feeding, however, distances between neighbors decreased at high densities. These results, when taken with those of Levin (1981) on competition between nearest neighbors (see previous section), suggests that densities are more tightly controlled when worms are in depositfeeding mode than in a suspension-feeding mode. Blake (1969, 1971) collected Dipolydora quadrilobata from a low intertidal beach at Cobscook Bay in northern Maine. The site was subject to a great tidal range and

7.4.1 Spionidae Grube, 1850 

 33

the D.  quadrilobata zone was narrow, no more than 2 m wide, when exposed at low tide. The tubes of D. quad­ rilobata were positioned equidistant from one another, approximately 2.5 cm apart, and the entire array of tubes resembled a cribbage board (Blake 1996). Although few quantitative samples were taken at the time, nearestneighbor distances would suggest that no more than 250 individuals of D. quadrilobata could occupy one square meter of the bottom. The distance between these worms was obviously maintained by the length of the palps, suggesting that this population was mostly deposit feeding. In contrast, the same species was collected in Massachusetts Bay in dense tube mats that were dominated by Spio limicola. Densities of S. limicola and D. quadrilobata at one station were calculated at 72,373 and 8,442 individuals per square meter, respectively (Blake 1996). These dense populations of D. quadrilobata would only be possible in a high-flux environment in which food is brought to the worms via the water column. In deep-water environments, spionids are among the most dominant of benthic communities both in terms of the number of species and the individuals comprising these assemblages. Blake and Grassle (1994) recorded 64  species of Spionidae in continental slope samples from off North and South Carolina. Among these, 53 were believed to be new to science. Similarly, from slope sediments off Northern California, 17 of 26 species were believed to be new to science (Blake et al. 2009). In these locations, species of Aurospio, Laonice, Prionospio, and Spiophanes are the most common spionid genera. In the Northern California location, Prionospio delta, a widespread deep-water species, was dominant in lower slope communities and seemed to be an early colonizer of disturbed sediments (Blake et al. 2009). In the original description of Aurospio dibranchiata, Maciolek (1981a) reported that the species comprised 5.1% of the fauna in core samples taken by Grassle (1977) at 1760 m off Woods Hole, MA; this species was also found in recolonization experiments conducted at the same site, suggesting an opportunistic lifestyle. In later studies along the US Atlantic coast, A. dibranchiata was consistently found to be among the top five numerical dominants in areas deeper than 2000 m (e.g., Blake and Grassle 1994). The systematics and biology of deep-water spionids is poorly known. A recent article by Paterson et al. (2016) reported on seven new species of abyssal spionids, indicative of the effort needed to document the diversity of ­deep-sea spionids. Because of opportunistic life histories and variable modes of development, several spionids and other polychaetes have been distributed over great distances by vectors such as ballast water used in transoceanic

34 

 7.4 Sedentaria: Sabellida/Spionida

shipping or export of commercially important oysters or other molluscs intended to support local fisheries or aquaculture ventures. Several of these species are now so widespread that their point of origin is in question. The following species of Spionidae are believed to have been transported to new geographic locations in ballast water, by hull fouling, or via transport of shellfish intended for commercial aquaculture. For several of these species, such as Boccardia proboscidea, Polydora hoplura, P.  paucibranchiata, and Marenzelleria viridis, introductions into new geographic areas seem to be recent. For others, the timing of movements or introductions are not known and the species are likely cryptogenic, with introductions having occurred within the last 400 years commensurate with the expansion of global commerce and shipping. For some species, such as P. hoplura, there is the potential for damage to local shellfisheries due to the borings produced by the worm. For Marenzelleria spp. in northern Europe, at least two cryptic species have been identified as having been introduced from North America; these species have become dominant and have altered the composition of local benthic communities. For species such as P. cornuta there is the potential that cryptic species occur among some populations. The 11 species discussed subsequently are certainly not the only spionids that have colonized sites beyond their place of origin, but are those for which introductions have been noticed and documented in various manners. Boccardia proboscidea was originally described by Hartman (1940) from intertidal zones along the California coast from Mendocino to San Diego. The species was reported as abundant in shale and limestone reefs where it bored into and formed tubes in softer rocks. Hartman (1940) was also the first to observe that B. proboscidea produced egg capsules with both lecithotrophic and planktotrophic larvae (see larval biology, discussed previously). Subsequent to Hartman’s article, the species was reported farther north from Oregon to British Columbia by Hartman and Reish (1950), Berkeley and Berkeley (1950), and later by Sato-Okoshi and Okoshi (1997). Woodwick (1963a) reported the species from additional habitats in California including soft sandy sediments and as a borer in shells occupied by hermit crabs. Fauchald (1977) recorded the species from Panama. The species therefore occupies a wide array of habitats in the intertidal zone over most of the Northeast Pacific from Canada to Panama. The first report of Boccardia proboscidea outside of the Northeast Pacific was from Japan by Imajima and Hartman (1964); Sato-Okoshi (1999b) subsequently provided additional data on the distribution and habitats

from Japan. Blake and Kudenov (1978) found the species to be the numerically dominant polychaete near a sewage outfall in Port Phillip Bay, Victoria, Australia. The species was subsequently identified from Hawaii (Bailey-Brock 2000), New Zealand (Read 2004), South Africa (Simon et al. 2010), Argentina (Jaubet et al. 2011, 2018), Spain (Martínez et al. 2006), Scotland (Hatton and Pierce 2013), along the Belgian and Dutch coasts (Kerckhof and Faasse 2014), and from the Atlantic coast of Morocco (Goumri et al. 2017 as Boccardia polybranchia). The opportunistic nature of Boccardia proboscidea includes tolerance for a wide range of habitats, including variable salinities and temperatures and a larval biology that includes both lecithotrophic and planktotrophic larvae in the same populations. The species has obviously been transported, presumably from the Northeast Pacific to distant locations and now has a distribution that is nearly cosmopolitan. Boccardia chilensis was originally described by Blake and Woodwick (1971) from specimens collected along the Chilean coast as part of the Lund University Chile Expedition of 1948 to 1949. It was subsequently reported from New South Wales and Victoria, Australia by Blake and Kudenov (1978) and from New Zealand by Read (1975). This species seems to be a trans-Pacific species limited to the Southern Hemisphere, where it inhabits soft sediments. Boccardia wellingtonensis was originally described by Read (1975) from New Zealand and subsequently reported from Chile by Blake (1983 as B. polybranchia fide Sato-& Takatsuka 2001) and Oyarzun and Brante (2015) and from South Africa by Simon et al. (2010). This species has a variable mode of reproduction and larval development similar to that of B. proboscidea. The presence of both lecithotrophic and planktotrophic larvae suggests that the species is capable of being widely distributed. Although first described from New Zealand, the actual place of origin is unknown. Polydora hamata was originally described from Virginia on the US Atlantic coast by Webster (1879a), who also reported it from New Jersey (Webster 1879b); Hartman (1951) reported the species from the Gulf of Mexico (Louisiana). On the Pacific coast, Berkeley (1927) described Boccardia uncata from British Columbia; this species was subsequently reported as far south as Southern California and Western Mexico (Berkeley and Berkeley 1952; Hartman 1961; Reish 1963). Okuda (1937), Imajima and Hartman (1964), and Radashevsky (1993) reported the species from Japan. Blake (1966) examined specimens from both the US Atlantic and Pacific coasts and concluded that they were the same species and referred all records to Boccardia hamata. D. Dean and J.A. Blake combined their separate



life history studies into a single article describing larvae of B. hamata from both the East and West Coasts of North America (Dean and Blake 1966). The East Coast studies were conducted in Connecticut, representing the first reports of the species from New England. Additional collections in New England suggest that the northern limit of the species is Cape Cod Bay, MA (Blake unpublished). Blake and Kudenov (1978) established the genus Boccar­ diella and assigned B. hamata as the type species. The habitats for B. hamata are primarily as a shell borer on the US Atlantic and Gulf coasts and in sediments and shells on the Pacific Coast. Until recently, Boccardiella hamata was limited to all three coasts of North America and Japan. However, ­Kerckhof and Faasse (2014) provided the first report of the species from Europe, where it was found among Pacific oysters being cultured on the southwestern delta in the Netherlands. This discovery suggests that B. hamata and possibly Boccardia proboscidea, which was found in the same habitat, may have been introduced into Europe with the oyster cultures. However, Kerckhof and Faasse (2014) do not rule out shipping and ballast water as the vector. Boccardiella ligerica was originally described from the Estuary of Loire, France by Ferronniére (1898); it is the senior synonym of Polydora redeki described by Horst (1920) from Holland (fide Blake and Woodwick 1971). The species has been reported several times from estuarine locations along the English Channel in France (Rullier 1960; Dauvin et al. 2003) and northern Germany (Augener 1939; Hempel 1957a,b). The systematics and morphology of the species was addressed by Blake and Woodwick (1971), with additional records clarified by Blake (1983). Based on these two latter accounts, the species inhabits sediments in estuarine locations with very low salinities. Globally, Boccardiella ligerica has been identified from California (Blake and Ruff 2007) with records from San Francisco Bay and the San Joaquin River Delta (Light 1977, 1978) and Newport Bay river outlets in Southern California (Kudenov 1983). US Atlantic records of the species extend from Florida to Virginia and Delaware Bay; dense populations of the species have been seen in the Cooper River near Charleston, SC (Blake unpublished). Boccar­ diella ligerica has been identified from various Caribbean islands and was identified from samples in Uruguay and Argentina in brackish water (Blake 1983). Global records of B. ligerica and other invasive species are summarized in a variety of online databases, some summarized in the World Register of Marine Species and World Polychaeta Database (Read and Fauchald 2017; Molnar et al. 2008). As with many widespread spionids, the actual point of origin of B. ligerica is not known.

7.4.1 Spionidae Grube, 1850 

 35

Polydora cornuta is a widely distributed species, reported from all three coasts of North America, the Caribbean Sea south to Brazil and Argentina, Europe, Australia–New Zealand, Asia from Russia, Japan, and Korea to China, and India. The origin of the species is unknown, but is likely the Pacific Ocean due to the presence of numerous congeners and closely related species. Radashevsky (2005) compared adult and larval morphology of the species from widely separated populations but was unable to detect consistent differences and concluded that all reports were of single species. There is, however, evidence that Polydora cornuta is potentially composed of several genetically distinct incipient or sibling species (Rice et al. 2008; Rice and Rice 2009). These authors attempted to crossbreed North American populations from Florida with West Coast (California) and East Coast (Maine) populations. The compatibility was low in all combinations (0%–7%) except for crosses with Florida females and California males in which compatibility was 42%. Interestingly, a comparison of the COI gene among these same three populations and from specimens from New Zealand demonstrated that three clearly defined and well-supported groups were present: (1) Florida, (2) California and New Zealand, and (3) Maine. The Maine haplotypes and California– New Zealand haplotypes were closer to one another than to Florida. The results of the cross-breeding experiments and low reproductive compatibility for the separate populations together with the genetic differences with the COI gene, suggest that morphologically similar yet genetically distinct populations of P. cornuta likely represent sibling or incipient species. More extensive genetic studies of these and other populations are needed to further understand the distribution of this species globally and whether one or several species are present. Polydora hoplura is a large spionid that bores tunnels into the shells of commercially important bivalve molluscs and other calcareous habitats and has likely been transported globally with shellfish being introduced to enhance local aquaculture. The species was originally described from Naples, Italy by Claparède (1869) and has subsequently been reported from the Mediterranean and northern Europe including the UK (Carazzi 1893; Lo Bianco 1893; Marion and Bobretzky 1875; McIntosh 1909; 1915; Wilson 1928; Soulier 1903; Mikac 2015). At the same time, P. hoplura has been reported from South Africa (Day 1955, 1967; Simon et al. 2006, 2010), New Zealand (Read 1975), and Australia (Blake and Kudenov 1978). Radashevsky et al. (2017) redescribed specimens from the type-locality in the Gulf of Naples and established a neotype. These authors also reported on new materials from South Korea.

36 

 7.4 Sedentaria: Sabellida/Spionida

A closely related species, Polydora uncinata was described by Sato-Okoshi (1998) from Japan and later identified from southwest Australia (Sato-Okoshi et al. 2008; Sato-Okoshi and Abe 2012) and Brazil (Sato-Okoshi and Takatsuka 2001; Radashevsky and Olivares 2005). Two recent articles, appearing at effectively the same time, using morphology and molecular data have determined that P. uncinata is in fact a junior synonym of P. hoplura (Radashevsky and Migotto 2017; Sato-Okoshi et al. 2016). Radashevsky and Migotto (2017) also reported P. hoplura from California, the first records from North America. Polydora hoplura thus occurs widely in Europe, Japan, South Korea, Australia–New Zealand, South America, and South Africa and is a significant pest of oysters and abalone as a borer into their shells. The molecular data from Sato-Okoshi et al. (2016) show no difference between populations in Japan, Australia, and South Africa. The recent identification of P. hoplura from several habitats in California by Radashevsky and Migotto (2017) seems to be a new arrival that might cause problems with local shellfisheries. The species has not been recorded in regional California faunal guides (Blake and Ruff 2009). Polydora colonia is a small spionid that builds tubes in soft sponges on which it feeds. Moore (1907) originally described the species from sponges collected from pilings near Woods Hole, MA, USA. The species has since been reported from Massachusetts to North Carolina and Florida along the US Atlantic coast, Jamaica (as P.  ancistrata Jones), South Africa, Brazil, and Argentina in the western North and South Atlantic (Blake 1971, 1983; Dauer 1974; Neves and Rocha 2008; Cangussu et al. 2010), and from Europe (Aguirre et al. 1986; Tena et  al. 2000; Zenetos et al. 2010; Occhipinti-Ambrogi et al. 2010). David  and Williams (2012) described the larval development and architomic asexual reproduction of the species from off Long Island, NY. The wide distribution of P. colonia in the Atlantic Ocean suggests its distribution has been the result of movement with the host sponge, Micro­ cion prolifera on the hulls of ships and subsequent colonization of the sponge and polychaete assemblages on docks and pilings in major harbors. However, the point of origin of the species is not known and careful comparison of molecular and morphological data is required to ascertain the origin and status of the polychaete as a cryptogenic or more recently introduced alien species in certain locations. The worm does not seem to cause any harm, but the role of the host sponge in local ecologies where it has been introduced needs to be investigated. Polydora websteri, often called the mud-blister worm, was originally described by Hartman (1943) from oyster

shells in Long Island Sound, CT, USA, but the actual geographic origin of this species is not known. Blake (1971) redescribed and documented the species from Newfoundland and Quebec in eastern Canada and from Maine to South Carolina along the US Atlantic coast. The species has been recorded widely from all three coasts of North America; it has also been recorded and studied in Hawaii (Bailey-Brock and Ringwood 1982), western South America (Blake 1983), Japan (Sato-Okoshi 1999a), ­Australia (Blake and Kudenov 1978), and New Zealand (Read 2010), where it is considered invasive. P. websteri is known to produce mud-blisters in commercial oyster shells throughout its range, thus lowering the market value of the oysters. It has therefore been the subject of several biological studies related to shell boring and effects on commercial molluscs (Hartman 1945, 1951, 1954, 1961, 1969; Medcof 1946; Owen 1957; Hopkins 1958; Foster 1971; Haigler 1969; Evans 1969; Blake and Evans 1973; Zottoli and Carriker 1974; Bergman et al. 1982). Sato-Okoshi and Abe (2012) provided the first molecu­ lar analysis using 18S rRNA comparing Polydora websteri (Japan and Australia) with two closely related species: P. calcarea (Japan and Australia) and P. haswelli (Japan). Their results demonstrated that although closely related, the three species were distinct. The results also demonstrated that there was no genetic difference between specimens of P.  websteri from Japan and Australia. Although the origin of P. websteri has not yet been confirmed, the species has most certainly been transported to distant locations with oysters and other molluscs intended for commercial aquaculture. Further molecular analysis will help understand the movement of this species globally. Pseudopolydora paucibranchiata is a relatively small tube-building spionid polychaete that forms dense assemblages in low intertidal to shallow subtidal sediments. The species was first described from Japan by Okuda (1937) and in Asia it ranges from the Kuril Islands and Japan south to the Yellow Sea and Taiwan (Imajima and Hartman 1964; Radashevsky 1993; Sato-Okoshi 1999b, Radashevsky and Hsieu 2000b). P. paucibranchiata also occurs in the Eastern Pacific from Washington to Baja California (Blake 1975; Blake and Woodwick 1975; Light 1977, 1978; Blake and Ruff 2007). The species has been introduced to Australia–New Zealand (Read 1975; Blake and Kudenov 1978; Hutchings and Turvey 1984) and more recently into Europe where it has been recorded from Norway (Ramberg and Schram 1982), Portugal (Rodrigues et al. 2011), Spain (Cacabelos et al. 2008), and the eastern Mediterranean Sea including the south coast of Turkey, the Aegean Sea, and the Sea of Marmara (Dagli and Çinar 2008; Çinar et al. 2011, 2012;



Dagli et al. 2011). The larvae of P. paucibranchiata are illustrated in Larink and Westheide (2011), a guide to European coastal plankton. There are no published accounts of P. paucibranchiata from either the US Atlantic or Gulf coasts; however, several specimens were identified by one of us (JAB) from the east coast of Florida as part of the U.S. EPA National Coastal Condition Assessment program in 2010. Larval development has been described for populations in the Sea of Japan (Myohara 1980) and California (Blake and Woodwick 1975). The species is assumed to have originated in the northwest Pacific and spread from there perhaps to California and Australia. Further expansion of the range could have continued from new locations; however, molecular data is required to confirm the point of origin of the species. Possible vectors for dispersal include ballast water, hull fouling, and sediments associated with transplants of the Pacific oyster (Crassostrea gigas) to new locations as an effort to develop commercial populations. Marenzelleria viridis was originally described by Verrill (1973) as Scolecolepis viridis from offshore New England. Hartman (1942), as part of a review of Verrill’s collections, transferred the species to Scolecolepi­ des without explanation. Maciolek (1984b) redescribed S. viridis and transferred it to Marenzelleria based on the close similarity of the species to Marenzelleria wireni, the type species of the genus. She also redescribed M. wireni based on syntypes and new materials from the Arctic. Maciolek (1984b) also reviewed the then known records of the species, which ranged from Nova Scotia to Virginia along the eastern coast of North America. George (1966) had earlier described the reproduction and larval development of the species from Nova Scotia (as S. viridis). Marenzelleria spp. was introduced, probably several times into northern Europe in the 1970s with abundant populations first observed in the North Sea (ca. 1979) and subsequently in the Baltic Sea in 1985 (Bick and Burckhardt 1989; Bastrop et al. 1997). The vector for the original introductions in Europe was likely through ballast water. Initially, the northern European species was identified as M. cf. viridis but with at least three types (I, II, and III) were identified based on allozyme polymorphisms (Röhner et al. 1996) and the mitochondrial gene marker, 16S rRNA (Bastrop et al. 1997). Types I and II were present in several North American and European populations. Type III was also present in Marenzelleria collected in North Carolina (Bastrop et al. 1997). Given the invasive nature of the introductions of Marenzelleria spp. into European waters, numerous articles on the biology, ecology, and systematics have been published (see Zettler 1997 for bibliography). Sikorski and

7.4.1 Spionidae Grube, 1850 

 37

Bick (2004) reviewed the taxonomic history of Marenzel­ leria and revised the genus, describing four species with synonyms including the assignment of types I and II identified in the genetic studies. A fifth species from North Carolina was indicated as provisional, but not named until described by Bick (2005b). Bick (2005b) provided a key to all five species; the species and their known distributions are listed in the following: 1. Marenzelleria wireni Augener, 1913. Restricted to but widely distributed in Arctic regions. 2. Marenzelleria arctia (Chamberlin, 1920). Including some M. wireni records; restricted to Arctic estuaries. 3. Marenzelleria viridis (Verrill, 1873). Including genetic type I, distributed on the North American Atlantic coast from Nova Scotia to Virginia and in Europe including Scotland and the North Sea. 4. Marenzelleria neglecta Sikorski and Bick, 2004. Including some previous M. viridis records and genetic type II; distributed on the US Atlantic coast from North Carolina to Georgia and in Europe in the North Sea and Baltic Sea; also introduced into California in the San Joaquin River delta, part of the San Francisco Bay system. 5. Marenzelleria bastropi Bick, 2005b. At present, this species, which is genetic type III, seems to be rare, having been collected only from Currituck Sound, NC, USA. A phylogenetic analysis using 16S rDNA, cytochrome b, and COI was developed by Blank and Bastrop (2009), which indicated that the basal species were M. wireni and M. arctia, thus suggesting an Arctic origin for the genus. Based on the morphological and genetic studies, it was evident that two North American species, M. viridis (genetic type I) and M. neglecta (genetic type II) were introduced into Europe independently as hypothesized by Bastrop et al. (1998). Studies on larval development of M. viridis by George (1966) and Bochert and Bick (1995) suggest that the species has a sufficiently long larval life to survive for up to 8 weeks, which is more than enough time to survive a trip across the Atlantic in ballast water and discharge into European waters. Bastrop et al. (1998) postulated that Marenzelleria in the North Sea (type I = M. viridis fide Sikorski and Bick 2004) was derived from populations introduced from North American sites north of Chesapeake Bay to New England and Nova Scotia, whereas Marenzelleria in the Baltic Sea (type II = M.  neglecta fide Sikorski and Bick 2004) was derived from populations south of Chesapeake Bay in the southeast United States.

38 

 7.4 Sedentaria: Sabellida/Spionida

Recently, Marenzelleria neglecta has invaded the mouth of the Don River, Taganrog Bay, and other sites in the mouth of Sea of Azov, which borders both Ukraine and Russia; the species is now dominant in several locations (Syomin et al. 2017). These authors also report M. neglecta in the Strait of Kertch and some sites in the Black Sea.

Phylogeny and taxonomy Spionidae comprise approximately 590 species in 38 genera. Although more than 70% of species belong to the eight largest genera, 19 genera are monotypic. Taxonomic history The systematic literature of the Spionidae is one of the most extensive among all of the Polychaeta. Currently, the Spionidae includes approximately 590 species and 38 valid genera (Read and Fauchald 2017; and additional references). The family Spionidae was established by Grube (1850) to include the genera Spio Fabricius, 1785, Polydora Bosc, 1802, Scolelepis Blainville, 1828, and Malacoceros Quatrefages, 1843. The first efforts to synthesize spionid systematics were by Carazzi (1893) and Mesnil (1896). Carazzi (1893) reviewed species of Polydora and established the genus Boccardia, which has branchiae anterior to chaetiger 5 and two types of modified spines. Mesnil (1896) divided the family into two groups based on external morphology: (1) species with a narrow prostomium, including Polydora, Boccardia, Laonice, Spio, Microspio, Nerinides, Aonides, Nerine, Spionides (= Laonice), and Pygospio; and (2) species with lateral processes or horns on the prostomium, including Scolelepis (= Malacoceros) and Marenzelleria. Mesnil (1896) also considered the distribution of branchiae, form of anal cirri, occurrence of dorsal hooded hooks, and presence of capillaries in segments with hooded hooks as significant generic characters. He removed the genus Disoma to a separate family (currently the genus Trochochaeta, family Trochochaetidae Pettibone). Söderström (1920) emphasized internal morphology, including reproductive characters. He observed that certain genera, including Spio, Microspio, Pygospio, and Polydora formed a well-defined group having similar nephridia, thin-membraned eggs, long-headed sperm, and produced egg capsules that were incubated by females within their tubes. For these genera, he established the subfamily Spioninae. Other spionids having thick-membraned eggs, a different nephridial structure, and short-headed sperm included the genera Nerine (= Malacoceros), Colobranchus (= Malacoceros), Scolecolepis (= Scolelepis), and Aonides

were referred to the subfamily Nerininae. Söderström (1920) also considered the nephridia and genital structures of Laonice to be sufficiently different to establish yet another subfamily, the Laonicinae. These categories were supported by studies of larval development by Hannerz (1956), sperm morphology by Franzén (1956), and adult morphology by Orrhage (1964). In the years since Söderström’s 1920 monograph, spionids have increasingly been reported globally, mostly from shallow-water habitats but also from the deep sea. Important works treating multiple species include: 1. European waters: Fauvel (1927); Sigvaldadóttir (1992, 2002); Sigvaldadóttir and Mackie (1993); HartmannSchroder (1996); Bick et al. (2010); Meißner et al. (2011). 2. South Africa: Day (1961, 1967); Simon (2009, 2011). 3. US Atlantic coast: Pettibone (1962; 1963); Blake (1971); Day (1973); Maciolek (1984a,b, 1985, 1987, 1990, 2000). 4. Gulf of Mexico and Caribbean Sea: Hartman (1951); Foster (1971); Delgado-Blas (2006, 2008). 5. Northeastern Pacific: Berkeley and Berkeley (1952); Hartman (1936, 1941, 1969); Banse and Hobson (1968); Hobson and Banse (1981); Light (1978); Woodwick (1963a,b); Blake and Woodwick (1971, 1972); Blake (1996). 6. Northwestern Pacific: Imajima (1959, 1989, 1990a–e, 1991, 1992); Radashevsky (1993; 1994a,b); Sato-Okoshi (1998, 1999a,b). 7. Taiwan: Radashevsky and Hsieh (2000a,b). 8. Central and Southern Pacific: Woodwick (1964); Ward (1981). 9. Australia–New Zealand: Blake and Kudenov (1978); Hutchings and Rainer (1979); Hutchings and Turvey (1984); Rainer (1973); Read (1975); Blake (1984);. Wilson (1990), Meißner and Götting (2015); Radashevsky (2015); Walker (2011). 10. South America and Antarctica: Hartman (1967); Blake (1983); Radashevsky and Lana (2009); Radashevsky et al. (2006). Deep-water taxa are now being treated more regularly. For example, most of Maciolek’s articles cited previously include species from the deep-water collections made in the Atlantic Ocean by Dr. Howard Sanders of the Woods Hole Oceanographic Institution; Paterson et al. (2016) described new species from worldwide deep-sea locations. Meißner et al. (2014) described spionids from Northeast Atlantic seamounts. However, large numbers of deep-sea spionids from the US Atlantic and Pacific slopes and elsewhere remain undescribed (Blake and Maciolek unpublished).



Phylogeny Morphological studies. Sigvaldadóttir (1998) studied the phylogenetic relationships of genera of the Prionospio complex using parsimony. For the generic analysis, she used 10 species representing all the genera and subgenera of this complex with Laonice as the outgroup. For the more inclusive Prionospio analysis, she used 16  species that included Orthoprionospio as the outgroup; this selection was not explained, but was inappropriate as Ortho­prionospio is considered as part of the Prionospio complex. Results of the generic analysis were that the subgenera P. (Minuspio) and P. (Aquilaspio) and the genus Apoprionospio were not part of a monophyletic Pri­ onospio and were thus all synonymized with Prionospio sensu lato. However, there are issues with the characters and character states used in this analysis in that pinnate branchiae as coded included both the pinnate and platelike forms that have entirely different morphologies (see section on branchial morphology and Fig. 7.4.1.3 D–F). In addition, the author referred P. banyulensis and P. pilkena to Aurospio, presumably based on branchiae being first present from chaetiger 3. In fact, there are other characters that are unique to the type species (A. dibranchiata) that should have been considered. The author acknowledged the preliminary nature of the analysis and that most of the data on characters and character states were derived from the literature rather than an actual review of specimens. For these reasons, the results of the phylogenetic analysis of Prionospio genera of Sigvaldadóttir (1998) should be used with caution. Yokoyama (2007), as part of his revision of Paraprion­ ospio, presented a cladistic analysis using parsimony that included 28 characters and nine species of Paraprio­nospio, Aurospio dibranchiata, Laubieriellus grasslei, Orthoprio­ nospio cirriformia, Prionospio (Aquilaspio) krusadensis, P. (Prionospio) steenstrupi, and S. benedicti; Laonice cirrata was the outgroup. The results demonstrated that Parapri­ onospio was a monophyletic genus, but that Prionospio was not because P. (A.) krusadensis exhibited a sister relationship to Paraprionospio and was well separated from a clade that contained P. (P.) steenstrupi and L. grasslei. These results indicate that Prionospio is paraphyletic and differ significantly from those of Sigvaldadóttir (1998), who considered that the subgenera of Prionospio were all part of a single monophyletic Prionospio. Yokoyama (2007) also demonstrated in this analysis that Paraprion­ ospio could be divided into four clades and was able to relate the species in each to their geographic origins. Rice and Levin (1998) presented a brief cladistic analysis to evaluate the relationships of three species and one separate subspecies of Streblospio using 16 characters and

7.4.1 Spionidae Grube, 1850 

 39

with Spiophanes kroyeri and P. pinnata as outgroups. The results consistently show S. benedicti and S. gynobranchi­ ata as a clade, with the other two species of Streblospio forming a sister group. Phylogenetic relationships among five Spiophanes species based on partial mitochondrial and nuclear sequences were investigated by Meißner and Blank (2009). Molecular data confirmed the results of the morphological studies in that specimens of “S. bombyx” from Europe and California were genetically distinct and form monophyletic clades in the resulting phylogenies. Thus, the results supported the validity of the newly described S. norrisi (Meißner and Blank, 2009) as a separate species that is morphologically and genetically distinct from European S. bombyx. Radashevsky et al. (2016a) compared molecular gene sequences of Pygospio from California and Oregon (USA), Scotland, and the White Sea and Sea of Okhotsk (Russia). Although the overall results showed widespread genetic similarity among P. elegans populations, the results also revealed two genetically distinct populations that diverged from P. elegans. Pygospio sp. 1 was from the Sea of Okhotsk and morphologically identical with P. elegans; P. sp. 2 was from Oregon and co-occurred with P. elegans but differed in the absence of neuropodial spoon hooks and likely represents a separate species. The authors suggest that these two populations might represent undescribed species but that further studies of their morphology and reproductive biology are required. Radashevsky et al. (2014, 2016b) evaluated the genus Rhynchospio using molecular sequences (mitochondrial 16S rDNA, nuclear 18S and 28S FDNA, and histone 3), adult morphology, and reproductive differences to help separate closely related species that were similar and had often been subjective synonyms. Based in part on these results, R. arenincola from the Eastern Pacific, long considered a synonym of R. glutaea, was resurrected and R.  glutaea was restricted to South America from where it was originally described. In addition, R. arenincola asiatica from the Kurile Islands was raised to full species status. Five species have a unique form of brooding and ent-aquasperm; another species, R. cf. foliosa from Oregon, has ect-aquasperm and presumably is a broadcast spawner. Sato-Okoshi et al. (2016) compared widespread populations of the shell borers, Polydora hoplura and P. unci­ nata from Australia, Japan, and South Africa, using four gene sequences: nuclear 18S rRNA, 28S rRNA, mitochondrial 16S rRNA, and cytochrome b. The results demonstrated that, in addition to morphological similarity, there were no genetic differences between these populations.

40 

 7.4 Sedentaria: Sabellida/Spionida

The authors concluded that the populations are based on specimens that were transported by artificial means and recommended that the two species be synonymized. As part of their study, gene sequences from other species deposited in GenBank were used in constructing trees. The results from the 28S rRNA and 16S rRNA trees, in addition to demonstrating the identical nature of widespread populations of P. hoplura and P. uncinata, also demonstrated the monophyly of the genera Polydora and Dipolydora. The synonymy of P. hoplura and P. uncinata was also recommended by Radashevsky and Migotto (2017) based on the morphological similarity of specimens from Brazil, California, Chile, Italy, Japan, New Zealand, Australia, and South Korea. Molecular studies. Molecular genetic studies suggest that Spionidae fall closest to Poecilochaetidae and Trochochaetidae, and this grouping also clusters with Sabellariidae (Zrzavý et al. 2009). Transcriptomics further support the close relationship of spionids with Sabellariidae (Weigert et al. 2014). Relationships of the genera. The first major effort to develop a cladistic-based family level phylogeny of polychaetes using morphological characters was by Rouse and Fauchald (1997). These authors established a phylogeny that arranged the polychaete families into six basic clades. The Spionidae were grouped with six other families into a clade (or order) termed Spionida. The two families most closely grouped with spionids were Apistobranchidae and Trochochaetidae. Other families assigned to Spionida were Longosomatidae (genus Heterospio), Magelonidae, Poecilochaetidae, and Chaetopteridae. Historically, this group of families has often been treated together in monographic or faunal works (e.g., Day 1967; Hartman 1969; Hartmann-Schröder 1996). Rouse and Pleijel (2001) developed a “polychaete metatree” based on a variety of sources. In that effort, the Spionidae were again placed into Spionida with the following taxa: Apistobranchus, Chaetopteridae, Magelona, Hete­rospio, Poecilochaetus, Trochochaeta, and Uncispionidae. The Spionida was a sister group to Terebellida, which includes the cirratuliform and terebelliform families. The first phylogenetic analysis of the genera Spionidae using morphology was by Sigvaldadóttir et al. (1997). These authors used 25 adult morphological characteristics of the type species of 28 spionid genera as part of a parsimony analysis. Poecilochaetus, Trochochaeta, and Uncispio were used as outgroups to root the analysis. The results bore little relationship to the earlier arrangements of Spionidae suggested by Hannerz and others. Instead, four clades of spionid genera were indicated: (1) Aonidella

and Xandaros; (2) Prionospio complex, Laonice, Spio­ phanes, and Aonides; (3) a large unresolved assemblage of genera including the Polydora complex, Scolelepis, Mal­ acoceros, and Spio; and (4) Atherospio, Pseudatherospio, and Pygospiopsis. The support for these clades was weak, and it is now apparent that the selection of outgroups was unfortunate because of the strong homology of egg and larval morphology of Poecilochaetus and Trochochaeta with several spionid genera. Blake and Arnofsky (1999), as part of a review of the reproduction and larval development of spioniform polychaetes, developed a preliminary phylogenetic analysis of 36 genera of Spionidae, Apistobranchidae, Trochochae­ tidae, Poecilochaetidae, Heterospionidae (= Longosomatidae), and Uncispionidae using 38 characters. Cossura and Cirrophorus were used as outgroups. Among the 38 characters, 14 were reproductive and developmental in nature. The results of this analysis clearly showed that the classification of Spionidae was paraphyletic in that there were two major clades consisting of the subfamily Spioninae and a larger clade consisting of all remaining spionid genera and the genera Heterospio, Poecilochaetus, Trocho­ chaeta, and Uncispio. A minor third clade consisting of the enigmatic genus Pygospiopsis (including Atherospio) was distinct. Apistobranchus behaved as an outgroup in this analysis and most certainly does not belong in the order Spionida. The same may be said of Magelona and Chaetopteridae once other data are considered. An expanded phylogenetic analysis using additional characters and taxa including the magelonids and chaetopterids was later developed as part of a presentation at the Sixth International Polychaete Conference in Curitiba, Brazil, in August 1998 (Blake and Arnofsky 2000). This analysis added further support to the preliminary results of Blake and Arnofsky (1999) and demonstrated that ­reproductive and developmental data, when used together with adult morphology, provide a robust suite of characters to better understand the interrelationships of spioniform polychaetes. Based on Blake and Arnofsky (1999), there is morphological evidence that the Spionidae, including its subfamilies, and the families Uncispionidae, Poecilochaetidae, and Trochochaetidae may be reduced to three clades or subfamily-level categories grouped within a more broadly defined family (Fig.  7.4.1.13  B). The first clade is represented by Pygospiopsis and two related genera, Atheros­ pio and Pseudatherospio (the latter recently synonymized with Pygospiopsis by Blake and Maciolek 2018) for which only a total of eight species are known. The second clade is restricted to the subfamily Spioninae, including Micro­ spio, Pygo­spio, Spio, and the Polydora complex. The remaining taxa constitute a third family-level clade, here



referred to the Nerininae, a family-level taxon established by Söderström (1920). This subfamily includes the former spionid subfamily Laonicinae and the genera Uncispio, Poecilochaetus, and Trochochaeta, all three of which are currently referred to family-level categories. Within the Nerininae, several taxa show close relationships. For example, among the trees generated by Blake and Arnofsky (1999), a distinct subclade always includes Pri­ onospio and its relatives. Dispio, Aonides, and Aonidella typically group together, sometimes with Uncispio and Spiophanes. Poecilochaetus and Trochochaeta invariably exhibit the most derived position in the majority of trees. Spiophanes does not seem to be well resolved among the Nerininae, possibly because its lack of branchiae is negative among the several branchial characters that were used in the analysis. In the taxonomic section that follows this phylogenetic review, the three categories or clades identified by Blake and Arnofsky (1999) together with some miscellaneous genera are used. The genera Heterospio, Uncispio, Poecilochaetus, and Trochochaeta were included in clade 3 in Blake and Arnofsky (1999) and Blake (2006), but need further analysis to be conclusively included within the Spionidae and therefore are treated separately in this handbook. A more recent assessment of Heterospio morphology and COI results suggest a closer affiliation with cirratuliform polychaetes rather than spioniforms (Blake and Maciolek 2019d). Relationship of Spionida families with other polychaetes. One of the early efforts to analyze polychaete phylogeny with molecular gene sequences used 70 18S rDNA sequences using the maximum parsimony and likelihood methods (Bleidorn et al. 2003). Four spionids were included: Aonides oxycephala, Scolelepis squamata, Pygospio elegans, and Polydora ciliata. The four spionids were separated in the same manner as in morphological studies, thereby supporting traditional monophyly evident from morphological studies. The close relationship of the four spionids with sabellids and serpulids evident in the likelihood tree was not discussed. A more robust analysis was completed by Rousset et al. (2007) using more than 250 sequences that focused on two ribosomal genes (18S rDNA and 28S rDNA), histone H3, and one mitochondrial gene (16S rDNA). The 217 taxa that were included in the analysis were all required to have an 18S rDNA sequence and at least two other gene sequences. The results of this analysis did not recover any evidence of monophyly of the Spionida as defined by Rouse and Fauchald (1997). Apistobranchus, Chaetopteridae, Mage­ lona, and Spionidae were in different parts of the tree and with different relationships. Apistobranchus was actually near the base of the tree. The genera of the Spionidae and

7.4.1 Spionidae Grube, 1850 

 41

Poecilochaetus, however, formed a clade that was a sister to one that included genera of the Sabellidae. Struck et al. (2008) presented an analysis of 18S rRNA and 28S rRNA sequences. This study was aimed at addressing the problem of multiple substitutions in nucleotide positions that tend to obliterate signal, a situation called saturation. In the first maximum likelihood tree, in which the possibility of saturation was excluded, genera of Spionidae (Polydora, Prionospio, and Scolelepis), Poecilochaetus, and Trochochaeta were grouped with some species of Sabellidae and Sabellariidae; the same result was obtained when saturation was not excluded. In both examples, Apistobranchus and Chaetopterus were unrelated to the spionids, thus again not supporting a monotypic Spionida sensu Rouse and Fauchald (1999). Zrzavý et al. (2009) developed an analysis that combined morphological and molecular characters to assess annelid phylogeny. They used 93 morphological characters and six genes (18S, 28S, and 16S rRNA, EFI a, H3, and COI). Unfortunately, the results were presented only at the family or genus level. Spionidae, Poecilochaetus, and Tro­ chochaeta formed a clade that grouped with Sabellidae and Sabellariidae in all of the analyses. Apistobranchus, Chaetopterus, and Magelona were in different parts of the trees. The most recent studies using molecular sequences to assemble a phylogeny of annelids were by Struck (2011), Struck et al. (2011), Weigert et al. (2014), and Weigert and Bleidorn (2016). These authors used transcriptomic data encompassing large numbers of amino acid sites (>170,000) from up to 622 genes (Weigert et al. 2014). The aim of these studies was to define an annelid phylogeny that would assist an effort to elucidate ancestral entities and characters at the base of the annelid tree. Struck et al. (2011) resurrected the older categories Errantia and Sedentaria (including Clitellata). The polychaete families in these categories included most of the annelid families. According to Weigert et al. (2014), Errantia and Sedentaria were derived from the basal groups Sipuncula, Amphinomidae, Chaetopteridae, Magelonidae, and Oweniidae. Spionids (with species tested by Weigert et al. (2014) of Pseudopolydora, Malacoceros, and Scolelepis) were within the Sedentaria in a clade with the Sabellariidae as a sister group. The close relationship of spionids and sabella­ riids had earlier been suggested by Struck et al. (2008) and Zrzavý et al. (2009). Although not discussed by any of these authors, a morphological similarity between the larvae of spionids and sabellariids is evident. Planktic larvae of both families develop long serrated provisional chaetae that are held in place by unique grasping cilia was first described for planktic larvae of Polydora (Wilson 1928) and for planktic larvae of Sabellaria (Wilson 1929).

42 

 7.4 Sedentaria: Sabellida/Spionida

Further discussion of these characters and potential relationships between spionids and sabellariids are discussed by Blake (2017). Taxonomy Spionidae Grube, 1850 Type genus: Spio Fabricius, 1785 Diagnosis: Spioniform polychaetes with elongate bodies, with presegmental region consisting of prostomium and peristomium, long segmental region, and postsegmental region or pygidium; anterior trunk segments sometimes larger than posterior segments. Prostomium blunt, bifurcated, pointed, or with frontal horns on the anterior margin; usually extending posteriorly as a caruncle overlying the peristomium and few to many anterior segments; occipital (or nuchal) tentacle present or absent; eyespots present or absent. Nuchal cilia present lateral to caruncle and sometimes extending over several trunk segments. Palps present at postectal corners of prostomium. Dorsal branchiae usually present, rarely absent; ventral branchiae present on one genus. Dorsal transverse rows of cilia present or absent, when present may extend from branchial bases across dorsum; other dorsal cilia present or absent. Parapodia biramous with cirriform or foliose postchaetal lamellae; prechaetal lamella present or absent. Chaetae include simple capillaries, hooded or nonhooded hooks, spines, and sabre chaetae. Pygidium with lobes, cirri, or disclike structure. Remarks: As currently defined, the Spionidae includes approximately 590 species distributed in 38 genera. This definition does not include the closely related genera Poecilochaetus, Trochochaeta, and Uncispio, which are treated separately in this handbook (Blake and Maciolek 2019a,b,c). The following account of the spionid genera divides them into four categories that more or less follow the clades identified by Blake and Arnofsky (1999) and Blake (2006): 1. Subfamily Nerininae Söderström, 1920 (Prionospio complex treated as separate unit). 2. Subfamily Spioninae Söderström, 1920 (Polydora complex treated as a separate unit). 3. Clade: Pygospiopsis, Atherospio, Pseudatherospio. 4. Five monotypic genera having no strong affinity with other spionids: Glandulospio, Glyphochaeta, Spiogalea, Spiophanella, Xandaros.

Nerininae Söderström, 1920 Aonidella Maciolek in López-Jamar, 1989 Type species: Prionospio cirrobranchiata Day, 1961. Three species Diagnosis: Prostomium broad, flattened anteriorly, sometimes weakly notched on the anterior margin (Fig.  7.4.1.13  A, B), lacking posterior caruncle but with posterior margin completely fused with dorsum; paired nuchal organs present extending posteriorly from prostomium on to chaetiger 21; occipital tentacle absent; eyespots present or absent. Peristomium partly fused to chaetiger 1 (Fig. 7.4.1.13 A). Dorsum flat, without dorsal crests. Branchiae from chaetiger 2, limited to anterior chaetigers (Fig. 7.4.1.13 A), 10 to 16 pairs; all simple, apinnate, elongate, separate from notopodial lamellae (Fig. 7.4.1.13 F). Notopodial postchaetal lamellae triangular, similar along body; neuropodial postchaetal lamellae narrower (Fig. 7.4.1.13 F). Interparapodial lateral pouches present or absent. Chaetae of two types: limbate capillaries anteriorly; bi-, tri- or quadridentate hooded hooks (Fig.  7.4.1.13  G) with somewhat perpendicular apical teeth and small secondary hood in posterior noto- and neuropodia. Ventral sabre chaetae absent. Dorsal crests absent. Rows of small holes or pits on dorsum of chaetigers of the branchiate region or adjacent to it (only observable with SEM; Fig. 7.4.1.13 C–E). Pygidium with four to six subequal anal cirri (Fig. 7.4.1.13 J). Remarks: Day (1961) described P. cirrobranchiata from South Africa, and later reported the same species from the continental shelf off North Carolina (Day 1973). This species differs from the typical Prionospio in several characters considered to be of generic importance: (1) the parapodial lamellae do not change in size or shape along the entire length of the body, and are triangular in both rami, rather than broadly oval or foliaceous as is characteristic of Prionospio species; (2) the prostomium is flattened rather than conical and does not continue posteriorly as a caruncle; (3) the angle between the small teeth and main tooth of the hooded hooks is much wider than in the hooks of Pri­ onospio species; (4) ventral sabre chaetae are lacking; and (5) the pygidium has four or more similar cirri, rather than the one long dorsomedial and two shorter ventrolateral cirri typical of Prionospio. Aonidella is similar to Aonides Claparède in the form of the hooded hooks, branchiae, and pygidium. In Aonides, the prostomium is conical, narrow, and tapered anteriorly and posteriorly, whereas in Aon­ idella, the prostomium is very broad, flattened anteriorly,

▸ Fig. 7.4.1.13: Aonidella and Aonides. A–C, Aonidella dayi: A, B, anterior end, dorsal view; C, middle body segments showing dorsal holes; D–E, details of dorsal holes (arrows); F, chaetiger 2, anterior view; G, hooded hook; H–J, Aonides paucibranchiata: H, anterior end, dorsal view; I, hooded hooks; J, pygidium with anal cirri. A, F, G, after Imajima (1992); B–E, originals; H–J, after Blake (1983). Scale bars: A, 500 µm; H, 200 µm; B, C, F, J 100 µm; I, D, 30 µm; E, 15 µm; G, 10 µm. Abbreviations: anC, anal cirri; br, branchiae; neL, neuropodial lamella; noL, notopodial lamella; nuO, nuchal organ; per, peristomium; pr, prostomium.



7.4.1 Spionidae Grube, 1850 

 43

44 

 7.4 Sedentaria: Sabellida/Spionida

almost spadelike (Fig. 7.4.1.13 A, B), and lacks a posterior caruncle; the posterior margin being fused to the dorsum. This genus was first described in an unpublished dissertation by Maciolek (1983), in which she moved Day’s species P. cirrobranchiata to the new genus and described a new species for the material from North Carolina. The names were not formally available but were both used by López-Jamar (1989), who reported the species from the Gulf of Cadiz, citing it as “Aonidella dayi Maciolek, 1983”, acknowledging the dissertation as the basis for the validity of both the genus and the species. He also published an illustrated description of A. dayi based on and extending Maciolek’s original description, thus making the genus and species names available. The authorship was discussed by N.J. Maciolek with two members of the ICZN, who recommended that the authorship should be: “Maciolek in López-Jamar, 1989” and cited the 3rd ICZN 1985, Article 50a. These criteria are intended to prevent a separate person from effectively publishing the work of another person. The same criteria are stated in the 1999 4th ICZN Edition, Article 50.1.1. Maciolek (2000) published a description of A. dayi as Maciolek in López-Jamar, 1989 and designated types. The same authorship was used by Sigvaldadóttir, Mackie and Pleijel (1997) in connection with a cladistic analysis of spionid genera and Greaves et al. (2011) with a new species description. A. dayi has also been reported from Japan by Imajima (1992). Greaves et al. (2011) noted that the nuchal organs of A. insolita (as Laonice) appear as short U-shaped ciliary bands lateral to the fused prostomium and dorsum; they also documented the presence of rows of unexplained holes or pits on the dorsum of chaetigers of the branchiate region or adjacent to it. Meißner et al. (2014) provided details of these rows of dorsal pits for A. cf. dayi. 1. Aonidella cirrobranchiata (Day, 1961). Southwest Africa; Bay of Biscay; shelf and slope depths. 2. Aonidella dayi Maciolek in López-Jamar, 1989. Massachusetts to North Carolina; Mediterranean Sea; Canary Islands; possibly Japan; shelf and slope depths. 3. Aonidella insolita (Greaves, Meißner and Wilson, 2011). Australia, Western Australia, Shark Bay, 393 m. Fide Meißner et al. (2014). Aonides Claparède, 1864 Type species: Aonides auricularis Claparède, 1864 [= A. oxycephala (Sars, 1862)], by monotypy. Synonym: Paranerine Czerniavsky, 1881. Type species: Nerine oxycephala Sars, 1862, by monotypy. Nine species Diagnosis: Prostomium conical, tapered both anteriorly and posteriorly (Figs.  7.4.1.1  E; 7.4.1.13  H); eyespots present or absent; occipital antenna present or absent.

Peristomium poorly developed. Branchiae from chaetiger 2, limited to a variable number of anterior chaetigers (Fig.  7.4.1.13  H), absent posteriorly; all apinnate, cirriform, separated from dorsal lamellae. Bi- or tridentate hooded hooks present in both noto- and neuropodia (Fig.  7.4.1.13  I). Pygidium with two short and three long anal cirri (Fig. 7.4.1.13 J). Remarks: Aonides is a small genus, with a total of nine species known, but several of these have not been reviewed since their original description. Nuchal organs are often not observed but metameric dorsal transverse ciliated bands from chaetiger 1 to the last branchial chaetiger are sometimes present. 1. Aonides californiensis Rioja, 1947. Pacific Ocean, Mexico, Gulf of California. 2. Aonides glandulosa Blake, 1996. Pacific Ocean, central California, shelf depths. 3. Aonides mayaguezensis Foster, 1969. Caribbean Sea, Puerto Rico, shallow subtidal. 4. Aonides nodosetosa Storch, 1966. Indian Ocean, Red Sea. 5. Aonides orensanzi Radashevsky, 2015. Southeast Pacific, Australia, Queensland, Great Barrier Reef, shallow subtidal with coral. 6. Aonides oxycephala (Sars, 1862). Northeast Atlantic, off Norway; also widespread in European waters. 7. Aonides paucibranchiata Southern, 1914. Northeast Atlantic Ocean, Ireland; widespread in European waters. 8. Aonides selvagensis Brito, Nunez and Riera, 2006. Southeast Atlantic Ocean, Selvagem Islands, off West Africa in marine cave, 15 m; also found on seamounts on the eastern flank of the mid-Atlantic Ridge south of the Azores. 9. Aonides trifida Estcourt, 1967. Pacific Ocean, New Zealand. Australospio Blake and Kudenov, 1978 Type species: Australospio trifida Blake and Kudenov, 1978 by monotypy. Two species Diagnosis: Prostomium with both anterior pointed projection and subdistal lateral horns; caruncle reduced, short, occipital tentacle absent. Peristomium reduced, with poorly developed lateral wings. Proboscis eversible, saclike. Branchiae from chaetiger 1, continuing almost to posterior end, basally fused with notopodial lamellae in anterior chaetigers, becoming nearly free posteriorly. Notopodial lamellae well-developed, entire; neuropodial lamellae well-developed, tending toward bilobate condition in middle chaetigers. Notochaetae all capillaries. Neuropodial chaetae include capillaries, hooded hooks and inferior sabrelike chaetae. Nature of pygidium unknown.



7.4.1 Spionidae Grube, 1850 

 45

Remarks: Australospio is closely allied to Scolelepis Blainville, Aonides Claparède, and Dispio Hartman in having a pointed prostomium and branchiae. Australospio differs in also bearing lateral horns on the prostomium, a characteristic typical of Malacoceros Quatrefages, Rhynchospio Hartman, and Scolecolepides Ehlers; however, in the last three genera, the prostomium is not anteriorly pointed. The branchiae begin on chaetiger 1 in both Australospio and Dispio and on chaetiger 2 in Aonides and Scolelepis. The notopodial lamellae are at least basally fused to the branchiae in Dispio, Australospio, and Scolelepis, whereas they are completely free in Aonides. The hooded hooks are bidentate in Austra­ lospio, bidentate to tridentate in Aonides, unidentate in adult Dispio species, and range from unidentate to multidentate in species of Scolelepis. Two species are known. 1. Australospio mokapu Ward, 1981. Pacific Ocean, Hawaii, Oahu, shallow water. 2. Australospio trifida Blake and Kudenov, 1978. Southeast Australia. Dispio Hartman, 1951 Type species: Dispio uncinata Hartman, 1951, by monotypy. 15 species Diagnosis: Prostomium fusiform pointed anteriorly, with short caruncle extending posteriorly (Fig. 7.4.1.14  A); eyespots present or absent. Peristomium moderately developed, forming low lateral wings (Fig. 7.4.1.14  A). Anterior parapodial lamellae lobed (Fig. 7.4.1.14 B) or entire. Prechaetal notopodial and neuropodial lobes present or absent. Branchiae from chaetiger 1, fused to notopodial lamellae for half or more of length (Fig. 7.4.1.14 A, B, E). Accessory branchiae present along posterior margin of notopodia in middle and posterior segments (Fig. 7.4.1.14 E). Notochaetae capillaries; neurochaetae include capillaries, hooded hooks (Fig.  7.4.1.14  C, D), and sabre chaetae. Pygidium with midventral flap and prominent anal cirri. Remarks: The type species, D. uncinata Hartman, was originally described from the Gulf of Mexico (Hartman 1951). The species has also been recorded from intertidal and shallow subtidal habitats in Southern California in coarse to fine sands (Hartman 1969), but some of these records refer to additional species (Delgado-Blas and Díaz-Díaz 2016). A total of 15 species have been described, but given the widespread reports of the type species, D. uncinata, it is likely that additional species are actually present. 1. Dispio anauncinata Delgado-Blas and Díaz-Díaz, 2016. Northeast Pacific, Southern California. 2. Dispio bescanzae Delgado-Blas and Díaz-Díaz, 2016. Atlantic coast of Venezuela. 3. Dispio brachychaeta Blake, 1983. Argentina. 4. Dispio elegans Delgado-Blas, Diaz-Diaz, and Vietez, 2018. Iberian Peninsula.

Fig. 7.4.1.14: Dispio uncinata. A, anterior end, dorsal view; B, chaetiger 1, anterior view; C, neuropodial hooded hooks and capillaries from middle neuropodium; D, hooded hook and capillary from posterior neuropodium; E, middle parapodium, anterior view. All after Hartman (1951). Not to scale. Abbreviations: acBr, accessory branchiae; br, branchia; car, caruncle; neP, neuropodium; noP, notopodium; pa, palp; per, peristomium; pr, prostomium.

5. Dispio glabrilamellata Blake and Kudenov, 1978. Australia, New South Wales. 6. Dispio latilamella Williams, 2007. Philippines. 7. Dispio lenislamellata Delgado-Blas and Díaz-Díaz, 2016. Northeast Pacific, Southern California. 8. Dispio longibranchiata Delgado-Blas and Díaz-Díaz, 2016. North Pacific, Southern California. 9. Dispio magna (Day, 1955). South Africa. 10. Dispio maroroi Gibbs, 1971. Western Pacific, Solomon Islands. 11. Dispio oculata Imajima, 1990. Sea of Japan, Wakasa Bay, Honshu, 5 m. 12. Dispio panamensis Delgado-Blas and Díaz-Díaz, 2016. Northeast Pacific, Panama. 13. Dispio remanei Friedrich, 1956. Southwest Atlantic Ocean, South America.

46 

 7.4 Sedentaria: Sabellida/Spionida

14. Dispio schusterae Friedrich, 1956. Pacific Ocean, El Salvador. 15. Dispio uncinata Hartman, 1951. Gulf of Mexico; Caribbean Sea; some records from Pacific Ocean and Mediterranean Sea may be other species. Laonice Malmgren, 1867 Type species: Nerine cirrata M. Sars, 1851, designated by Malmgren, 1867. 41 species Synonyms: Mandane Kinberg, 1866. Type species: Mandane brevicornis Kinberg, 1866. Fide Sikorski 2011. Spionides Webster and Benedict, 1887. Type species: Spi­ onides cirratus Webster and Benedict, 1887. Diagnosis: Prostomium anteriorly rounded (Fig.  7.4.1.15  A, B) to slightly incised (Fig.  7.4.1.15  D), or bell-shaped (Fig. 7.4.1.15 C); nuchal organ(s) extending posteriorly for variable number of chaetigers (Fig. 7.4.1.15 A–D); occipital antenna usually present (Fig.  7.4.1.15  A–D). Peristomium with reduced lateral wings absent or poorly developed and separated from the prostomium and moderately developed (Fig. 7.4.1.15 B–D) or, in other species, enlarged and fused to anterior margin of prostomium (Fig.  7.4.1.15  A). Branchiae from chaetiger 2, apinnate (Figs.  7.4.1.2  C; 7.4.1.16 A, B, E–F) or with digitiform pinnules, separated from or partially fused to notopodial postchaetal lamellae, continuing posteriorly for at least one-half of body length; noto- and neuropodial postchaetal lamellae large, expanded in anterior chaetigers (Figs. 7.4.1.2 C; 7.4.1.16 A, B, E), reduced posteriorly (Fig. 7.4.1.16 F). Interparapodial lateral pouches present (Fig.  7.4.1.15  C). Notopodia with capillaries; notopodial hooded hooks present or absent; neurochaetae include capillaries, hooded hooks, and sabre chaetae; hooks with main fang and one to several apical teeth (Fig.  7.4.1.16  C, D, G–I). Pygidium with anal cirri. Remarks: Species of Laonice are typically larger and more robust than species of Prionospio and are characterized by having an occipital antenna, branchiae from chaetiger 2, and the presence of interparapodial or genital pouches. One species, L. dayianum Sikorski, 1997, has been described as lacking an occipital tentacle. At present, 41  species of Laonice are recognized (Read and Fauchald 2017). Several recent articles have greatly improved our knowledge of this genus: Greaves et al. (2011); Sikorski (2011); Sikorski and Pavlova (2016, 2018); Bogantes et al. (2018). 1. Laonice annenkowae Zachs, 1925. Arctic Ocean, off Murmansk. 2. Laonice antarcticae Hartman, 1953. Southeast Atlantic, off Uruguay and Argentina; Antarctic Peninsula.

Fig. 7.4.1.15: Laonice species. A, L. cirrata, anterior end, dorsal view; B, L. nuchala, anterior end, dorsal view; C, L. antarcticae, anterior end, dorsal view; D, L. weddellia, anterior end, dorsal view. A, B, after Blake (1996); C, D, after Blake (1983). Scale bars: A, B, D, 500 µm; C, 150 µm. Abbreviations: br, branchia; car, caruncle; ipGP, interparapodial genital pouch; neP, neuropodium; noL, notopodial lamella; nuO, nuchal organ; ocAn, occipital antenna; per, peristomium; pr, prostomium.

3. Laonice antipoda Sikorski, 2011. South Africa. 4. Laonice appelloefi Söderström, 1920. Off Norway; European waters. [Laonice maciolekae Aguirrezabalaga and Ceberio, 2005] Fide Meißner et al. 2014. 5. Laonice asaccata Sigvaldadóttir and Desbruyères, 2003. Mid-Atlantic Ridge: hydrothermal vent fields of Lucky Strike, Longatchev, and Rainbow, 1600–3047 m. 6. Laonice bahusiensis Söderström, 1920. Off Sweden; widespread in the Arctic Ocean. 7. Laonice bassensis Blake and Kudenov, 1978. Australia, Victoria, Bass Strait, shelf depths. 8. Laonice blakei Sikorsky and Jirkov, In: Sikorsky, Jirkov and Tsetlin, 1988. Arctic Ocean, slope depths, 960– 2510 m; Norwegian and Greenland Seas, 930–3429 m (Sikorski et al. 2017). 9. Laonice branchiata Nonato, Bolivar and Lana, 1986. Off Brazil, 5–39 m. 10. Laonice brevicornis (Kinberg, 1966). Off Brazil; Caribbean Sea, Puerto Rico, shelf depths. Fide Sikorski 2011. [Laonice aperata Radashevsky and Lana, 2009] Fide Sikorski 2011.



7.4.1 Spionidae Grube, 1850 

 47

Fig. 7.4.1.16: Laonice species. A–D, L. nuchala: A, chaetiger 3, anterior view; B, posterior chaetiger, anterior view; C, hooded hook and capillary; D, detail of hooded hook. E–I, L. weddellia: E, chaetiger 5, anterior view; F, chaetiger 100, anterior view; G–I, hooded hooks in different views. A–D, after Blake 1996; E–I, after Blake (1983). Scale bars: A, B, E–F, 500 µm; C, D, 50 µm; G–I, 20 µm. Abbreviations: br, branchiae; neL, neuropodial lamella; neP, neuropodium; noL, notopodial lamella; nuO.

[Laonice petersenae Radashevsky and Lana, 2009] Fide Sikorski 2011. 11. Laonice brevicristata Pillai, 1961. Sri Lanka. 12. Laonice cirrata (M. Sars, 1851). Type-locality off Norway; widely reported elsewhere and with several subspecies. [Laonice pugettensis Banse and Hobson, 1968] Fide Sikorski 2003. 13. Laonice costaricensis Sikorski and Pavlova, 2018. Costa Rica, Cocos Island. 14. Laonice cricketae Sikorski and Pavlova, 2016. Off West Africa, Guinea Bay, 380 m. 15. Laonice dayianum Sikorski, 1997. Western North Atlantic, off North Carolina, 200 m. 16. Laonice foliata (Moore, 1923). Pacific Ocean, California, Monterey Bay. 17. Laonice galatheae Sikorski and Pavlova, 2016. Off West Africa, 46–200 m. 18. Laonice hermaphroditica Blake and Kudenov, 1978. Australia, Queensland, Moreton Bay. 19. Laonice japonica (Moore, 1907). Japan, off Honshu Island, 112 m. 20. Laonice junoyi Aguirrezabalaga and Ceberio, 2005. Eastern Atlantic, Bay of Biscay, Capbreton Canyon, 984–1029 m.

21. Laonice lemniscata Greaves, Meißner and Wilson, 2011. Australia, Western Australia, 193 m. 22. Laonice magnacristata Maciolek, 2000. Western North Atlantic, 2900 m; Northeast Atlantic, Whittard Canyon, 1000–3356 m (Sikorski et al. 2017). 23. Laonice natae Sikorski, Gunton, and Pavlova, 2017. Northeast Atlantic, abyssal depths Whittard Canyon, west of Bay of Biscay, 3373–3429 m. 24. Laonice norgensis Sikorski, 2003. Off Norway; North Sea; 106–298 m. 25. Laonice nuchala Blake, 1996. Pacific Ocean, California, 90–395 m. 26. Laonice olgae Sikorski and Pavlova, 2016. Off South Africa, 272 m. 27. Laonice papillibranchiae Ward, 1981. Pacific Ocean, Hawaii, off Oahu Island, 5.5 m, sand. 28. Laonice parvabranchiata Radashevsky and Lana, 2009. Off Brazil, 206–225 m. 29. Laonice pectinata Greaves, Meißner and Wilson, 2011. Australia, Western Australia, 99–1440 m. 30. Laonice pinnulata Radashevsky and Lana, 2009. Pacific Ocean, off Costa Rica, shallow subtidal. 31. Laonice plumisetosa Bogantes, Halanych and Meissner, 2018. Norwegian Sea, off Iceland, 1369–2402 m.

48 

 7.4 Sedentaria: Sabellida/Spionida

32. Laonice quadridentata Blake and Kudenov, 1978. Australia, Victoria, Port Phillip Bay. Note: Sikorsky and Pavlova (2016) referred L. quadridentata to synonymy with L. brevicornis with little or no justification. There are no records of the species between its original Southeast Australia location and type locality of L. brevicornis in Brazil. 33. Laonice rasmusseni Sikorski and Pavlova, 2018. Off Georgia, SE United States, 137 m. 34. Laonice rossica Sikorski, 2003. Northeast Pacific, off Kamchatka. 35. Laonice sacculata (Moore, 1923). Pacific Ocean, Monterey Bay, California. 36. Laonice sarsi Söderström, 1920. North Sea to West Barents Sea; Norwegian coast; Northeast Scotland; 25–405 m. 37. Laonice shamrockensis Sikorski, 2003. Northeast Atlantic, Shamrock Canyon, 1700 m. 38. Laonice sinica Sikorski and Wu, 1998. Yellow Sea, China. 39. Laonice vieitezi López, 2011. Antarctica, Bellingshausen Sea, 605 m. 40. Laonice weddellia Hartman, 1978. Southern Ocean and Antarctica, deep water. 41. Laonice whittardensis Sikorski, Gunton, and Pavlova, 2017. Northeast Atlantic, abyssal depths Whittard Canyon, west of Bay of Biscay, 3511–3661 m. Lindaspio Blake and Maciolek, 1992 Type species. Lindaspio dibranchiata Blake and ­Maciolek, 1992. Three species Diagnosis: Prostomium incised, developed into two frontal lobes or weak horns (Fig. 7.4.1.17 A); caruncle short; occipital tentacle lacking. Peristomium lacking lateral wings. Dorsal branchiae from chaetiger 2 (Fig. 7.4.1.17 F), ventral branchiae from an anterior segment (Fig. 7.4.1.17 G); branchiae closely associated with parapodial lamellae (Fig.  7.4.1.17  F, G), continuing to posterior end. Chaetiger 1 reduced, with notopodia reduced to single lamella lacking notochaetae; notopodia and neuropodia with capillaries and hooded hooks (Fig.  7.4.1.17  D, E); some anterior notopodia with rosettes or clusters of heavy pointed spines (Fig. 7.4.1.17 B); anterior neuropodia with fascicles of heavy spines (Fig.  7.4.1.17 C). Interparapodial pouches absent. Pygidium simple, conical, lacking cirri. Remarks: Lindaspio was originally described with two species from Eastern Pacific hydrothermal vents (Blake and Maciolek 1992). The genus is closely related to species belonging to the nearshore genus Scolecolepides as revised by Maciolek (1984b). Both genera have anterior chaetigers with modified neuropodial spines and with the prostomium anteriorly bifurcated, sometimes expanded into frontal horns. Lindaspio, however, has branchiae beginning

Fig. 7.4.1.17: Lindaspio dibranchiata. A, anterior end, dorsal view; B, notopodial spines from anterior chaetiger; C, modified neuropodial spines, unworn and worn; D, neuropodial hooded hooks; E, notopodial hooded hooks; F, anterior parapodium, anterior view; G, posterior parapodium posterior view. All after Blake and Maciolek (1992). Scale bars: A, 2 mm; B, 100 µm; C, 20 µm; D, E, 10 µm; F, G, 500 µm. Abbreviations: br, branchia; neP, neuropodium; noL, notopodial lamella; noP, notopodium; pa, palp; pr, prostomium.

from chaetiger 2 instead of chaetiger 1 and, uniquely, has ventral branchiae in addition to dorsal branchiae. Lindaspio species also have notopodial spines in some anterior chaetigers. The two original species, L. dibranchi­ ata and L. southwardorum are from hydrothermal vents along the Pacific continental margin (Blake and Maciolek 1992). Lindaspio sebastiena is from offshore Congo, West Africa, in an area of active oil and gas production (Bellan et al. 2003). L. southwardorum is approximately 16 cm long and as such is one of the largest spionids ever collected. 1. Lindaspio dibranchiata Blake and Maciolek, 1992. Pacific Ocean, Gulf of California, Guaymas Basin, Southern Trough hydrothermal mounds, ~2000 m. 2. Lindaspio sebastiena Bellan, Dauvin and Laubier, 2003. Atlantic Ocean, West Africa, Republic of Congo, 150 m. 3. Lindaspio southwardorum Blake and Maciolek, 1992. Pacific Ocean, Juan de Fuca Ridge, Middle Valley Segment, hydrothermal vents, 2425 m.



Malacoceros Quatrefages, 1843 Type species: Spio vulgaris Johnson, 1827:335, designated by Pettibone, 1963:98. 16 species Synonyms: Colobranchus Schmarda, 1861:66. Type species: C. tetracerus Schmarda, by monotypy. Uncinia Quatrefages, 1866:439. Type species: Colobranchus ciliatus Keferstein, 1862:439, by monotypy (= C. tetracerus Schmarda, 1861). Scolecolepis Malmgren, 1867:90. Type species: Spio vul­ garis Johnson, 1827:335, by original designation. Diagnosis: Prostomium broad anteriorly, triangular (Fig.  7.4.1.1  B–D), T- or bell-shaped (Fig.  7.4.1.18  A); frontal horns typically present (Figs. 7.4.1.1 B–D; 7.4.1.3 A; 7.4.1.18  A); occipital antenna absent. Eyespots present in pairs (Fig. 7.4.1.1 D), irregularly arranged or eyespots absent. Caruncle entire, trilobed, or buttonlike. Nuchal organs as two small ciliated grooves posterolateral to the caruncle. Palps ventrally grooved. Peristomium reduced to moderately developed. Branchiae from chaetiger 1 (Figs. 7.4.1.1 B;

Fig. 7.4.1.18: Malacoceros indicus. A, anterior end, dorsal view; B, sabre chaeta; C, hooded hook; D, chaetiger 15, anterior view; E, posterior parapodium, posterior view. All after Blake (1996). Scale bars: A, 50 µm; B, C, 20 µm; D, E, 200 µm. Abbreviations: br, branchiae; neL, neuropodial lamella; noL, notopodial lamella, per, peristomium; postL, postchaetal lamella; preL, prechaetal lamella; pr, prostomium.

7.4.1 Spionidae Grube, 1850 

 49

7.4.1.3 A; 7.4.1.18 A) to end or near end of body; free from or basally fused to notopodial lamellae (Fig. 7.4.1.18 D–E). Transverse ciliated bands across the dorsum present. Chaetae include simple capillaries, scalpel chaetae, neuropodial uni-, bi-, tri-, or quadridentate hooded hooks (Fig.  7.4.1.18  C). Sabre chaetae present (Fig.  7.4.1.18  B). Pygidium with 2 to 30 anal cirri (Fig. 7.4.1.1 B) or with two anal cirri and a rounded or spatuliform dorsal lobe. Remarks: Malacoceros is a companion genus to Rhynchos­ pio, having frontal horns, but with branchiae from chaetiger 1 instead of chaetiger 2. The most widely reported species is M. indicus, originally described by Fauvel (1928) from the Indian Ocean, but currently reported from locations as distant as the Caribbean, Chile, Australia, and Japan. Foster (1971) redescribed the syntype of M. indicus; it was also examined by Delgado-Blas and Salazar-Silva (2011). Intraspecific variability is acknowledged to be large. Foster (1971) found differences between the original description and the co-syntype, namely, in the number of teeth on the hooded hooks and the start of the branchiae. Whereas Fauvel (1928) described the hooks as bidentate, Foster found that the syntype actually had tri- and quadridentate neuropodial hooded hooks, with either two or three very small apical teeth in a single row above the main fang; she concluded that her specimens from the Caribbean were the same species as Fauvel’s from India, allowing for variability in origin of the hooks. Delgado-Blas and Salazar-Siva (2011), however, thought that differences between Caribbean specimens and the syntype, for example, in the shape of the parapodial lamellae, pointed to the Caribbean specimens belonging to a new species, although they did not describe one in that article. An extensive discussion about intraspecific variability of M. indicus was also provided by Meißner and Götting (2015). Moreover, the latter authors also provided first information on molecular markers for M. indicus collected at Lizard Island, Great Barrier Reef, Australia, and expressed the urgent need for integrative taxonomic studies of this species. Sixteen species are known. 1. Malacoceros cariacoensis Delgado-Blas and Díaz-Díaz, 2010. Caribbean Sea, Venezuela. 2. Malacoceros derjugini (Ushakov, 1948). Arctic Ocean, Murmansk Coast. 3. Malacoceros divisus Hutchings and Rainer, 1979. Australia, New South Wales, Careel Bay. 4. Malacoceros fuliginosus (Claparède, 1870). Northeast Atlantic and Mediterranean Sea, widespread in European seas. 5. Malacoceros girardi Quatrefages, 1843. Northeast Atlantic and Mediterranean Sea. 6. Malacoceros indicus (Fauvel, 1928). India, type locality Indian Ocean: Gulf of Mannar (Krusadai Island, India); also reported from shallow water to shelf depths: Australia (Queensland; New South Wales);

50 

7.

8.

9. 10. 11. 12.

13.

14. 15. 16.

 7.4 Sedentaria: Sabellida/Spionida

New Caledonia; Philippines (Aklan province); Japan; Southwest Africa; Caribbean Sea; Chile; USA (Southern California; Massachusetts to Georgia); Costa Rica (Golfo de Nicoya). [Malacoceros punctata (Hartman, 1961)] fide Blake 1996. Malacoceros jennicus Graff, Blake and Wishner, 2008. Caribbean Sea, Kick’em Jenny, a hydrothermally active submarine volcano in the Lesser Antilles, 262 m. Malacoceros jirkovi Sikorski, 1992. Norwegian Sea, 140 m; Northeast Atlantic Ocean, Great Meteor Seamount, 288 m. Malacoceros laevicornis (Rathke, 1837). Black Sea, Crimea. Malacoceros longiseta Delgado-Blas and Díaz-Díaz, 2013. Caribbean Sea, Venezuela. Malacoceros reductus Blake and Kudenov, 1978. Australia, New South Wales, intertidal. Malacoceros samurai Hourdez, Desbruyères and Laubier, 2006. Hydrothermal vents, southern East Pacific Rise at 17°25′S, depth not stated. Malacoceros tetracerus (Schmarda, 1861). Northeast Atlantic and Mediterranean Sea, widespread in European seas. Malacoceros tripartitus Blake and Kudenov, 1978. Australia, Victoria, Port Phillip Bay. Malacoceros vanderhorsti (Augener, 1927). Caribbean Sea; Curacao (type locality). Malacoceros vulgaris Quatrefages, 1843. North Sea; Mediterranean Sea.

Marenzelleria Mesnil, 1896. Emended Augener 1913 and Maciolek 1984b Type species: Marenzelleria wireni Augener, 1913 by subsequent designation. Five species Diagnosis: Prostomium bell-shaped, broadly rounded or incised anteriorly (Fig.  7.4.1.19  A, G); occipital tentacle absent; eyespots present or absent. Peristomium well developed, distinctly separated from chaetiger  1 (Fig.  7.4.1.19  A, G). Branchiae from chaetiger 1 basally fused to large notopodial lamellae (Fig.  7.4.1.19  A, B), continuing for one-half body length; posterior podial lamellae reduced (Fig.  7.4.1.19  C, D). Anterior chaetae all capillaries; neuropodial and notopodial hooded hooks present posteriorly; hooks bi- or tridentate (Fig. 7.4.1.19 F). Ventral sabre chaetae present. Pygidium with a ring of anal cirri (Fig. 7.4.1.19 E). Remarks: Marenzelleria was redescribed by Maciolek (1984b) and revised by Sikorski and Bick (2004). At the same time as Maciolek’s article, species of the genus were discovered in and around the North Sea and Baltic Sea as

Fig. 7.4.1.19: Marenzelleria. A–F, M. viridis: A, anterior end, dorsal view; B, chaetiger 55, anterior view; C, chaetiger 100, anterior view; D, chaetiger 190, anterior view; E, posterior end, dorsal view; F, neuropodial hooded hook. G, M. wireni, anterior end, dorsal view. All after Maciolek (1984b). Scale bars: A, 500 µm; B, 100 µm; C, D; 250 µm; E, G, 200 µm; F, 20 µm. Abbreviations: anC, anal cirrus; br, branchiae; neL, neuropodial lamella; noL, notopodial lamella; nuO, nuchal organ; per, peristomium; pr, prostomium.

introduced species that began to establish dense populations. These discoveries led to considerable research on the systematics and ecology of these alien species. At present, at least two species occur in both North American and European waters. The tolerance of some species to low salinity may have contributed to their dispersal, likely via ballast water. See details on Marenzelleria in the Introduced species section. At present, five species, all from the northern hemisphere, are known. 1. Marenzelleria arctia (Chamberlin, 1920). Alaskan Arctic; Kamchatka. 2. Marenzelleria bastropi Bick, 2005b. Western North Atlantic Ocean, North Carolina. 3. Marenzelleria neglecta Sikorski and Bick, 2004. North Atlantic: Baltic Sea and North Sea; North Carolina to Georgia; California, San Francisco Bay delta system; Sea of Azov and Black Sea (Syomin et al. 2017). 4. Marenzelleria viridis (Verrill, 1873). Widespread in the North Atlantic: Nova Scotia to Delaware; Scotland, North Sea. 5. Marenzelleria wireni Augener, 1913. Widespread in Arctic seas: Spitsbergen, Barents Sea, White Sea, Kara Sea, Chukchi Sea, Beaufort Sea; low water to 55 m.



Rhynchospio Hartman, 1936 Type species: Rhynchospio arenincola Hartman, 1936, by monotypy. 11 species Diagnosis: Prostomium with frontal horns (Fig. 7.4.1.20 A), caruncle variously developed; eyespots present or absent; occipital antenna absent. Branchiae from chaetiger 2 free from dorsal lamellae or only fused basally (Fig. 7.4.1.20 A–C). Notochaetae all capillaries. Neurochaetae include capillaries, hooded hooks (Fig. 7.4.1.20 D), and sabre chaetae. Pygidium with cirri or lobes. Remarks: Rhynchospio has been considered both as a genus (Hartman 1936, 1959, 1969; Day 1967; Fauchald 1977; Blake and Kudenov 1978; Imajima 1991) and as a subgenus of Malacoceros (Pettibone 1963; Foster 1971). Rhynchospio is considered as a full genus here because Malacoceros and Rhynchospio form a generic pair that is analogous to Dispio/Scolelepis and Spio/Microspio in having branchiae first present from the first/second chaetiger. Recent studies by Radashevsky (2007, 2015) and Radashevsky et al. (2014, 2016a) reported on new details of adult morphology, reproduction, and larval brooding that further justify the separation of the two genera; in addition, several species considered as synonyms or subspecies of other species have been redefined. Eleven species are known. 1. Rhynchospio arenincola Hartman, 1936. California. 2. Rhynchospio asiatica Chlebovitsch, 1959. Northwest Pacific, Kurile Islands. 3. Rhynchospio australiana Blake and Kudenov, 1978. Australia, Western Australia, Perth. 4. Rhynchospio darwini Radashevsky, 2015. Australia, Northern Territory, Darwin; Queensland, Great Barrier Reef. 5. Rhynchospio foliosa Imajima, 1991. Japan, Hokkaido Island.

Fig. 7.4.1.20: Rhynchospio arenincola. A, anterior end, dorsal view; B, anterior parapodium, anterior view; C, posterior parapodium, anterior view; D, hooded hook. All after Imajima (1991) (as R. glutaea). Not to scale. Abbreviations: br, branchiae; neL, neuropodial lamella; noL, notopodial lamella; per, peristomium; pr, prostomium.

7.4.1 Spionidae Grube, 1850 

 51

6. Rhynchospio glutaea (Ehlers, 1897). Southeast Pacific Ocean, Chile, Strait of Magellan. 7. Rhynchospio glycera Blake and Kudenov, 1978. Australia, New South Wales. 8. Rhynchospio inflata (Foster, 1971). Caribbean Sea, Bahamas, Bimini. 9. Rhynchospio mzansi Simon, Williams and Henninger, 2017. South Africa. 10. Rhynchospio nhatrangi Radashevsky, 2007. South China Sea, Vietnam, Bay of Nha Trang. 11. Rhynchospio tuberculata Imajima, 1991. Japan, Honshu Island, Sagami Bay. Scolecolepides Ehlers, 1907 Type species: Scolecolepides benhami Ehlers, 1907, by monotypy. Five species Diagnosis: Prostomium with frontal or lateral horns (Fig.  7.4.1.21  A). Branchiae present from chaetiger 1

Fig. 7.4.1.21: Scolecolepides uncinatus. A, anterior end, dorsal view; B, chaetiger 1, anterior view; C, chaetiger 10, anterior view; D, chaetiger 100, anterior view; E, anterior capillary notochaeta from chaetiger 5; F–H, thick neuropodial spines, chaetiger 12; I, J, neuropodial hooded hooks. All after Blake (1983). Scale bars: A, 1 mm; B–D, 500 µm; E–J, 50 µm. Abbreviations: br, branchiae; neL, neuropodial lamella; neP, neuropodium; noL, notopodial lamella; nuO, nuchal organ; per, peristomium; pr, prostomium.

52 

 7.4 Sedentaria: Sabellida/Spionida

(Fig. 7.4.1.21 A, B, limited to anterior chaetigers or continuing throughout the body; branchiae basally fused to dorsal lamellae (Fig. 7.4.1.21 B, C). Notopodial lamellae enlarged, elongate anteriorly, tapering apically (Fig.  7.4.1.21  B, C), smaller posteriorly (Fig.  7.4.1.21  D). Anterior chaetae mostly capillary, with ventral acicular spines present (Fig. 7.4.1.21 F–H). Uni- or bidentate hooded hooks present in both neuropodia and notopodia (Fig. 7.4.1.21 I, J). Pygidium with cirri surrounding anus. Remarks: Five species are currently assigned to Scoleco­ lepides; four are shallow-water species from the southern hemisphere; one upper slope species was described from off North Carolina. The genus was redefined by Maciolek (1984), who referred some species to Marenzelleria. Five species are known. 1. Scolecolepides aciculatus Blake and Kudenov, 1978. Australia, Victoria, Port Phillip Bay, and Western Port Bay. 2. Scolecolepides benhami Ehlers, 1907. New Zealand. 3. Scolecolepides carunculatus Maciolek, 1984b. Western North Atlantic Ocean, North Carolina, off Cape Lookout, 650 m. 4. Scolecolepides freemani Mitchell and Edwards, 1988. New Zealand. 5. Scolecolepides uncinatus Blake, 1983. Southeast Atlantic Ocean, Argentina, intertidal. Scolelepis Blainville, 1828 Type species: Lumbricus squamata Müller, 1806, by monotypy. 84 species Synonyms: Aonis sensu Audouin and Milne Edwards, 1833 [not Savigny, 1822]. Asetocalamyzas Tzetlin, 1985 (dwarf male of a spionid, not a parasitic syllid as originally described). Nerine Johnston, 1838. Type species: Nerine foliosa (Audouin and Milne Edwards, 1834). Nerinides Mesnil, 1896. Type species: Nerinides longi­ rostris (Quatrefages, 1943). Nerinopsis Ehlers, 1913. Type species: Nerinopsis hys­ tricosa Ehlers, 1913, indeterminate planktic larva of Scolelepis. Pseudomalacoceros Czerniavsky, 1881. Type species: Malacoceros longirostris Quatrefages, 1843. Pseudonerine Augener, 1926. Type species: Pseudonerine antipoda Augener, 1926. Scolecolepis Malmgren, 1867 (alternate spelling for Scolelepis, Blainville, 1828). Diagnosis: Prostomium pointed anteriorly (Figs. 7.4.1.1 H; 7.4.1.2 A; 7.4.1.22 A, L, M; 7.4.1.23 A, F), extending posteriorly as narrow caruncle; caruncle attached (Fig. 7.4.1.1 H) or

detached posteriorly (Fig. 7.4.1.22 M, N); occipital antenna present (Figs. 7.4.1.22 L; 7.4.1.23 A, F) or absent (Fig. 7.4.1.22 A, M, N). Peristomium well developed (Fig.  7.4.1.22  A, L–N), lateral wings present or absent; palps without ciliated groove, often with thickened basal sheath (Fig. 7.4.1.23 D). Branchiae from chaetiger 2 (Fig.  7.4.1.22  A, L–N), to near posterior end; anterior branchiae either completely fused to notopodial lamellae (Figs. 7.4.1.22 M, N; 7.4.1.23 A, B, F), partially fused (Fig.  7.4.1.22  A–C, L), or entirely free; posterior branchiae usually free from notopodial lamellae (Fig.  7.4.1.23  C); accessory branchiae present or absent. Anterior chaetae limbate capillaries (Fig.  7.4.1.22  G–K); neuropodial hooded hooks present; notopodial hooded hooks present or absent; hooks either falcate with zero to two small apical teeth and straight or only weakly curved shaft (Fig. 7.4.1.22 O–Q) (subgenus Scolelepis); or multidentate with large main fang, several apical teeth, and strongly curved shaft (Fig. 7.4.1.23 G, E) (subgenus Parascolelepis). Pygidium an oval disc (Fig. 7.4.1.22 R) or multilobed. Remarks: Scolelepis is a large genus with more than 80 known species; it seems to be limited to inshore and continental shelf depths, not having been reported from the deep sea. The most important recent revision of the genus was by Maciolek (1987), who established the two currently recognized subgenera, reviewed all of the thenknown species, and described three new species. More recently, Sikorski and Pavlova (2015) summarized and listed the known species and subspecies of Scolelepis by subgenus. The most widely reported species is S. squamata, which was originally described from Denmark, but this is largely because several local species were synonymized with S. squamata by Pettibone (1963). Delgado-Blas (2006) reviewed and redescribed several of these and removed them from synonymy; he also described three new species from the Caribbean. Surugiu (2016) has provided the most complete redescription, including the variability of S. squamata from European waters. The following list of 84 species is taken from Maciolek (1987), Sikorski and Pavlova (2015), and Read and Fauchald (2017). Named subspecies are not included. Subgenus Scolelepis (Parascolelepis) Maciolek, 1987 1. Scolelepis (Parascolelepis) bousfieldi Pettibone, 1963. Western North Atlantic, Canada to North Carolina. 2. Scolelepis (Parascolelepis) burkovskii Sikorski, 1994. Barents Sea, shallow water. 3. Scolelepis (Parascolelepis) carrascoi Maciolek, 1986. Replacement name for S. blakei Carrasco, 1981, homonym of S. blakei Hartmann-Schröder, 1980. Chile. 4. Scolelepis (Parascolelepis) geniculata Imajima, 1992. Japan.



7.4.1 Spionidae Grube, 1850 

 53

Fig. 7.4.1.22: Scolelepis (Scolelepis) species. A–K, S. chilensis: A, anterior end, dorsal view; B, chaetiger 30, anterior view; C, posterior chaetiger, anterior view; D–F, neuropodial hooded hooks; G, H, capillary notochaetae, anterior row, anterior chaetiger; I, inset of H (not to scale); J, K, capillary notochaetae, posterior row, anterior chaetiger. L, S. eltaninae, anterior end, dorsal view. M, S. pettiboneae, anterior end, dorsal view; N–R, S. foliosa: N, anterior end, dorsal view; O–Q, neuropodial hooded hooks; R, posterior end, dorsal view. A–L, after Blake (1983); M–R, after Maciolek (1987). Scale bars: A, 500 µm; B, C, 300 µm; D, G–K, R, 50 µm; L–N, 1 mm; E–F, 20 µm; O–Q, 10 µm. Abbreviations: br, branchia; neL, neuropodial lamella; neP, neuropodium; noL, notopodial lamella; noP, notopodium; ocAn, occipital antenna; pa, palp; per, peristomium; pr, prostomium; prob, proboscis; pyg, pygidium.

5. Scolelepis (Parascolelepis) gilchristi (Day, 1961). South Africa. 6. Scolelepis (Parascolelepis) globosa Wu and Chen, 1964. East China Sea, intertidal. 7. Scolelepis (Parascolelepis) korsuni Sikorski, 1994. North Sea, 108 m. 8. Scolelepis (Parascolelepis) papillosa (Okuda, 1937). Northwest Pacific, Korea. 9. Scolelepis (Parascolelepis) precirriseta Blake and Kudenov, 1978. Australia. 10. Scolelepis (Parascolelepis) quinquedentata (HartmannSchröder, 1965). Chile, low water. 11. Scolelepis (Parascolelepis) texana Foster, 1971. Gulf of Mexico; Massachusetts to North Carolina; California.

12. Scolelepis (Parascolelepis) towra Blake and Kudenov, 1978. Australia, New South Wales. 13. Scolelepis (Parascolelepis) tridentata (Southern, 1914). Northeastern Atlantic; northern Europe, shallow water. 14. Scolelepis (Parascolelepis) yamaguchchii (Imajima, 1959). Northwest Pacific, Japan. Subgenus Scolelepis (Scolelepis) Blainville, 1828 15. Scolelepis (Scolelepis) acuta (Treadwell, 1914). Pacific Ocean, California. 16. Scolelepis (Scolelepis) agilis (Verrill, 1873). New England. 17. Scolelepis (Scolelepis) aitutakii Gibbs, 1972. Pacific Ocean, Cook Islands. 18. Scolelepis (Scolelepis) alaskensis (Treadwell, 1914). Pacific Ocean, Alaska.

54 

 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.23: Scolelepis (Parascolelepis) species. A–E, S. (Parascolelepis) texana: A, anterior end, dorsal view; B, chaetiger 3, anterior view; C, chaetiger 18 anterior view; D, base of palp and palpal sheath; E, hooded hook. F, G, S. (Parascolelepis) bousfieldi: F, anterior end, dorsal view; G, hooded hook. A–E, after Imajima (1992) and Blake (1996); F, G, after Maciolek (1987). Scale bars: F, 100 µm; G, 10 µm; A–E, not to scale. Abbreviations: br, branchia; neL, neuropodial lamella; neP, neuropodium; noL, notopodial lamella; noP, notopodium; ocAn, occipital antenna; pa, palp; per, peristomium; pr, prostomium; preL, prechaetal lamella; postL, postchaetal lamella.

19. Scolelepis (Scolelepis) alisonae Williams, 2007. Philippines. 20. Scolelepis (Scolelepis) anakenae Rozbaczylo and Castilla, 1988. Pacific Ocean, Eastern Island. 21. Scolelepis (Scolelepis) andradei Delgado-Blas, Diaz and Linero-Arana, 2010. Caribbean Sea, Venezuela. 22. Scolelepis (Scolelepis) angulata Zhou, 2014. Yellow Sea, China. 23. Scolelepis (Scolelepis) antipoda (Augener, 1926). New Zealand. 24. Scolelepis (Scolelepis) arenicola Hartmann-Schroder, 1959. Pacific Ocean, El Salvador. 25. Scolelepis (Scolelepis) balihaiensis HartmannSchröder, 1979. Australia, Western Australia. 26. Scolelepis (Scolelepis) bifida Hutchings and Turvey, 1984. Australia, South Australia. 27. Scolelepis (Scolelepis) blakei Hartmann-Schröder, 1980. Australia, Western Australia, Dampier. 28. Scolelepis (Scolelepis) bonnieri (Mesnil, 1896). Northeast Atlantic, coast of France. 29. Scolelepis (Scolelepis) branchia Imajima, 1992. Pacific Ocean, Japan. 30. Scolelepis (Scolelepis) brevibranchia HartmannSchröder, 1991. Southwest Pacific Ocean, Chile. 31. Scolelepis (Scolelepis) bullibranchia Rossi, 1982. Pacific Ocean, California. 32. Scolelepis (Scolelepis) cantabra (Rioja, 1918). Spain, Cantabrian Sea. 33. Scolelepis (Scolelepis) carunculata Blake and Kudenov, 1978. Australia, Victoria, Western Port Bay. 34. Scolelepis (Scolelepis) chilensis (Hartmann-Schröder, 1962). Pacific Ocean, Chile.

35. Scolelepis (Scolelepis) crenulata Hartmann-Schröder, 1991. Southwest Pacific Ocean, Chile. 36. Scolelepis (Scolelepis) daphoinos Zhou, Ji and Li, 2009. China, northern seas. 37. Scolelepis (Scolelepis) denmarkensis HartmannSchröder, 1983. Australia, Western Australia. 38. Scolelepis (Scolelepis) dicha Hutchings, Frouin and Hily, 1998. Pacific Ocean, French Polynesia, Tahiti. 39. Scolelepis (Scolelepis) edmondsi Hutchings and Turvey, 1984. Australia, South Australia. 40. Scolelepis (Scolelepis) eltaninae Blake, 1983. Southern Ocean, Antarctica. 41. Scolelepis (Scolelepis) finmarchicus Sikorski and Pavlova, 2015. Norway, Barents Sea (Kola Bay). 3–150 m. 42. Scolelepis (Scolelepis) foliosa (Audouin and Milne Edwards, 1833). Northeast Atlantic, France; Northwest Atlantic, Massachusetts. 43. Scolelepis (Scolelepis) gaucha (Orensanz and Gianuca, 1974). Brazil. 44. Scolelepis (Scolelepis) goodbodyi (Jones, 1962). Caribbean Sea, Jamaica. 45. Scolelepis (Scolelepis) hutchingsae Dauer, 1985. Australia, Queensland, Great Barrier Reef; Philippines. 46. Scolelepis (Scolelepis) inversa Meißner and Götting, 2015. Australia, Queensland, Great Barrier Reef. 47. Scolelepis (Scolelepis) knightjonesi (de Silva, 1961). Sri Lanka. 48. Scolelepis (Scolelepis) kudenovi Hartmann-Schröder, 1981. Australia, Western Australia; Japan. 49. Scolelepis (Scolelepis) laciniata Eibye-Jacobsen, 1997. Thailand.



50. Scolelepis (Scolelepis) lamellata (McIntosh, 1909). Northwest Atlantic, off Northwest Africa. 51. Scolelepis (Scolelepis) lamellicincta Blake and Kudenov, 1978. Australia, Victoria, Western Port Bay. 52. Scolelepis (Scolelepis) laonicola (Tzetlin, 1985). White Sea. 53. Scolelepis (Scolelepis) lefebvrei (Gravier, 1905). Red Sea. 54. Scolelepis (Scolelepis) lighti Delgado-Blas, 2006. Gulf of Mexico. 55. Scolelepis (Scolelepis) lingulata Imajima, 1992. Pacific Ocean, Japan. 56. Scolelepis (Scolelepis) longirostris (Quatrefages, 1843). Northeast Atlantic Ocean, English Channel. 57. Scolelepis (Scolelepis) magnicornuta Williams, 2007. Philippines. 58. Scolelepis (Scolelepis) magnus Ozolinsh, 1990. Sea of Japan, Peter the Great Bay. 59. Scolelepis (Scolelepis) marionis Branch, 1998. Southern Ocean, Marion Island. 60. Scolelepis (Scolelepis) melasma Hutchings, Frouin and Hily, 1998. Pacific Ocean, French Polynesia, Tahiti. 61. Scolelepis (Scolelepis) mesnili Bellan and Lagardère, 1971. Atlantic coast of France, Ile d’Oeron. 62. Scolelepis (Scolelepis) minuta (Treadwell, 1939). Gulf of Mexico, Texas. 63. Scolelepis (Scolelepis) neglecta Surugiu, 2016. E North Atlantic, Bay of Biscay, Spain, 25 m. 64. Scolelepis (Scolelepis) occidentalis Hartman, 1961. Pacific Ocean, California. 65. Scolelepis (Scolelepis) occipitalis Blake and Kudenov, 1978. Australia, New South Wales. 66. Scolelepis (Scolelepis) oligobranchia (Chlebovitsch, 1959). Northeast Pacific, Kurile Islands. 67. Scolelepis (Scolelepis) perrieri (Fauvel, 1902). West Africa, Senegal. 68. Scolelepis (Scolelepis) pettiboneae Maciolek, 1986. Western North Atlantic, off Georgia. 69. Scolelepis (Scolelepis) pigmentata (Reish, 1959). Pacific Ocean, Southern California. 70. Scolelepis (Scolelepis) phyllobranchia Blake and Kudenov, 1978. Australia. 71. Scolelepis (Scolelepis) planata Imajima, 1992. Pacific Ocean, Japan. 72. Scolelepis (Scolelepis) quadridentata Maciolek, 1986. Western North Atlantic, Virginia, 16 m. 73. Scolelepis (Scolelepis) sagittaria Imajima, 1992. Pacific Ocean, Japan. 74. Scolelepis (Scolelepis) squamata (O.F. Müller, 1806). Type locality, Denmark; widely reported elsewhere. 75. Scolelepis (Scolelepis) unidentata (Day, 1973). Western North Atlantic, New Jersey to South Carolina. 76. Scolelepis (Scolelepis) variegata Imajima, 1992. Pacific Ocean, Japan.

7.4.1 Spionidae Grube, 1850 

 55

77. Scolelepis (Scolelepis) vazaha Eibye-Jacobsen and Soares, 2000. 78. Scolelepis (Scolelepis) vexillata Hutchings and Rainer, 1979. Australia, New South Wales, Careel Bay. 79. Scolelepis (Scolelepis) victoriensis Blake and Kudenov, 1978. Australia, Victoria, Western Port Bay. 80. Scolelepis (Scolelepis) villosivaina Williams, 2007. Philippines. 81. Scolelepis (Scolelepis) viridis Blake and Kudenov, 1978. Australia, Queensland, Great Barrier Reef. 82. Scolelepis (Scolelepis) vossae Delgado-Blas, 2006. Atlantic coast of Florida. 83. Scolelepis (Scolelepis) westoni Maciolek, 1986. Western North Atlantic Ocean, off North Carolina, 33–36 m. 84. Scolelepis (Scolelepis) williami (de Silva, 1961). Sri Lanka. Spiophanes Grube, 1860 Type species: Spiophanes kroyeri Grube, 1860, by monotypy. 31 species Synonym: Morants Chamberlin, 1919. Type species: Morants duplex Chamberlin, 1919:17, by monotypy. Fide Blake 1996. Diagnosis: Body elongate (Fig.  7.4.1.1  A); prostomium subtriangular (Fig. 7.4.1.24 A), bell-shaped (Fig. 7.4.1.24 C) or rarely rounded (Fig. 7.4.1.24 B), anterior margin never incised; frontal or lateral horns present (Figs. 7.4.1.1  A; 7.4.1.24 A) or absent; eyespots present or absent; occipital antenna present or absent. Nuchal organs as two ciliated bands along dorsum (Figs. 7.4.1.3  B; 7.4.1.24  A, C), maximally extending to chaetiger 17, or as pair of dorsal loops not extending beyond chaetiger 6 (Fig. 7.4.1.24 B). Branchiae absent. Dorsal and transverse ciliated crests or bands usually present (Fig. 7.4.1.3 C). Body divided into three regions: anterior region extending to chaetiger 4, with well-developed parapodial lamellae; middle body region from chaetiger 5 to last chaetiger bearing capillary chaetae rather than hooks in neuropodia (chaetigers 13–15); posterior region with neuropodial hooks. Middle chaetigers of Spiophanes species usually with parapodial glandular organs on chaetigers 5 to 7 (8) and with chaetal spreaders of different types (see Meißner and Hutchings 2003; Fig.  7.4.1.4  C, D); from chaetiger 9, glands open as simple vertical slits. Ventrolateral intersegmental pouches present or absent between neuropodia. Chaetiger 1 with one to two conspicuous crooklike chaetae in neuropodium (Fig.  7.4.1.24  D); otherwise neurochaetae in anterior and middle body region all capillaries (Fig. 7.4.1.24  G), arranged in one to two rows; posterior region with quadridentate hooks, hood present or absent (Figs.  7.4.1.4  F; 7.4.1.24  H–I). Notochaetae all capillaries (Fig. 7.4.1.24 E), in middle body region usually arranged in three rows; otherwise in two rows or indistinct rows.

56 

 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.24: Spiophanes species. A, S. anoculata, anterior end, dorsal view; B, S. wigleyi, anterior end, dorsal view; C–J, S. duplex: C, anterior end, dorsal view; D, chaetiger 1, anterior view; E, notochaeta, posterior notopodium; F, inferior sabre chaeta; G, capillary neurochaeta, anterior neuropodium; H–I, neuropodial hook, lateral and frontal view; J, posterior end, dorsal view. A, B, after Blake (1996); C, original; D, after Hartman (1941); E–J, after Blake (1983). Scale bars: A, B, J, 300 µm; C, 500 µm; E–I, 10 µm; D, not to scale. Abbreviations: anC, anal cirrus; neL, neuropodial lamella; noL, notopodial lamella; nuO, nuchal organ; per, peristomium; pr, prostomium.

Bacillary chaetae may be present from chaetigers 5 to 8. One to two ventral sabre chaetae (Fig. 7.4.1.24 F) usually from chaetiger 4, rarely from chaetigers 5 or 10, or sometimes not present until neuropodial hooks appear. Pygidium with two or more anal cirri (Fig. 7.4.1.24 J). Remarks: The following list of 31 species is based on extensive revisionary work by Meißner and Hutchings (2003), Meißner (2005), and Meißner and Blank (2009). 1. Spiophanes abyssalis Maciolek, 2000. North Atlantic: Bay of Biscay; Canary Islands; 1922–2356 m. 2. Spiophanes afer Meißner, 2005. Mediterranean Sea: off Spain; off Israel. Southwest Atlantic Ocean: off Namibia; Indian Ocean; off South Africa. 3. Spiophanes algidus Meißner, 2005. Southern Ocean, near Crozet Island, 2010 m. 4. Spiophanes anoculata Hartman, 1960. Eastern Pacific, off California, 1200–2800 m. 5. Spiophanes aucklandicus Meißner, 2005. New Zealand. 6. Spiophanes berkeleyorum Pettibone, 1962. Northeast Pacific, Alaska to California.

7. Spiophanes bombyx (Claparède, 1870). North Atlantic Ocean, European coasts; Mediterranean Sea. 8. Spiophanes cirrata M. Sars in G.O. Sars, 1872. 9. Spiophanes dubitalis Meißner and Hutchings, 2003. Australia, Victoria, Bass Strait, 82 m. 10. Spiophanes duplex (Chamberlin, 1919). Eastern Pacific Ocean: California to Costa Rica; off Chile; Gulf of Mexico and Caribbean Sea; Brazil and Argentina. 11. Spiophanes fimbriata Moore, 1923. Eastern Pacific Ocean: British Columbia to California; Chile. 12. Spiophanes inflatus Meißner, 2005. Indian Ocean: Mozambique; South Africa. 13. Spiophanes japonicum Imajima, 1991. Japan; Australia, New South Wales to Victoria, Bass Strait. 14. Spiophanes kimballi Meißner, 2005. North Pacific Ocean, off California, 73–291 m. 15. Spiophanes kroyeri Grube, 1860. North Atlantic Ocean: Baffin Bay; off Greenland; North Sea. Reported widely, but many records need to be re-examined (Meißner 2005). 16. Spiophanes longicirris Caullery, 1915. Indonesia. 17. Spiophanes longisetus Meißner, 2005. Western North Atlantic, 3753–4663 m. 18. Spiophanes lowai Solis-Weiss, 1983. Eastern Pacific Ocean: Mexico; Costa Rica. 19. Spiophanes luleevi Averincev, 1982. Antarctica, Davis Sea. 20. Spiophanes malayensis Caullery, 1915. Indian Ocean. 21. Spiophanes mediterraneus Meißner, 2005. Mediterranean Sea off Israel, 309–700 m. 22. Spiophanes modestus Meißner and Hutchings, 2003. Australia: Queensland, New South Wales; Western Australia. 23. Spiophanes norrisi Meißner and Blank, 2009. Eastern Pacific Ocean: Alaska to Chile, intertidal to shallow subtidal. 24. Spiophanes pisinnus Meißner and Hutchings, 2003. Australia, New South Wales. 25. Spiophanes prestigium Meißner and Hutchings, 2003. Australia, Tasmania. 26. Spiophanes reyssi Laubier, 1964. Mediterranean Sea, off France, 360 m. 27. Spiophanes similis Meißner, 2005. Southeastern Pacific Ocean, off Peru, 1296–1317 m; Western North Atlantic Ocean, off South Carolina, 218 m. 28. Spiophanes tcherniai Fauvel, 1950. Southern Ocean, Antarctica. 29. Spiophanes uschakowi Zachs, 1933. Northern Sea of Japan, Peter the Great Bay. 30. Spiophanes viriosus Meißner and Hutchings, 2003. Australia, Queensland.



31. Spiophanes wigleyi Pettibone, 1962. Widespread: Northern and Southern Pacific Ocean: Australia, Japan, California; Northern and Southern Atlantic Ocean: Ireland, Norway, South Africa; Indian Ocean; 60–1300 m. Nerininae: the Prionospio complex Remarks: The genera and species that are collectively referred to as the Prionospio complex include a diverse assemblage of spionids that have (1) slender, cylindrical bodies, (2) branchiae of various forms (simple or with digitiform pinnules or flattened plates) first present from chaetiger 1 to 3 and limited to the anterior part of the body, (3) a prostomium that is relatively simple, without frontal horns or an occipital antenna and usually with red eyespots (4) bi- to multidentate hooded hooks in both noto- and neuropodia, (5) well-developed anterior parapodial lamellae, and (6) hard-membraned eggs. Within these rather general features, there exists considerable variation. The entire complex represents one of the most diverse species assemblages within the Spionidae. The systematics of the Prionospio complex has been the subject of extensive study during the past three decades. In most treatments prior to 1971, the genus Pri­ onospio Malmgren, 1867 was defined broadly as having branchiae present from either chaetiger 1 or 2. This definition allowed for the inclusion of typical Prionospio with branchiae from chaetiger 2 and P. pinnata Ehlers, 1901, with branchiae from chaetiger 1. The genus Parapri­ onospio was established by Caullery (1914) for the latter species, but that genus was more or less ignored until the 1970s. The first important revision of the Prionospio complex was by Foster (1971), who separated Prionospio species into five distinct genera based on the type and arrangement of branchiae; the branchial structure was clarified by Maciolek (1985), who suggested the term “apinnate” for branchiae lacking any form of pinnules. 1. Prionospio Malmgren, 1867, sensu stricto. Branchiae from chaetiger 2, with a combination of pinnate and apinnate branchiae. 2. Apoprionospio Foster, 1969. Branchiae from chaetiger 2, four pairs, first three apinnate, fourth with platelike pinnules. 3. Paraprionospio Caullery, 1914. Branchiae from chaetiger 1, three pairs, platelike pinnules. 4. Aquilaspio Foster, 1971. Branchiae from chaetiger 2, two to four pairs, digitiform pinnules. 5. Minuspio Foster, 1971. Branchiae from chaetiger 2, 4 to 40 pairs, apinnate.

7.4.1 Spionidae Grube, 1850 

 57

Blake and Kudenov (1978), as part of a monograph on Australian spionids, added Streblospio and a new genus, Orthoprionospio, to this complex, while at the same time used Prionospio, Aquilaspio, and Minuspio as subgenera of Prionospio sensu lato. These authors synonymized Apopri­ onospio with Prionospio because they considered the specific order in which branchiae are arranged a species-level feature, rather than a genus-level character. Light (1978) provided detailed descriptions, illustrations, and keys for the spionids of San Francisco Bay. In his treatment, he used Paraprionospio, Apoprionospio, Aquilaspio, Minuspio, and Prionospio sensu stricto as subgenera of Prionospio sensu lato. Maciolek (1981a,b) described two new deep-sea genera, Aurospio and Laubieriellus, which are part of this same complex. Maciolek (1985) subsequently provided a major revision of the Prionospio complex, in which genera and all known species were reviewed. She observed that the development and morphology of pinnules on the branchiae of various species, especially for several new deep-sea species, was more complicated than previously understood. She noted that branchiae could be entirely smooth (apinnate), weakly sculptured or wrinkled, have a variable number of digitiform pinnules, or have more elaborate platelike pinnules. These criteria allowed for further refinement of the generic definitions and she resurrected the genus Apoprionospio on the basis that it has platelike rather than digitiform pinnules on the branchiae and thus differs from Prionospio sensu stricto. Maciolek followed Blake and Kudenov (1978), however, in regarding Pri­ onospio, Aquilaspio, and Minuspio as subgenera of ­Prionospio sensu lato. Imajima (1989, 1990a–e), as part of a series of studies on the Spionidae of Japan, reviewed all Japanese species in Apoprionospio, Prionospio sensu lato, and Streblospio. Imajima followed Maciolek’s (1985) generic/subgeneric arrangement. As part of these studies, 12 new species were described and other previously known species completely redescribed and illustrated. Wilson (1990) re-examined Australian species related to P. steenstrupi and P. cirrifera and described eight new species. Wilson accepted all of the genera summarized by Maciolek (1985), but decided that the subgeneric categories of Prionospio were artificial and did not use them. Hylleberg and Nateewathana (1991) described additional new species of Prionospio from shallow waters off Thailand. These authors accepted the generic and subgeneric categories of Prionospio proposed by Maciolek (1985). Blake (1996) also retained the subgeneric categories of Prion­ ospio and retained Apoprionospio as a separate genus.

58 

 7.4 Sedentaria: Sabellida/Spionida

Sigvaldadóttir (1998) conducted a cladistic analysis of the Prionospio complex and concluded that separation of Minuspio, Aquilaspio, and Apoprionospio as separate genera or subgenera of Prionospio sensu stricto was not supported. In general, the conclusions of Sigvaldadóttir (1998) have been followed by subsequent workers. However, the character states used by Sigvaldadóttir did not consider that pinnate and platelike branchiae of Apo­ prionospio and Paraprionospio were different. Because of this, both of these genera are treated here as valid. In the meantime, Tamai (1981) and Yokoyama and Tamai (1981) identified a new series of characters in four morphological “forms” of Paraprionospio in Japan, but did not formally assign these “forms” to new species. The new characters include the presence of flattened and bifoliate pinnules on branchiae as well as the presence of accessory pinnules or filaments at the base of the third pair of branchiae. Wilson (1990) used these characters and described a new species of Paraprionospio from Australia and redescribed the type species, P. pinnata, from Chile. Yokoyama (2007) completely revised the genus Paraprionospio and, at that time, described the “forms” from earlier articles as new species. Apoprionospio Foster, 1969 Type species: Apoprionospio dayi Foster, 1969, by original designation. Two species Diagnosis (after Blake 1996): Prostomium subtriangular, broad anteriorly, often with medial peak (Fig. 7.4.1.25 A), caruncle extends posteriorly to end of chaetiger 1 (Fig.  7.4.1.25  A); occipital antenna absent. ­Peristomium reduced, fused with chaetiger 1, surrounding prostomium posteriorly as a yoke (Fig. 7.4.1.25 A); lateral wings absent. Notopodial postchaetal lamellae of anterior chaetigers lateral rather than dorsomedial. Neuropodial postchaetal lamellae enlarged on chaetiger 2. Branchiae from chaetiger 2, with four pairs; the first three pairs are apinnate, whereas the fourth pair is larger, with flattened platelike pinnules (Figs. 7.4.1.3 F; 7.4.1.25 A). Anterior chaetae capillaries; multidentate hooded hooks present in posterior noto- and neuropodia (Fig.  7.4.1.25  C, D), neuropodial sabre chaetae present (Fig. 7.4.1.25 D). Pygidium with one long dorsomedial cirrus and two shorter ventrolateral lobes (Fig. 7.4.1.25 B). Remarks: Apoprionospio is limited to species of the Pri­ onospio complex having branchiae from chaetiger 2 and at least one pair with platelike pinnules. Two species are known from North America, of which one, A. pygmaea (Hartman 1961), is relatively common in the Eastern

Fig. 7.4.1.25: Apoprionospio pygmaea. A, anterior end, dorsal view; B, posterior end, dorsal view; C, hooded hooks; D, inferior sabre chaeta. All original. Not to scale. Abbreviations: anC, anal cirrus; br, branchia; noL, notopodial lamella; per, peristomium; pr, prostomium.

Pacific. This genus is here reinstated because the platelike branchiae are more similar to those of Paraprionospio than the digitiform pinnules found on the branchiae in many species of Prionospio sensu stricto. To do otherwise would require that Paraprionospio be reevaluated. 1. Apoprionospio dayi Foster, 1969. US Atlantic coast, Massachusetts to North Carolina, 20–145 m. 2. Apoprionospio pygmaea (Hartman 1961). US Pacific coast, Central and Southern California; Gulf of Mexico; Virginia. Aurospio Maciolek, 1981a Type species: Aurospio dibranchiata Maciolek, 1981a. Six species Diagnosis (modified from Maciolek 1981a): Prostomium broadly rounded anteriorly, prolonged posteriorly as a keel (Fig.  7.4.1.26  A, E); eyespots zero to two pairs, occipital tentacle absent. Peristomium partly fused to chaetiger 1, not developed into lateral wings or hood (Fig.  7.4.1.26  A, E). Branchiae two pairs on chaetigers 3 to 4, short, fingerlike partly fused to notopodial lamellae (Fig. 7.4.1.26 B, F). Interramal or interparapodial pouches absent. Anterior chaetae all capillaries; neuro- and notopodial multidentate hooded hooks from chaetigers 9 to 11 and 24 to 38, respectively, in type species; hooks multidentate without secondary hood (Fig.  7.4.1.26  D); neuropodial sabre chaetae present from chaetigers 9 to 11 (Fig. 7.4.1.26 C). Pygidium with one long medial cirrus and two short lateral cirri. Remarks: Although the original description Aurospio and its type species, A. dibranchiata, were well-defined and illustrated by Maciolek (1981a), subsequent researchers



7.4.1 Spionidae Grube, 1850 

 59

Fig. 7.4.1.26: Aurospio dibranchiata. A, anterior end, dorsal view; B, chaetigers 3 and 4, posterior view; C, chaetiger 15, anterior view; D, neuropodial hooded hook; E, anterior end, SEM, left lateral view; F, detail of branchiae of chaetigers 3 and 4. All after Maciolek (1981). Scale bars: A–C, E, 20 µm; D, 2.5 µm; F, 4 µm. Abbreviations: br, branchia; dCr, dorsal crest; neL, neuropodial lamella; noL, notopodial lamella; pa, palp; per, peristomium; pr, prostomium; prob, proboscis.

(Sigvaldadóttir 1992; Mincks et al. 2009; Patterson et al. 2016) have misconstrued the differences between Auros­ pio and Prionospio and have taken species that clearly belong to Prionospio and referred them to Aurospio. These decisions were based almost entirely on the first occurrence of branchiae from chaetiger 3 instead of chaetiger 2. Therefore, several of the species listed in the following should be referred to Prionospio. This issue will be addressed more fully in a subsequent study (Maciolek and Blake, in preparation). 1. Aurospio abranchiata Neal, Paterson and Soto in ­Paterson et al. 2016. Northeast Atlantic Ocean, Porcupine Abyssal Plain, 4800 m. 2. Aurospio banyulensis (Laubier, 1966). Mediterranean Sea. 3. Aurospio dibranchiata Maciolek, 1981a. Widespread globally in continental slope and abyssal depths. 4. Aurospio foodbancsia (Mincks, Dyal, Paterson, Smith and Glover 2009). Antarctic Peninsula, shelf depths. 5. Aurospio pilkena (Wilson, 1990). Australia, Victoria, Bass Strait, 27–113 m.

6. Aurospio tribranchiata Paterson and Soto in Paterson et al. 2016. Northeast Atlantic Ocean, Porcupine Abyssal Plain, 4800 m. Laubieriellus Maciolek, 1981b Type species: Laubieriellus grasslei Maciolek, 1981b. By original designation. Three species Diagnosis (after Maciolek 1981b): Prostomium rounded anteriorly or with weak medial incision; continued posteriorly as a keel, lacking occipital antenna. Peristomium partly fused to chaetiger 1. Branchiae from ­chaetiger 2, four pairs, each branchia elongate, cylindrical, smooth, separate from notopodial lamella. Neuropodial prechaetal lamellae connected in ventral crest on several anterior chaetigers from chaetiger 2. Notopodial postchaetal lamellae connected with dorsal crests on several postbranchial chaetigers. Anterior chaetae all capillaries; multidentate hooded hooks in posterior neuropodia; notopodial hooks absent. Pygidium with two short ventrolateral lobes and one long dorsomedial cirrus.

60 

 7.4 Sedentaria: Sabellida/Spionida

Remarks: Laubieriellus species lack notopodial hooded hooks and thus, although similar, differ from most species of Prionospio. In addition, Laubieriellus species have ventral crests, which connect neuropodia on several anterior chaetigers. Three species are known. 1. Laubieriellus cacatua Erickson and Wilson, 2018. Western Australia, 101–696 m. 2. Laubieriellus grasslei Maciolek, 1981b. Galapagos Rift hydrothermal vents, 2447 m. 3. Laubieriellus salzi (Laubier, 1970). Eastern Mediterranean Sea. Orthoprionospio Blake and Kudenov, 1978 Type species: Orthoprionospio cirriformia Blake and Kudenov, 1978. Monotypic Diagnosis (after Blake and Kudenov 1978): Prostomium rounded on anterior margin; caruncle absent; occipital antenna absent. Peristomium well-developed, forming prominent lateral wings alongside prostomium. Chaetiger

1 well developed, distinctly separate from peristomium, parapodia indistinguishable from those of succeeding chaetigers; notopodial lamellae of all anterior chaetigers foliose, becoming reduced in posterior segments; dorsal ridges lacking. Branchiae beginning on chaetiger 1, 18 to 22 pairs, all cirriform. Anterior chaetae all capillary; multidentate hooded hooks in both neuropodia and notopodia of posterior segments; hooks with apical teeth not closely overlapping main fang; without secondary hood; inferior sabre chaetae present in middle and posterior segments. Pygidium with one reduced, conical ventral lobe and four very small lateral papillae. Remarks: A single species is known. Orthoprionospio cirriformia Blake and Kudenov, 1978. Southeast Australia. Paraprionospio Caullery, 1914 Type species: Prionospio pinnata Ehlers, 1901, designated by Caullery, 1914. 10 species

Fig. 7.4.1.27: Paraprionospio and Prionospio species. A–D, I, Paraprionospio cordifolia: A, anterior end, dorsal view; B, chaetiger 1, anterior view; C, chaetiger 2, anterior view; D, chaetiger 3, anterior view; I, pygidium. E–H, Prionospio alata: E, anterior end, lateral view; F–G, neuropodial hooded hooks; H, chaetiger 9, neuropodium. A–D, I after Yokoyama and Tamai (1981) (as Paraprionospio form B); E–H after Hartman (1960) (as Prionospio pinnata). None to scale. Abbreviations: anC, anal cirrus; br, branchia; neL, neuropodial lamella; noL, notopodial lamella; pa, palp; per, peristomium; pr, prostomium.



Diagnosis (modified from Yokoyama 2007): Prostomium fusiform with rounded (Fig.  7.4.1.27  A), truncated or bluntly pointed anterior end, extending posteriorly as a raised ridge to chaetiger 1 (Fig.  7.4.1.27  A). Peristomium fused with achaetous segment, forming conspicuous lateral wings enfolding prostomium (Fig.  7.4.1.27  A, E). A pair of grooved palps present with membranous basal sheath (Fig. 7.4.1.27 A, E). Three pairs of branchiae on chaetigers 1 to 3, all with densely packed lamellar plates attached serially on inner to posterior face of shaft except in basal region and distal tip (Fig. 7.4.1.27 B–E). Transverse ridge between branchial bases on chaetiger 1 (Fig.  7.4.1.27  A). Notopodial postchaetal lamellae of anterior chaetigers enlarged, triangular (Fig.  7.4.1.4  A), reduced posteriorly; neuropodial postchaetal lamellae of anterior chaetigers enlarged, rounded (Fig. 7.4.1.4 A), reduced posteriorly. Notopodial and neuropodial capillaries limbate and granulated in anterior chaetigers, replaced by nonlimbate, slender capillaries without granulations in middle and posterior chaetigers. Neuropodial hooded hooks multidentate (Fig. 7.4.1.27 F–G); geniculate, from chaetiger 9, accompanied by alternating capillaries and one or two sabre chaetae (Fig.  7.4.1.27  H). Notopodial hooded hooks not as geniculate as neuropodial hooks, appearing from the middle body region. Notopodial and neuropodial hooks with primary and secondary hoods. Shallow ventral furrow running longitudinally from middle to end of body. Membranous dorsal crests appearing from chaetiger 21 present or absent. Eversible proboscis bilobate. Muscular gizzard present. Pygidium with two short lateral cirri and one long medial cirrus (Fig. 7.4.1.27 I). Remarks: The taxonomic characters important in systematics of Paraprionospio are mostly ones that were identified or elaborated on by Tamai (1981), Yokoyama and Tamai (1981), Wilson (1990), and Yokoyama (2007). These characters include the location, presence, absence, and structure of various papillae, lamellae, palp plates, and dorsal/ventral parapodial ridges that had either not been previously observed in Paraprionospio species or were not considered important. Additional chaetal details, when combined with these new characters, provide an array of characters that can be compared and contrasted. Until recently, the most commonly identified species of Paraprionospio, P. pinnata (Ehlers), was considered to be a widespread, and apparently cosmopolitan species (Foster 1971; Blake and Kudenov 1978; Blake 1983, 1996; Maciolek 1985). Revisionary work by Yokoyama (2007) essentially restricted the distribution of P. pinnata to off western South America. Additional species have been described, bringing the total to 10 species now recognized in the genus. The most common North American species is P. alata, which includes most records formerly referred

7.4.1 Spionidae Grube, 1850 

 61

to P. pinnata. Most species are from relatively shallow subtidal or shelf depths; P. lamellibranchia is from upper slope depths. 1. Paraprionospio africana Augener, 1918. West Africa. 2. Paraprionospio alata (Moore, 1923). Pacific Ocean, British Columbia to California; Gulf of Mexico; Atlantic Ocean, Virginia. [Prionospio treadwelli Hartman, 1951 (new name for Prionospio plumosa Treadwell, 1931 homonym]. Fide Yokoyama 2007. [Prionospio tamaii Delgado-Blas, 2004] Fide Yokoyama 2007. [Prionospio yokoyamai Delgado-Blas, 2004] Fide Yokoyama 2007. 3. Paraprionospio coora Wilson, 1990. Australia, offshore New South Wales to Tasmania, 6–124 m; off Japan; East China Sea. 4. Paraprionospio cordifolia Yokoyama 2007. Western Japan, East China Sea; Hong Kong, subtidal. 5. Paraprionospio cristata Zhou, Yokoyama, and Li, 2008. East China Sea, subtidal. 6. Paraprionospio inaequibranchia (Caullery, 1914). India; Indonesia; Malaysia. 7. Paraprionospio lamellibranchia Hartman, 1975. Mozambique Channel, 423 m. 8. Paraprionospio oceanensis Yokoyama, 2007. Off Japan, shelf depth, 35–70 m. 9. Paraprionospio patiens Yokoyama, 2007. Off Japan; Indonesia. 10. Paraprionospio pinnata (Ehlers, 1901). Off Chile. Prionospio Malmgren, 1867 Type species: Prionospio steenstrupi Malmgren, 1867, by monotypy. 100 species Synonyms: Ctenospio M. Sars, 1867. Type species: C.  plumosus M. Sars, 1867, by monotypy. Nomen nudum (= Prionospio plumosus Sars, 1872). Anaspio Chamberlin, 1920. Type species: A. boreus Chamberlin, 1920, by monotypy. Fide Maciolek, 1981a. Aquilaspio Foster, 1971. Type species: Prionospio sexocu­ lata Augener, 1918, by original designation. Minuspio Foster, 1971. Type species: Prionospio cirrifera Wirén, 1883, by original designation. Diagnosis: Prostomium anteriorly rounded or truncate (Figs.  7.4.1.28  A, D, L; 7.4.1.29  A), sometimes weakly incised, often with peaks (Fig. 7.4.1.29 B, C, E, G), without frontal horns; subtriangular, rectangular or oval in shape, caruncle extending at least to chaetiger 1 (Figs. 7.4.1.28 A, D, E, L; 7.4.1.29  A–C, E, G); eyespots present or absent;

62 

 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.28: Examples of Prionospio sensu stricto. A–C, P. cf. steenstrupi: A, anterior end, dorsal view; B, midbody chaetiger, anterior view; C, posterior chaetiger, posterior view. D, P. fauchaldi, anterior end, dorsal view. E–K, P. orensanzi: E, anterior end, dorsal view; F, G, capillary notochaetae, chaetiger 7, anterior and posterior rows, respectively; H, inferior sabre chaeta; I–K, neuropodial hooded hooks in various views. L, P. heterobranchia, anterior end, dorsal view. A–D, L after Maciolek (1985); E–K after Blake (1983). Scale bars: A, D, L 100 µm; B, C, 50 µm; E, 300 µm; F–I, 20 µm; J, K, 10 µm. Abbreviations: br, branchia; dCr, dorsal crest; neL, neuropodial lamella; noL, notopodial lamella; pa, palp; per, peristomium; pr, prostomium.

occipital antenna absent. Peristomium at least partially fused with chaetiger 1, often surrounding prostomium with free, flattened lateral wings (Fig. 7.4.1.29 F). Parapodia of chaetiger 1 reduced; noto- and neuropodial lamellae largest in branchial region (Fig.  7.4.1.2  D), reduced thereafter; notopodial lamellae often connected by low to high dorsal ridges or crests (Figs.  7.4.1.2  F; 7.4.1.28  A, E). Branchiae from chaetiger 2 limited to anterior chaetigers, 2 to 15 pairs, rarely more; branchiae all apinnate (Fig. 7.4.1.29 A–C, F), all pinnate (Fig. 7.4.1.29 G), or various combinations of both (Figs.  7.4.1.3  D; 7.4.1.28  A, D–E, L); pinnate branchiae with pinnules digitiform (Figs. 7.4.1.2 E; 7.4.1.3 D, E; 7.4.1.28 A, E, L; 7.4.1.29 G), not platelike; each branchia entirely free from dorsal lamella. Interparapodial pouches present (Fig.  7.4.1.29  A) or absent. Anterior chaetae limbate capillaries (Figs. 7.4.1.28 F–H; 7.4.1.29 K); posterior noto- and neuropodial hooded hooks present, bi-, tri-, or multidentate (Figs.  7.4.1.28  I, J; 7.4.1.29  H, I), with secondary hood. Neuropodial sabre chaetae present

(Fig. 7.4.1.29 J) or absent (P. perkinsi Maciolek, 1985). Pygidium with one long dorsomedial cirrus and two shorter ventrolateral lobes (Fig. 7.4.1.29 D), all three sometimes fused. Remarks: This definition closely follows that of Maciolek (1985), with modifications as required by recent investigations. With the subgeneric categories (Aquilaspio with all pinnate branchiae and Minuspio with all apinnate branchiae) included, there are more than 100 species, making Prionos­ pio the largest spionid genus. The majority of species are offshore ranging from low subtidal to shelf depths where they sometimes are dominant in benthic communities. Prionos­ pio species are also highly diverse in slope and abyssal sediments; many deep-water species have yet to be described. 1. Prionospio aluta Maciolek, 1985. Northwest Atlantic, 400 m. 2. Prionospio amarsupiata Neal and Altamira in Paterson et al., 2016. Widespread in the deep sea: Portuguese margin canyons, 3199–4488 m; Southern Ocean, near Crozet Island, 3500 m; equatorial Pacific;

7.4.1 Spionidae Grube, 1850 



 63

Fig. 7.4.1.29: Examples of Prionospio, other branchial forms. A, P. aluta, anterior end, dorsal view. B, P. cirrifera, anterior end, dorsal view. C, D, P. perkinsi: C, anterior end, dorsal view; D, pygidium. E, F, P. delta: E, anterior end, dorsal view; F, anterior end, lateral view. G–K, P. aucklandica: G, anterior end, dorsal view; H, I, neuropodial hooded hooks; J, sabre chaeta; K, capillary notochaeta from anterior chaetiger. A–F, after Maciolek (1985); G–K, after Blake and Kudenov (1978). Scale bars: A, 300 µm; B, E, F, 100 µm; C, D, 50 µm; H–K, 20 µm. Abbreviations: anC, anal cirrus; br, branchia; car, caruncle; dCr, dorsal crest; neL, neuropodial lamella; noL, notopodial lamella; pa, palp; per, peristomium; pr, prostomium.

3. 4. 5. 6. 7.

8.

Northeast Atlantic, Cape Verde Abyssal Plain, 4500 m and Madeira Abyssal Plain, 4800 m. Prionospio anatolica Dagli and Çinar, 2011. Eastern Mediterranean Sea, south coast of Turkey, 10 m. Prionospio andamanensis Hylleberg and Nateewathana, 1991. Thailand, Andaman Sea, 10–30 m. Prionospio anneae Radashevsky, 2015. Australia, Queensland, Great Barrier Reef, 5–16 m. Prionospio anuncata Fauchald, 1972. Eastern Pacific Ocean, off Mexico, >1000 m; Japan. Prionospio aucklandica Augener, 1923. New Zealand, Auckland Island; Australia, Queensland, New South Wales, Western Australia. Prionospio austella Delgado-Blas, 2015. Southern Gulf of Mexico, off Campeche, 91 m.

9. Prionospio australiensis Blake and Kudenov, 1978. Australia, Queensland, Moreton Bay. 10. Prionospio bocki Söderström, 1920. Kobe Bay, Japan; Madagascar. 11. Prionospio branchilucida Altamira, Glover and Paterson in Paterson et al., 2016. Widespread in the deep sea: Equatorial Pacific and Central Pacific Oceans, 4078–5027 m; Northeast Atlantic, Cape Verde and Madeira Abyssal Plains 4800–5041 m. 12. Prionospio caribensis Delgado-Blas, 2014. Caribbean Sea, off Mexico. 13. Prionospio caspersi Laubier, 1962. Mediterranean Sea; Japan. 14. Prionospio cerastae Radashevsky, 2015. Australia, Queensland, Great Barrier Reef, 5–10 m.

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 7.4 Sedentaria: Sabellida/Spionida

15. Prionospio cirrifera Wirén, 1883. Kara Sea. 16. Prionospio convexa Imajima, 1990. Japan, 25–57 m. 17. Prionospio cooki Radashevsky, 2015. Australia, Queensland, Great Barrier Reef, 3–10 m. 18. Prionospio coorilla Wilson, 1990. Australia, Victoria, Port Phillip Bay; Tasmania. 19. Prionospio cornuta Hylleberg and Nateewathana, 1991. Thailand, Andaman Sea, 10–20 m. 20. Prionospio crassumbranchiata Delgado-Blas, 2015. Southern Gulf of Mexico, off Veracruz, Tabasco, and Campeche, 29–188 m. 21. Prionospio cristata Foster, 1971. Western North Atlantic, North Carolina; widespread in the Gulf of Mexico. 22. Prionospio decipiens Söderström, 1920. Portugal. 23. Prionospio delta Hartman, 1965. Widespread deep-water species. Off northeast South America; Gulf of Mexico; off California, slope depths. 24. Prionospio depauperata Imajima, 1990. Japan, 8–920 m. 25. Prionospio dubia Day, 1961. South Africa; North Atlantic: Australia, Victoria; Japan. 26. Prionospio ehlersi Fauvel, 1928. Morocco; Mediterranean Sea; Australia; Southwest Africa; Japan. 27. Prionospio elegantula Imajima, 1990. Japan, 29–101 m. 28. Prionospio elongata Imajima, 1990. Japan, 34–145 m. 29. Prionospio ergeni Dagli and Çinar, 2009. Eastern Mediterranean Sea, Turkey, 3–25 m. 30. Prionospio fallax Söderström, 1920. Northeast Atlantic Ocean, Scotland to Mediterranean Sea, shelf depths. 31. Prionospio fauchaldi Maciolek, 1985. Northwest Atlantic, 530 m; Eastern Pacific, slope depths. 32. Prionospio festiva (Grube, 1872). Adriatic Sea. 33. Prionospio grossa Imajima, 1990. Japan, 80–154 m. 34. Prionospio henriki Hylleberg and Nateewathana, 1991. Thailand, Andaman Sea, 10–30 m. 35. Prionospio hermesia Neal and Paterson in Paterson et al., 2016. Northeast Atlantic Ocean, canyons on the Portuguese margin, 3214–4364 m. 36. Prionospio heterobranchia Moore, 1907. Western North Atlantic, New England region, intertidal to low water. 37. Prionospio jamaicensis Delgado-Blas, 2014. Jamaica, 0–10 m. 38. Prionospio japonica Okuda, 1935. Japan, intertidal to 5 m. 39. Prionospio jonatani Delgado-Blas, 2015. Southern Gulf of Mexico, Veracruz, Tabasco, Campeche and Yucatán, 38–147 m. 40. Prionospio jubata Blake, 1996. Eastern Pacific Ocean, California, shelf depths, 90–295 m. 41. Prionospio kaplani Altamira, Glover and Paterson in Paterson et al., 2016. Central and Equatorial Pacific Ocean, 4300–4942 m.

42. Prionospio kirrae Wilson, 1990. Australia, Victoria and Tasmania, 29–84 m. 43. Prionospio komaeti Hylleberg and Nateewathana, 1991. Thailand, Andaman Sea, 10 m. 44. Prionospio krusadensis Fauvel, 1929. Indian Ocean; Japan. 45. Prionospio kulin Wilson, 1990. Australia, Northern Territory, Queensland, New South Wales and Victoria, 16–137. 46. Prionospio laciniosa Maciolek, 1985. Off West Africa, 527–542 m. 47. Prionospio lighti Maciolek, 1985. Eastern Pacific Ocean, Washington to California, intertidal to shallow subtidal. 48. Prionospio lineata Imajima, 1990. Japan, intertidal to 96 m. 49. Prionospio lylei Radashevsky, 2015. Australia, Queensland, Great Barrier Reef, 6–21 m. 50. Prionospio maciolekae Dagli and Çinar, 2011. Eastern Mediterranean Sea, 50 m. 51. Prionospio malayensis (Caullery, 1914). Malaysia; Andaman Sea, Thailand, 10–30 m. 52. Prionospio marsupiala Blake, 1996. Eastern Pacific Ocean, California, slope depths, 565 m. 53. Prionospio membranacea Imajima, 1990. Japan, intertidal to 90 m. 54. Prionospio multibranchiata Berkeley, 1927. Eastern Pacific, British Columbia; Japan. 55. Prionospio multicristata Hutchings and Rainer, 1979. Australia, New South Wales. 56. Prionospio multipinnulata (Blake and Kudenov, 1978). Australia, New South Wales; Victoria; Tasmania. 57. Prionospio neenae Hylleberg and Nateewathana, 1991. Thailand, Andaman Sea, 10 m. 58. Prionospio newportensis Reish, 1959. Eastern North Pacific Ocean, Southern California, shallow subtidal. 59. Prionospio nielseni Hylleberg and Nateewathana, 1991. Thailand, Andaman Sea, 10–20 m. 60. Prionospio nirripa Wilson, 1990. Australia, Victoria, Bass Strait, 21–99 m. 61. Prionospio oligopinnulata Delgado-Blas, 2015. Southern Gulf of Mexico, Campeche, Yucatán, 17 m. 62. Prionospio oshimensis Imajima, 1990. Japan, Oshima Strait, 50–58 m. 63. Prionospio pacifica Zhou and Li 2009. China, East and South China Seas, shelf depths. 64. Prionospio paradisea Imajima, 1990. Japan, 5–730 m; China, East and South China Seas. 65. Prionospio patagonica Augener, 1923. Southwest Pacific, southern Chile to Patagonia, intertidal. 66. Prionospio paucipinnulata Blake and Kudenov, 1978. Australia, New South Wales, Victoria, Port Phillip Bay.



67. Prionospio perkinsi Maciolek, 1985. Western North Atlantic, Florida. 68. Prionospio peruana Hartmann-Schröder, 1962. Southeast Pacific, Peru. 69. Prionospio phuketensis Hylleberg and Nateewathana, 1991. Thailand, Andaman Sea, 10–20 m. 70. Prionospio plumosa M. Sars in G.O. Sars, 1872. Eastern North Atlantic, Norway. 71. Prionospio polybranchiata Fauvel, 1929. Indian Ocean. 72. Prionospio pulchra Imajima, 1990. Japan, intertidal to 67 m. 73. Prionospio pyramidalis (Hutchings and Turvey, 1984). Australia, South Australia, intertidal. 74. Prionospio queenslandica Blake and Kudenov, 1978. Australia, Queensland. 75. Prionospio rosariae Delgado-Blas, 2014. Caribbean Sea, Mexico, low water. 76. Prionospio rotalis Mohammad, 1970. Arabian Gulf, Kuwait, intertidal. 77. Prionospio rotunda Delgado-Blas, 2015. Southern Gulf of Mexico, Yucatan; Caribbean Sea, Mahahual, shallow. 78. Prionospio rugosa Sigvaldadóttir, 1997. China, Hong Kong. 79. Prionospio runei Hylleberg and Nateewathana, 1991. Thailand, Andaman Sea, 10–30 m. 80. Prionospio saccifera Mackie and Hartley, 1990. China, Hong Kong 11–21 m; Red Sea, Gulf of Suez, 43–49 m. 81. Prionospio saldanha Day, 1961. South Africa. 82. Prionospio sandersi Maciolek, 1981b. Southeast Pacific, Galapagos Rift hydrothermal vents, 2447 m. 83. Prionospio sexoculata Augener, 1918. West Africa; Japan. 84. Prionospio sishaensis Wu and Chen, 1964. South China Sea. 85. Prionospio somaliensis Cognetti-Varriale, 1988. Indian Ocean, Somalia. 86. Prionospio spongicola Wesenberg-Lund, 1958. Caribbean Sea, Trinidad. 87. Prionospio steenstrupi Malmgren, 1867. Northeast Atlantic (Iceland), shelf depths. Fide Sigvaldadóttir and Mackie 1993. 88. Prionospio tatura Wilson, 1990. Australia, Victoria and Western Australia. 89. Prionospio tetelensis Gibbs, 1971. Pacific Ocean, Solomon Islands. 90. Prionospio texana Hartman, 1951. Gulf of Mexico, Texas coast. 91. Prionospio thalanji Wilson and Humphreys, 2001. Australia, Western Australia, from a marine cave. 92. Prionospio tridentata Blake and Kudenov, 1978. Australia, New South Wales. 93. Prionospio tripinnata Maciolek, 1985. Mediterranean Sea, 500–509 m.

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 65

94. Prionospio Sigvaldadóttir and unilamellata Desbruyères, 2003. Mid-Atlantic Ridge vent fields, 1690–3520 m. 95. Prionospio vallensis Neal and Paterson in Paterson et  al., 2016. Northeast Atlantic, canyons along Portuguese Margin, 3199–4419 m. 96. Prionospio variegata Imajima, 1990. Japan, 10–150 m. 97. Prionospio vermillionensis Fauchald, 1972. Eastern Pacific, Gulf of California, Guaymas Basin, 495 m. 98. Prionospio wambiri Wilson, 1990. Australia, New South Wales to Tasmania, intertidal to 55 m. 99. Prionospio wireni Maciolek, 1985. Western North Atlantic, North Carolina, intertidal. 100. Prionospio yuriel Wilson, 1990. Australia, New South Wales, Victoria, South Australia. Streblospio Webster, 1879 Type species: Streblospio benedicti Webster, 1879 by monotypy. Four species Synonym: Heterobranchus Buchanan, 1890: 175. Type species: Heterobranchus shrubsolii Buchanan, 1890. Fide McIntosh, 1915. Diagnosis: Prostomium anteriorly rounded (Fig. 7.4.1.30 B), not continuing posteriorly as caruncle; eyespots present; small occipital tentacle posterior to prostomium present or absent. Peristomium fused to chaetiger 1, forming moderately developed peristomial wings. Branchiae one pair on chaetiger 1 (Figs.  7.4.1.1  G; 7.4.1.30  A, B). Notopodial lamellae on chaetiger 2 forming prominent transverse dorsal collar or fold (Figs. 7.4.1.1 G; 7.4.1.30 A, B); posterior

Fig. 7.4.1.30: Streblospio benedicti. A, anterior end, lateral view of adult; B, anterior end, lateral view of juvenile; C, neuropodial hooded hook. A, C, after Hartman (1936); B, original. None to scale. Abbreviations: br, branchia; pa, palp; per, peristomium; pr, prostomium; prob, proboscis.

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 7.4 Sedentaria: Sabellida/Spionida

lamellae forming low ridges across dorsum; interparapodial pouches absent. Notochaetae all capillaries; neurochaetae include capillaries, multidentate hooded hooks (Figs.  7.4.1.4  G, H; 7.4.1.30  C), and ventral sabre chaetae. Pygidium reduced, with two ventral lappets. Remarks: Four species are known. All have unusual forms of viviparity or brooding of larvae in pouches or with branchiae (see section on development of viviparous species). Both lecithotrophic and planktotrophic forms of larval development are known (Blake 2006). 1. Streblospio benedicti Webster, 1879. Widespread in North America: New England to Florida, Gulf of Mexico, California. 2. Streblospio gynobranchiata Rice and Levin, 1998. Gulf of Mexico, Florida; introduced into the Mediterranean. 3. Streblospio padventralis Delgado-Blas, Díaz-Díaz and Viéitez, 2018. Iberian Peninsula. 4. Streblospio shrubsolii (Buchanan, 1890). Widespread in European waters: England, Atlantic coast of France; Mediterranean. Spioninae Söderström, 1920 Spioninae: the Polydora complex Remarks: Spionids having a modified fifth chaetiger are collectively called “polydorids” or the “Polydora complex,” and represent the largest and most diverse group within the family, with approximately 115 recognized species. The generic arrangement has been extensively revised in recent years, with nine genera currently recognized: Amphipolydora, Boccardia, Boccardiella, Carazziella, Dipolydora, Polydora, Polydorella, Pseudopolydora, and Tripolydora (Blake and Kudenov 1978; Blake 1983, 1996). Amphipolydora Blake, 1983 Type species: Polydora abranchiata Hartman, 1953. Designated by Blake 1983. Two species Diagnosis (modified from Blake 1983): Prostomium entire on anterior margin, extending posteriorly as caruncle (Fig. 7.4.1.31 A); eyespots present or absent; occipital tentacle absent. Chaetiger 1 without notochaetae. Modified chaetiger 5 with two types of major spines: (1) first type with an expanded end with terminal tooth and surrounding collar (Fig. 7.4.1.31 E–G); (2) second type a simple acicular spine, dorsal to first (Fig. 7.4.1.31 C, D); noto- (Fig. 7.4.1.31 B) and neuropodial capillaries present. Hooded hooks from chaetiger 7, bidentate, with conspicuous angle between teeth (Fig.  7.4.1.31  I); no constriction or manubrium on shaft. Branchiae absent. Prominent bacillary glands on dorsal surface of anterior chaetigers (Fig.  7.4.1.31  A). Pygidium reduced, with two to four lobes (Fig. 7.4.1.31 H).

Fig. 7.4.1.31: Amphipolydora abranchiata. A, anterior end, dorsal view; B, capillary notochaeta from chaetiger 5; C, D, acicular spines from chaetiger 5; E–G, major spines from chaetiger 5; H, posterior end, lateral view; I, neuropodial hooded hook. All after Blake (1983). Scale bars: A, H, 100 µm; B–G, I, 20 µm. Abbreviations: bacG, bacillary gland; br, branchia; ch5, chaetiger 5; pa, palp; per, peristomium; pr, prostomium; pyg, pygidium.

Remarks: This genus is unusual among polydorids in entirely lacking branchiae. Both species also have prominent groups of bacillary glands on the dorsal surface of some anterior chaetigers. The genus resembles Boccardia and Carazziella in having two types of major spines in chaetiger 5. Two species are known, both from the southern hemisphere. A. abranchiata occurs in coarse sediments in shelf depths off Argentina, whereas A. vestalis occurs in shallow subtidal sponges in New Zealand. A. abranchiata has a smooth collar on the expanded end of the first type of major spine in chaetiger 5; in contrast, A. vestalis has prominent teeth along the margin of the collar (Blake 1983; Paterson and Gibson 2003). Both species are reported to have architomic asexual reproduction; sexual reproduction and larval development are also described for A. vestalis (Gibson and Patterson 2003). 1. Amphipolydora abranchiata (Hartman 1953). Off Argentina, in sand and gravel, 100 m.



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 67

Boccardia Carazzi, 1893 Type species: Boccardia polybranchia Haswell, 1885, by monotypy. 24 species Synonyms: Perialla Kinberg, 1866:253. Type species: Perialla claparedi Kinberg, 1866, by monotypy. Fide Blake (1983). Paraboccardia Rainer, 1973:550. Type species: Paraboc­ cardia syrtis Rainer, 1973, by original designation. Fide Blake and Kudenov (1978). Neoboccardia Buzhinskaja, 1985. Type species: Boccar­ dia perata Khlebovitsch, 1959, by monotypy. Fide Blake (1996).

Diagnosis (modified from Blake 1996): Prostomium anteriorly rounded (Fig.  7.4.1.32  A) or incised (Fig.  7.4.1.32  C, E), extending posteriorly as caruncle (Fig. 7.4.1.32 A, C, E). Chaetiger 1 with or without notochaetae. Chaetiger 5 modified, with two types of major spines, one type simple, smooth, falcate (Fig.  7.4.1.33  A, D, H); second type with expanded apex bearing collar (Fig.  7.4.1.33  E) or cloak of bristles (Figs. 7.4.1.4 O; 7.4.1.33 B, C, G, I); few or no capillary notochaetae. Bidentate hooded hooks with conspicuous angle between teeth (Figs.  7.4.1.4  L; 7.4.1.33  K–M), some species with hooks losing apical tooth in posterior segments (Fig. 7.4.1.33 N, O); hooks without constriction or manubrium on shaft; hooks first appear on chaetigers 7 to 11. Posterior notopodial spines present (Fig. 7.4.1.33 J, P) or absent. Branchiae from chaetiger 2, absent from chaetiger 5, then present, continuing for variable number of chaetigers (Fig. 7.4.1.32 A, C, E). Pygidium disclike, with or without

Fig. 7.4.1.32: Boccardia species morphology. A, B, B. berkeleyorum: A, anterior end, dorsal view; B, posterior end, dorsal view. C, D, B. chilensis: C, anterior end, dorsal view; D, posterior end, dorsal view. E–F, B. pugettensis: E, anterior end, dorsal view; F, posterior end, lateral view. A–D, after Blake and Woodwick (1971); E, F, after Blake (1979b). Scale bars: A, 150 µm; B, 100 µm; C, 250 µm; D, E, 500 µm; F, 300 µm. Abbreviations: br, branchia; car, caruncle; ch5, chaetiger 5; ocAn, occipital antenna; per, peristomium; pr, prostomium; pyg, pygidium.

Fig. 7.4.1.33: Boccardia species chaetae. A–C, K, P, B. berkeleyorum: A, falcate major spine from chaetiger 5; B, C, bristle-topped major spines from chaetiger 5; K, neuropodial hooded hook; P, posterior chaetiger, posterior view. D–F, L, B. chilensis: D, humped falcate major spine from chaetiger 5; E, F, major spines from chaetiger 5 with distal concavity; L, neuropodial hooded hook. G–J, M–O, B. pugettensis: G–I major spines from chaetiger 5; J, spine from posterior notopodia; M–O, sequence of neuropodial hooded hooks with loss of apical tooth from anterior to posterior chaetigers. A–F, K–L, P, after Blake and Woodwick (1971); G–J, M–O, after Blake (1979b). Scale bars: A–F, P, 100 µm; G–I, L, 50 µm; M–O, 25 µm; J, K, 20 µm.

2. Amphipolydora vestalis Paterson and Gibson, 2003. Northern New Zealand; bores into sponges, shallow subtidal.

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separate lobes, or reduced to lobes or cuffs (Fig. 7.4.1.32 B, D, F). Remarks: Species of Boccardia are recognized by having branchiae anterior and posterior to the modified fifth chaetiger and by having two types of large modified spines in chaetiger 5. Boccardia is one of the largest of the polydorid genera, with 24 described species with a mixture of sediment dwellers and calcareous borers among these. All except two of the 24 known species of Boccardia occur in the Indo-Pacific or close boundaries, with most species either in the Eastern Pacific along the coasts North and South America or from New Zealand and Australia. B. chilensis, B. polybranchia, B. proboscidea, and B. welling­ tonensis occur widely in the Pacific and B. proboscidea has also been introduced into Europe and South Africa. Only two species occur outside the boundaries of the Pacific Ocean: Boccardia semibranchiata described from the Mediterranean Sea by Guerin (1990) and Boccardia sala­ zari from the Caribbean Sea by Delgado-Blas (2008). 1. Boccardia acus (Rainer 1973). New Zealand, subtidal, borer in calcareous substrates. 2. Boccardia androgyna Read, 1975. New Zealand, subtidal in sponges. 3. Boccardia anophthalma (Rioja, 1962). Mexico, Gulf of California, subtidal, bores into gastropod shells. Fide Blake 1981. 4. Boccardia basilaria Hartman, 1961. California. Shelf depths, in mud. 5. Boccardia berkeleyorum Blake and Woodwick, 1971. California, intertidal; bores into shells and coralline algae. 6. Boccardia chilensis Blake and Woodwick, 1971. Chile, Australia, New Zealand. 7. Boccardia columbiana Berkeley, 1927. British Columbia to California, bores into calcareous substrates. 8. Boccardia fleckera Hutchings and Turvey, 1984. Australia, South Australia, intertidal. 9. Boccardia galapagense Blake, 1986. Galapagos Islands, shallow subtidal, bores into coral rock. 10. Boccardia jubata Rainer, 1973. New Zealand. 11. Boccardia knoxi (Rainer, 1973). New Zealand, subtidal, bores into calcareous substrates. 12. Boccardia lamellata (Rainer, 1973). New Zealand, intertidal in crevices or on shells. 13. Boccardia natrix (Söderström, 1920). South America. 14. Boccardia otakouica Rainer, 1973. New Zealand, subtidal in bivalve shells. 15. Boccardia perata (Chlebovitsch, 1959). Kurile Islands. 16. Boccardia polybranchia (Haswell, 1885). Australia; South America; Europe. 17. Boccardia proboscidea Hartman, 1940. Eastern Pacific; Australia; Argentina; South Africa; Europe.

18. Boccardia pseudonatrix Day, 1961. South Africa, intertidal. 19. Boccardia pugettensis Blake, 1979. Northeast Pacific, British Columbia, Puget Sound, intertidal to shallow subtidal in sediment. 20. Boccardia salazari Delgado-Blas, 2008. Mexico, Caribbean Sea. 21. Boccardia semibranchiata Guérin, 1990. Europe. Mediterranean coast of France, Etang du Prévost, Hérault, shallow subtidal. 22. Boccardia syrtis (Rainer, 1973). New Zealand, intertidal to subtidal in sediments. 23. Boccardia tricuspa (Hartman 1939). California, intertidal, a borer in calcareous substrates. 24. Boccardia wellingtonensis Read, 1975. New Zealand, intertidal; Chile. Boccardiella Blake and Kudenov, 1978 Type species: Polydora hamata Webster, 1879b, by original designation. Seven species Diagnosis (modified from Blake and Kudenov 1978): Prostomium entire or incised (Fig.  7.4.1.34  A, J) anteriorly, extending posteriorly as caruncle. Chaetiger 1 with or without notochaetae. Chaetiger 5 strongly modified, with one type of major spine in single curved row, smaller companion chaetae present (Fig.  7.4.1.34  F, M, N); major spines typically simple, straight or falcate without accessor teeth of flanges (Fig.  7.4.1.34  C–E, L); capillary notochaetae present (Fig. 7.4.1.34 G). Bidentate hooded hooks from chaetiger 7 (Fig. 7.4.1.34 H, O), main fang and shaft forming oblique angle, with acute angle between main fang and secondary tooth; main fang and secondary tooth subequal; constriction on shaft absent; posterior notopodial spines or hooks present (Fig.  7.4.1.34  I, P) or absent. Branchiae from chaetiger 2, present or absent on chaetiger 5, continuing for variable number of chaetigers. Pygidium disclike, or reduced to small lobes or lappets (Fig. 7.4.1.34 B, K), with or without small cirri or papillae. Remarks: Boccardiella was established by Blake and Kudenov (1978) to accommodate a group of Boccardia species that have only one type of major spine on the modified fifth chaetiger. Most species have posterior notopodial spines that resemble recurved boat hooks (Fig. 7.4.1.34 I, P) that project toward a medial channel in posterior chaetigers (Fig.  7.4.1.34  B, K). In terms of chaetal characteristics, Boccardiella species are closer to some species of Dipolydora than to species of Boccardia. Seven species are known. Three species occur in Australia and New Zealand (B. bihamata, B. limnicola, and B. magniovata); one species occurs in Argentina (B. occipitalis); three species are known in the Northeastern Pacific including California



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 69

Fig. 7.4.1.34: Boccardiella species. A–I, B. hamata: A, anterior end, dorsal view; B, posterior end, dorsal view; C–E, major spines, chaetiger 5; F, companion chaetae with major spines of chaetiger 5; G, superior dorsal notochaeta from chaetiger 5; H, neuropodial hooded hook; I, curved spine from posterior notopodium. J–P, B. ligerica: J, anterior end, dorsal view; K, posterior end, dorsal view; L, major spine from chaetiger 5; M, N, companion chaetae with major spines of chaetiger 5; O, neuropodial hooded hook; P, curved spine from posterior notopodium. A–I, after Blake (1966); J–P, after Blake and Woodwick (1971). Scale bars: A, B, 300 µm; J, K, 200 µm; C–E, L–N, 50 µm; F, G, I, P, 25 µm; O, 20 µm; H, 10 µm. Abbreviations: br, branchiae; car, caruncle; ch5, chaetiger 5; per, peristomium; pr, prostomium; pyg, pygidium.

(B. hamata, B. ligerica, and B. truncata). Of these, B. liger­ ica occurs globally in low-salinity waters in which it has been introduced and become established. Readers are referred to Blake and Woodwick (1971) and Blake and Kudenov (1978) for details regarding these species. 1. Boccardiella bihamata Blake and Kudenov, 1978. Southeast Australia, intertidal in sediment. 2. Boccardiella hamata (Webster, 1879). British Columbia to California; New England; intertidal in sediment or shells. 3. Boccardiella ligerica (Ferronnière, 1898). Widespread; introduced in low-salinity waters. 4. Boccardiella limnicola (Blake and Woodwick, 1976). Australia: Queensland to Southeast Australia, intertidal in low-salinity waters. 5. Boccardiella magniovata (Read, 1975). New Zealand, intertidal, a borer in bivalve shells. 6. Boccardiella occipitalis Blake, 1983. Argentina, intertidal.

7. Boccardiella truncata (Hartman, 1936). California, intertidal in sandstone reefs. Carazziella Blake and Kudenov, 1978 Type species: Polydora citrona Hartman, 1941, designated by Blake and Kudenov, 1978. 13 species Diagnosis (after Blake and Kudenov 1978): Prostomium anteriorly rounded or incised, extending posteriorly as caruncle (Fig.  7.4.1.35  A); eyespots present. Chaetiger 1 with or without notochaetae. Chaetiger 5 modified, with two types of heavy spines arranged in double curved row: (1) first type with expanded tip bearing cusps or bristles (Fig.  7.4.1.35  B, C–E); (2) second type simple, falcate (Fig.  7.4.1.35  B); both types usually with distal bristles; superior dorsal notochaetae present (Fig.  7.4.1.35  F) or absent; neurochaetae of chaetiger 5 a well-developed fascicle of capillaries. Bidentate neuropodial hooded

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Fig. 7.4.1.35: Carazziella hobsonae. A, anterior end, dorsal view; B–E, major spines of chaetiger 5; F, superior dorsal notochaetae of chaetiger 5; G, neuropodial hooded hook; H, posterior end, dorsal view; I, pygidium in posterior view. All after Blake (1979a). Scale bars: A, H, I, 250 µm; B–F, 25 µm; G, 10 µm. Abbreviations: br, branchia; car, caruncle; pa, palp; per, peristomium; pr, prostomium; pyg, pygidium.

hooks begin on chaetigers 7 to 14, with conspicuous angle between teeth and main fang (Fig. 7.4.1.35 G), without constriction on shaft. Branchiae begin posterior to chaetiger 5 (Fig. 7.4.1.35 A). Pygidium with two to four lobes or four digitiform cirri (Fig. 7.4.1.35 H, I). Remarks: Carazziella is characterized by having two types of major spines in two rows on chaetiger 5 and branchiae beginning posterior to chaetiger 5. The genus is closely related to Boccardia in the modification of chaetiger 5, but differs in having branchiae first present posterior to chaetiger 5. Twelve species are known, of which five occur in Australia and New Zealand, and three are from North America. Only two species occur outside the Pacific Ocean: C. patagonica from Argentina and C. hobsonae from the US Atlantic and Gulf coasts. Readers are referred to Blake and Kudenov (1978), Blake (1979a, 1984, 1996), and Sato-Okoshi (1998) for species descriptions. 1. Carazziella calafia Blake, 1979. Central California to western Mexico, intertidal to 40 m. 2. Carazziella carrascoi Blake, 1979. Chile, Bahiá de Concepción, subtidal in mixed sediments. 3. Carazziella citrona (Hartman 1941). Southern California, intertidal. 4. Carazziella hirsutiseta Blake and Kudenov, 1978. Australia, New South Wales, Botany Bay, intertidal.

5. Carazziella hobsonae Blake, 1979. Gulf of Mexico, Florida, shallow subtidal; Massachusetts, Buzzards Bay, subtidal (Blake unpublished). 6. Carazziella hymenobranchiata Blake and Kudenov, 1978. Australia, Victoria, Port Phillip Bay. 7. Carazziella patagonica Blake, 1979. Argentina, shallow subtidal sediments. 8. Carazziella phillipensis Blake and Kudenov, 1978. Australia, Victoria, Port Phillip Bay, shallow subtidal. 9. Carazziella proberti Blake, 1984. New Zealand, off South Island, 122 m. 10. Carazziella reishi (Woodwick, 1964). Pacific Ocean: Eniwetok Atoll; Johnston Atoll; intertidal in coral rock. 11. Carazziella quadricirrata (Rainer, 1973). New Zealand, shallow subtidal associated with encrustation on bivalve shells. 12. Carazziella spongilla Sato-Okoshi, 1998. Japan, low-salinity brackish lake, with freshwater sponges. 13. Carazziella victoriensis Blake and Kudenov, 1978. Australia, Victoria, Port Phillip Bay and Western Port Bay, shallow subtidal; New South Wales, Hawkesbury River. [Polydora penicillata Hutchings and Rainer, 1979]. Fide Walker 2011.



Dipolydora Verrill, 1879 Type species: Polydora concharum Verrill, 1879, designated by Verrill (1881). 43 species Diagnosis (after Blake 1996): Prostomium entire (Fig.  7.4.1.36  C) or incised anteriorly (Fig.  7.4.1.36  A, B, E–K), extending posteriorly as caruncle; eyespots present or absent. Chaetiger 1 with notochaetae. Chaetiger 5 modified, with major spines of one type, with (Figs. 7.4.1.4 N; 7.4.1.37 A, C, E, J) or without accompanying companion chaetae; spines arranged in single curved row; spines simple, falcate (Fig.  7.4.1.37  A, B), with lateral flanges (Figs.  7.4.1.4  I, N; 7.4.1.37  C, D), teeth (Fig.  7.4.1.37  F, I), and/or apical bristles (Figs. 7.4.1.4 K, P; 7.4.1.37 E, F) with superior notochaetae dorsal to modified spines and companion chaetae (Fig. 7.4.1.37 G). Posterior notopodial spines present or absent (Fig. 7.4.1.37 H, K). Neuropodial hooded hooks bidentate, usually with recurved shaft without constriction or manubrium, main fang forming wide angle with shaft and narrow, acute angle with apical tooth (Fig. 7.4.1.37 B); hooks first present from chaetigers 7 to 17. Pygidium disclike, cuff-shaped, with two, three, or four lobes of various forms (Fig. 7.4.1.36 F, H, J, L), or with four or more small papillae (Fig. 7.4.1.36 D). Anterior part of digestive tract sometimes with enlarged, thick, gizzardlike structure (Fig. 7.4.1.6 A, D). Remarks: The genus Dipolydora was revalidated by Blake (1996). The main characters used to separate species of Dipolydora from Polydora include the presence instead of absence of notochaetae on chaetiger 1; bidentate hooded hooks with a recurved shaft without constriction or manubrium and with the main fang forming a wide angle with the shaft and a narrow, acute angle with the apical tooth; the pygidial morphology is variable rather than simple; and some groups of Dipolydora species have a gizzardlike structure in the digestive tract. Approximately 43 species of Dipolydora are known, including several that are poorly known and require study. 1. Dipolydora aciculata (Blake and Kudenov, 1978). Australia, Victoria, subtidal in abalone shells. 2. Dipolydora akaina Blake, 1996. Pacific Ocean, off Central California, continental shelf, 75–168 m, rock outcrops. 3. Dipolydora alborectalis (Radashevsky, 1993). Northwest Pacific Ocean, Sea of Japan, Kurile Islands, Kamchatka; Bering Sea; bores into mollusk shells. 4. Dipolydora anatentaculata Delgado-Blas, 2008. Gulf of Mexico, Florida, in gastropod shells. 5. Dipolydora anoculata (Moore, 1907). New England, Woods Hole, MA, USA. Valid species: Fide Blake (1971), Radashevsky and Petersen 2005.

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 71

6. Dipolydora antonbruunae (Blake, 1983). Pacific Ocean, Peru, low water, bores into gastropod shells. 7. Dipolydora armata (Langerhans, 1880). Type locality: Madeira. Widespread globally in coralline and other calcareous habitats. [Polydora monilaris Ehlers, 1905. New Zealand]. Referred to Dipolydora armata by Day 1954, Blake 1983, and Radashevsky and Nogueira 2003. [Polydora rogeri Martin, 1996]. Fide Radashevsky and Nogueira 2003. 8. Dipolydora barbilla (Blake, 1981). Mexico, Gulf of California, subtidal, bores into gastropod shells. 9. Dipolydora bidentata (Zachs, 1933). Pacific Ocean, Central and Northern California; Sea of Japan; Kurile Islands; intertidal to shallow subtidal, bores into calcareous structures. 10. Dipolydora bifurcata (Blake, 1981). Pacific Ocean, Northern California, intertidal, bores into coralline algae. 11. Dipolydora blakei (Maciolek, 1984a). Off New England, USA, slope depths, 200 m; Mediterranean Sea, Aegean Sea, 18–63 m; off Brazil, shelf and slope depths, 60–1048 m; in sediment (Radashevsky and Simboura 2013). 12. Dipolydora brachycephala (Hartman, 1936). Eastern Pacific, Washington to California, intertidal in sediment. Fide Light 1978; Blake 2006; Ruff and Blake 2007. 13. Dipolydora capensis (Day, 1955). South Africa, intertidal in shells of mollusks. 14. Dipolydora cardalia (Berkeley, 1927). Pacific Ocean, British Columbia; Bering Sea; North Japan Sea; Kamchatka. 15. Dipolydora carunculata Radashevsky, 1993. Northwest Pacific Ocean, Sea of Japan, Kurile Islands; bores into mollusk shells. 16. Dipolydora caulleryi (Mesnil, 1897). Atlantic Ocean, European waters; New England, USA; intertidal in sediment. 17. Dipolydora coeca (Örsted, 1843). Widespread in European waters; South Africa; a borer in calcareous substrates. [Polydora saint-josephi Eliason, 1920] Fide HartmannSchroder 1996. 18. Dipolydora commensalis (Andrews, 1891). Western North Atlantic Ocean, Nova Scotia to North Carolina; North Pacific Ocean, Alaska to California; Sea of Japan; Kurile Islands; intertidal, commensal in shells of hermit crabs. Fide Blake 1971, Blake and Evans 1973, Radashevsky 1993, Blake and Ruff 2007. 19. Dipolydora concharum (Verrill, 1880). Atlantic Ocean, Eastern Canada to New England; off West Greenland; Sea of Japan; subtidal in shells of bivalve molluscs.

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 7.4 Sedentaria: Sabellida/Spionida



7.4.1 Spionidae Grube, 1850 

 73

Fig. 7.4.1.37: Dipolydora species chaetae. A, B, D. socialis: A, major spines and companion chaetae from chaetiger 5; B, neuropodial hooded hooks, with reduction of apical tooth from anterior to posterior chaetigers. C, D. concharum, major spines and a companion chaeta from chaetiger 5. D, D. commensalis, major spines of chaetiger 5. E, D. caulleryi, major spines and companion chaeta from chaetiger 5; F–H, D. quadrilobata: F, major spines from chaetiger 5; G, superior dorsal notochaeta from chaetiger 5; H, posterior notopodial spines. I–K, D. barbilla: I, major spine from chaetiger 5; J, companion chaeta from chaetiger 5; K, posterior notopodial spine. A–H, after Blake (1971); I–K, after Blake (1981). Scale bars: A, E, F–H, 50 µm; C, D, I–K, 20 µm; B, 10 um. Arrows following letters denote groups of chaetae associated with that letter.

20. Dipolydora contoyensis Delgado-Blas, 2008. Caribbean Sea, off Mexico, intertidal, rock fragments. 21. Dipolydora elegantissima (Blake and Woodwick, 1972). Central California, intertidal, bores into shells of hermit crabs. 22. Dipolydora flava (Claparède, 1870). Atlantic Ocean, widespread in European waters, UK, France, Portugal; Mediterranean Sea; New Zealand. 23. Dipolydora giardi (Mesnil, 1896). Atlantic Ocean, widespread in European waters; Mediterranean Sea. Also reported widely including South Africa; California, Chile, Australia, and elsewhere as a borer in mollusk shells; but may be a complex of species. Fide Radashevsky and Petersen 2005. 24. Dipolydora goreensis (Augener, 1918). West Africa.

25. Dipolydora hartmanae (Blake, 1971). Atlantic Ocean, North Carolina, USA, subtidal, on seafloor with broken shell fragments. 26. Dipolydora huelma Sato-Okoshi and Takatsuka, 2001. Pacific Ocean, Chile, near Puerto Montt, intertidal borer in gastropod shells. 27. Dipolydora langerhansi (Mesnil, 1896). North Atlantic Ocean, Madeira, intertidal. 28. Dipolydora magellanica (Blake, 1983). Pacific Ocean, Southwest Chile, shelf depths, 64 m, boring into calcareous substrata. 29. Dipolydora melanopalpa Manchenko and Radashevsky, 2002. Sea of Japan, Peter the Great Bay, subtidal from scallop shells.

◂ Fig. 7.4.1.36: Dipolydora species dorsal morphology. A, D. caulleryi, anterior end; B, D. blakei, anterior end; C, D, D. commensalis: C, anterior end; D, posterior end; E, F, D. barbilla: E, anterior end; F, posterior end; G, H, D. socialis: G, anterior end; H, posterior end; I, J, D. quadrilobata: I, anterior end; J, posterior end; K, L, D. concharum: K, anterior end; L, posterior end. A, C, D, G–L, after Blake (1971); E, F, after Blake (1981). Scale bars: A, 100 µm; B, E, F, I, J, 200 µm; C, G, H, K, L, 50 µm; D, 20 µm. Abbreviations: br, branchia; car, caruncle; pa, palp; per, peristomium; pr, prostomium; pyg, pygidium.

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 7.4 Sedentaria: Sabellida/Spionida

30. Dipolydora normalis (Day, 1957). Southwest Indian Ocean, Natal, and Mozambique. 31. Dipolydora notialis (Blake and Kudenov, 1978). Australia, South Australia in abalone shells. 32. Dipolydora paracaulleryi Meißner, Bick, Guggolz and Götting, 2014. Northeast Atlantic Ocean, Great and Little Meteor Seamounts, 300 m, in coarse sediments. 33. Dipolydora peristomialis (Hartman 1976). Arabian Sea, 35 m. 34. Dipolydora pilikia (Ward, 1981). Pacific Ocean, Hawaii, Oahu, intertidal in sediment over coral rubble. 35. Dipolydora pilocollaris (Blake and Kudenov, 1978). Australia, Victoria, Port Phillip Bay, subtidal. 36. Dipolydora protuberata (Blake and Kudenov, 1978). Australia, Victoria, Port Phillip Bay, subtidal in sediment. 37. Dipolydora quadrilobata (Jacobi, 1883). Northern Europe, Germany; Atlantic Ocean: Massachusetts to North Carolina; Jamaica; South Africa; Northwest Pacific, Peter the Great Bay, Sea of Japan; Northeast Pacific British Columbia to California; low intertidal to shelf depths in sediments. 38. Dipolydora socialis (Schmarda, 1861). Pacific Ocean, British Columbia to California; Chile; Gulf of Mexico; Atlantic Ocean, New England. Fide Blake 1971. [Polydora caeca magna Berkeley, 1927] Fide Blake 1979b. [Polydora neocardalia Hartman, 1961]. Fide Blake 1996. [Polydora socialis plena Berkeley and Berkeley, 1936]. Fide Blake 1971, 1996. 39. Dipolydora tentaculata (Blake and Kudenov, 1978). Australia, Queensland and New South Wales, intertidal. 40. Dipolydora tetrabranchia (Hartman 1945). Atlantic Ocean, North Carolina, shallow subtidal, bores into bivalve shells. 41. Dipolydora tridenticulata (Woodwick, 1964). Central Pacific, bores into coral rock: Philippines, bores into gastropod shells inhabited by hermit crabs. Fide Williams 2001. 42. Dipolydora trilobata (Radashevsky, 1993). Northwest Pacific Ocean, Sea of Japan, Kurile Islands, Kamchatka; Bering Sea; bores into calcareous substrata. 43. Dipolydora vulcanica (Radashevsky, 1994). Northwest Pacific Ocean, Kurile Islands, Kamchatka; Northeast Pacific Ocean, Aleutian Islands, intertidal to 20 m, in sediment on stones and algae in areas of hydrothermal gas vents. Polydora Bosc, 1802 Type species: Polydora cornuta Bosc, 1802. See Blake and Maciolek (1987). 53 species

Synonym: Leucodore Johnston, 1838. Type species: Leucodore ciliatus Johnston, 1838. Fide Mesnil (1896). Diagnosis (modified from Blake 1996): Prostomium entire (Fig. 7.4.1.38 D) or incised anteriorly (Fig. 7.4.1.38 A, C, F), extending posteriorly as caruncle; eyespots present or absent. Chaetiger 1 without notochaetae. Chaetiger 5 greatly modified, with major spines of one type (except postlarvae or juveniles of a few species in which the first major spine is large, falcate, and differs from the second and subsequent spines that develop and eventually replace it), usually accompanied by slender companion chaetae (Fig. 7.4.1.39 A, G); spines arranged in single curved row; spines typically curved apically with accessory teeth or flanges (Fig.  7.4.1.39  A, C, D, F), or collars (Fig.  7.4.1.39  I). Posterior notopodial spines present (Fig.  7.4.1.39  J) or absent. Neuropodial hooded hooks from chaetigers 7 to 14, bidentate with conspicuous angle between teeth and with constriction and manubrium on shaft (Fig.  7.4.1.39  B, E, H). Pygidium saucer-shaped or disclike, border usually entire except for dorsal gap (Fig.  7.4.1.38  B, E, G). Anterior part of digestive tract usually without gizzardlike structure. Remarks: This genus includes some of the most familiar spionids, including numerous species that are borers in mollusk shells and are often considered pests of the shellfish industry. The criteria currently used to separate species of Polydora from related genera were presented by Blake (1996) and include the absence of notochaetae on chaetiger 1; bidentate hooded hooks with a constriction and manubrium on the shaft and with the main fang forming a right angle with the shaft and a wide angle with the apical tooth; a simple and disclike pygidium; a gizzardlike structure in the anterior part of the digestive tract is rare but when present is inconspicuous. At least 54 species are currently included in Polydora. 1. Polydora aggregata Blake, 1969. New England, Maine; intertidal, forms dense accumulations or tube mats. Fide Blake 1971. 2. Polydora alloporis Light, 1970. California, subtidal, burrows into the hydrocoral, Allopora californica. 3. Polydora aura Sato-Okoshi, 1998. Japan, intertidal and subtidal; bores into shells of mollusks. 4. Polydora bioccipitalis Blake and Woodwick, 1972. California bores into shells occupied by hermit crabs; Peru–Chile, bores into shells of the bivalve, Meso­ desma donacium, Fide Riascos et al. 2008, 2009. 5. Polydora brevipalpa Zachs, 1933. Northwest Pacific Ocean, Sea of Japan; Kurile Islands; subtidal, 3–40 m, in shells of scallops. [Polydora variegata Imajima and Sato, 1984]. Fide Radashevsky 1993.



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Fig. 7.4.1.38: Polydora species dorsal morphology. A, B, P. cornuta: A, anterior end; B, posterior end. C, P. websteri, anterior end. D, E, P. colonia: D, anterior end; E, posterior end. F, G, P. aggregata: F, anterior end; G, posterior end. A, B, after Blake and Maciolek (1987); C–G, after Blake (1971). Scale bars: A, B, 500 µm; C, F, G, 200 µm; D, E, 100 µm. Abbreviations: br, branchia; car, caruncle; ocAn, occipital antenna; pa, palp; per, peristomium; pr, prostomium; pyg, pygidium.

6. Polydora calcarea (Templeton, 1836). Atlantic Ocean, Europe; Northwest Pacific Ocean, Sea of Japan; bores into calcareous substrates. Fide Radashevsky and Pankova 2006. 7. Polydora carinhosa Radashevsky, Lana and Nalesso, 2006. Brazil, shallow subtidal; bores into oyster shells. 8. Polydora cavitensis Pillai, 1965. Philippines and Indonesia, intertidal in sediments; mud tubes associated with mussels in Philippines. Fide Williams 2007. 9. Polydora ciliata (Johnston, 1838). North Sea, England, intertidal, in crevices in rocks with sediment; reported widely elsewhere, and likely erroneously, as both a borer and nonborer. See Mustaquim 1986; Radashevsky and Pankova 2006 for discussion of two closely related species, probably P. calcarea (a borer) and P. ciliata (nonborer).

10. Polydora cirrosa Rioja, 1943. Pacific Ocean, Western Mexico, Southern California, Ecuador in soft sediments. Fide Blake 1996. 11. Polydora colonia Moore, 1907. Inhabits sponges; type locality, Massachusetts, USA; also widely reported from the Atlantic Ocean: North Carolina, Jamaica, South Africa, Brazil, Argentina; Mediterranean Sea; likely an alien species in some locations. Fide David and Williams (2012a,b). 12. Polydora cornuta Bosc, 1802. Type-locality, South Carolina, USA. Inhabits soft sediments; opportunistic, sometimes forming dense populations. Reported widely: North America, all three coasts; Caribbean Sea; Brazil, Argentina, Europe; Australia, China, Japan, Pacific coast of Russia. Cryptic species may be present. Fide Blake and Maciolek 1987; Radashevsky 2005; Rice et al. 2008.

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Fig. 7.4.1.39: Polydora species chaetae. A, B, P. cornuta: A, major spines and companion chaetae of chaetiger 5. C–E, P. websteri: C, D, major spines of chaetiger 5; E, neuropodial hooded hook. F–H, P. aggregata: F, major spines of chaetiger 5; G, companion chaeta from chaetiger 5; H, neuropodial hooded hook. I, J, P. colonia: I, major spines of chaetiger 5; J, posterior notopodial hook. A, B, after Blake and Maciolek (1987); C–J, after Blake (1971). Scale bars: A, C, D, F, G, I, J, 20 µm; B, E, H, 10 µm. Arrows following letters denote groups of chaetae associated with that letter.

13.

14.

15. 16.

17. 18.

19.

[Polydora ligni Webster, 1879] fide Blake and Maciolek 1987. Polydora curiosa Radashevsky, 1994. Northwest Pacific, Kurile Islands, shallow subtidal, bores into mollusk shells. Polydora ecuadoriana Blake, 1983. Pacific Ocean, Ecuador; southern Gulf of Mexico; southwestern Atlantic Ocean, Brazil; intertidal, bores into calcareous substrates. Fide Blake 1983; Radashevsky et al. 2006. Polydora fulva Grube, 1878. Philippine Islands. Polydora fusca Radashevsky and Hsieh, 2000. Kinmen Island off mainland China, intertidal in sediments in brackish water. Fide Radashevsky and Hsieh 2000a. Polydora gaikwadi Day, 1973. Indian Ocean, Ratnagiri, India; intertidal boring into gastropod shells. Polydora glycymerica Radashevsky, 1993. Sea of Japan, Peter the Great Bay, shallow subtidal, bores into bivalve shells. Polydora haswelli Blake and Kudenov, 1978. Australia and New Zealand; Brazil; a borer into commercially

important oysters and mussels. Fide Blake and Kudenov 1978; Read 2010. 20. Polydora hermaphroditica Hannerz, 1956. Sweden, Gullmar Fjord. 21. Polydora heterochaeta Rioja, 1939. Pacific Ocean, Mexico, Gulf of California and Acapulco. Fide Blake 1981. 22. Polydora hoplura Claparède, 1869. Type locality: Italy, Gulf of Naples. Widespread borer in shells of commercially important bivalves. Recorded from England, Spain, South Africa, Brazil, Australia, New Zealand, Japan, Korea, California, and Chile. Fide Radashevsky and Migitto 2017; Sato-Okoshi et al. 2016. [Polydora uncinata Sato-Okoshi, 1998]. Fide Radashevsky and Migitto 2017; Sato-Okoshi et al. 2016. 23. Polydora hornelli Willey, 1905. Indian Ocean, Gulf of Mannar, India. 24. Polydora kaneohe Ward, 1981. Hawaii, Oahu, shallow subtidal in coral rock. 25. Polydora laticephala Hartmann-Schröder, 1959. Pacific Ocean, El Salvador, intertidal, in sand.



26. Polydora latispinosa Blake and Kudenov, 1978. Australia, Victoria, Port Phillip Bay, subtidal, bores into shells of scallops and oysters. 27. Polydora limicola Annenkova, 1934. Sea of Japan, Russia. Reported more widely, but records likely belong to other species. Fide Williams and Radashevsky 1999. 28. Polydora lingshuiensis Ye, Tang, Wu, Su, Wang, Yu and Wang, 2015. 29. Polydora mabinii Williams, 2001. Philippines, Batangas, intertidal in hermit crab shells. 30. Polydora maculata Day, 1963. South Africa, 7 m off south coast, extracted from hermit crab shells. 31. Polydora manchenkoi Radashevsky and Pankova, 2006. Sea of Japan, shallow subtidal, bores into gastropod shells occupied by hermit crabs. 32. Polydora nanomon Orensky and Williams, 2009. Jamaica, shallow subtidal in shells occupied by hermit crabs. 33. Polydora narica Light, 1969. Off central California, 30–70 m, in association with ampharetid polychaetes. 34. Polydora neocaeca Williams and Radashevsky, 1999. Western North Atlantic, Rhode Island, intertidal and shallow subtidal; bores into living gastropod shells and those occupied by hermit crabs, bivalve shell fragments. 35. Polydora nuchalis Woodwick, 1953. Pacific Ocean: Central California to Gulf of California (Mexico), intertidal, may form dense assemblages. Fide Blake 1996. 36. Polydora pacifica Takahashi, 1937. Central Pacific, Palau, bores into oyster shells. 37. Polydora paucibranchis Ehlers, 1913. Kerguelan Islands. 38. Polydora posthamata Jones, 1962. Madeira. Renamed by Jones 1962 to replace Polydora hamata Langerhans, 1880, a homonym of P. hamata Webster, 1879, the latter now referred to Boccardiella. 39. Polydora punctata Hartmann-Schröder, 1959. Pacific Ocean, El Salvador. 40. Polydora pygidialis Blake and Woodwick, 1972. Pacific Ocean, British Columbia to central California, intertidal to 90 m, bores into calcareous substrates. Fide Blake 1996. 41. Polydora quintanarooensis Delgado-Blas, 2008. Southern Gulf of Mexico, in rocks. 42. Polydora rickettsi Woodwick, 1961. Pacific Ocean, western Mexico; Southwest Chile; Brazil; intertidal and shallow subtidal, bores into shells, barnacles, gastropods, and commercial bivalves. Fide Woodwick 1961 (original description, Mexico); Blake 1983 (first record from Chile, from gastropod shells); Sato-Okoshi and Takasuka 2001 (second record from Chile, shells of molluscs); Radashevsky and Cárdenas 2004 (third record from Chile, details of morphology and biology including description of larval development from egg

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through metamorphosis); Bertrán et  al. 2005 (Chile, studies on infestation in Crepidula); Radashevsky et al. 2006 (first record from Brazil). 43. Polydora robi Williams, 2000. Philippines, bores into gastropod shells occupied by hermit crabs. Fide Williams 2001. 44. Polydora spondylana Mohammad, 1973. Arabian Gulf, Kuwait, subtidal, 2–3 m, in blue-black, nacreous “blister” on the inner surface of the shell of the thorny oyster Spondylus sp. 45. Polydora spongicola Berkeley and Berkeley, 1950. Intertidal to low subtidal; tubes in sponges. Pacific Ocean, British Columbia to California; Northwest Pacific. Fide Woodwick 1963b; Blake 1996. [Polydora uschakovi Buzhinskaja, 1971] Fide Radashevsky 1993. 46. Polydora triglanda Radashevsky and Hsieh, 2000. Taiwan, intertidal and shallow subtidal; bores into shells of oysters. Fide Radashevsky and Hsieh 2000a. 47. Polydora umangivora Williams, 2001. Philippines and Indonesia, intertidal in shells occupied by hermit crabs. 48. Polydora villosa Radashevsky and Hsieh, 2000. Taiwan, bores into living coral. Fide Radashevsky and Hsieh 2000a. 49. Polydora vulgaris Mohammad, 1972. Arabian Gulf, Kuwait, bores into shells of pearl oysters. 50. Polydora websteri Hartman in Loosanoff and Engle, 1943. Type-locality, US Atlantic Ocean, Long Island Sound, Connecticut, intertidal, bores into oyster shells. Global distribution: Pacific Ocean, Australia, New Zealand, California to Panama; Gulf of Mexico; US Atlantic coast. Likely an invasive species, distributed with cultured oysters where it bores U-shaped burrows and may form mud blisters. Fide Radashevsky and Williams 2000; Read 2010. 51. Polydora wobberi Light, 1970. Pacific Ocean, Mexico, Bahia de San Francisquito, Baja California, shallow subtidal, associated with Lophogorgia sp. 52. Polydora wolokowensis Zachs, 1925. Arctic Ocean, Kola Fjord. 53. Polydora woodwicki Blake and Kudenov, 1978. Australia, Victoria, Port Phillip Bay, bores into abalone shells. Polydorella Augener, 1914 Type species: Polydorella prolifera Augener, by monotypy. Five species Diagnosis (modified from Williams 2004): Body short, with only 14 to 16 segments (Fig. 7.4.1.40 A, B). Prostomium with anterior incision (Fig. 7.4.1.40 A) or rounded; caruncle short, extending posteriorly to segment 2 (Fig. 7.4.1.40 A) or absent. Segment 1 with small notopodia or notopodia entirely absent, without notochaetae; neuropodia present,

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 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.40: Polydorella stolonifera. A, entire worm, dorsal view; B, SEM of entire worm, dorsolateral view; C, SEM of fascicle of pennoned (bristle-tipped) and simple spines from chaetiger 5; D–F, pennoned (bristle-tipped) spines from chaetiger 5; G, simple spine from chaetiger 5; H, neurochaeta from chaetiger 5; I, neuropodial hooded hook. A, D–I, after Blake and Kudenov (1978); B, C, originals. Scale bars: A, B, 200 µm; C–I, 20 µm. Abbreviations: br, branchia; car, caruncle; pa, palp; pr, prostomium; pyg, pygidium.

with minute neurochaetae or neurochaetae absent. Segments 2 to 4 with simple, capillary neurochaetae or acicular spines accompanied by capillaries. Segment 5 modified with two types of spines arranged in a double row: dorsal row simple, falcate to straight (Fig.  7.4.1.40  C, G); ventral row with expanded distal end, bearing denticulate edge, bristles (Fig. 7.4.1.40 C–F) or digitiform bosses; with or without capillary notochaetae; with neurochaetae in form of acicular spines and/or capillaries (Fig. 7.4.1.40 H). Neuropodial bidentate hooded hooks from segment 8; approximately right angle between main fang and shaft, narrow angle between main fang and apical tooth, with constriction on shaft (Fig.  7.4.1.40  I); without accompanying capillaries. One or two pairs of branchiae from segment 7 (Fig. 7.4.1.40 A, B) or absent. Pygidium reduced (Fig.  7.4.1.40  A). Asexual reproduction via paratomy; growth zone between segments 10 and 11 or 11 and 12 (see Fig. 7.4.1.12 A–F). Constructs tubes on surfaces of sponges.

Remarks: All known species of Polydorella are small, usually less than 2 mm but no more than 4 mm long, and live on the surface of sponges where they construct mud tubes; all species exhibit paratomic asexual reproduction (see discussion in Asexual Reproduction). Evidence of sexual reproduction with egg capsules in the tubes or eggs in the body females has been observed in P. kamakamai, P. prolifera, and P. smurovi and likely occurs in the other species. A summary of the morphology and biology of these species was presented by Williams (2004). 1. Polydorella dawydoffi Radashevsky, 1996. South China Sea, Vietnam and Thailand; Philippines; Red Sea. Fide Radashevsky 1996; Williams 2004. 2. Polydorella kamakamai Williams, 2004. Philippines, shallow subtidal from sponges (Clathria cervicornis). 3. Polydorella prolifera Augener, 1914. Australia, West Australia; Queensland, Lizard Island, Great Barrier Reef. Fide Blake and Kudenov 1978; Radashevsky 2015.



4. Polydorella smurovi Tzetlin and Britayev, 1985. Red Sea, Eritrea, underwater coral bank near Dahlak Archipelago, 25 m, on a red sponge. 5. Polydorella stolonifera (Blake and Kudenov, 1978). Australia, Victoria, Western Port Bay, Crawfish Rock, 5 m, on sponges. Fide Blake and Kudenov 1978; Williams 2004. Pseudopolydora Czerniavsky, 1881 Type species: Polydora antennata Claparède, 1870, by original designation. 25 species Synonyms: Carazzia Mesnil, 1896. Type species: Polydora antennata Claparède, 1870, by original designation. Neopygospio Berkeley and Berkeley, 1954. Type species: Neo­ pygospio laminifera Berkeley and Berkeley, 1954, by monotypy (= Pseudopolydora kempi Southern). Fide Banse, 1972.

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Diagnosis (modified from Blake 1996): Prostomium entire (Fig. 7.4.1.41 D) or incised (Fig. 7.4.1.41 A) anteriorly, extending posteriorly as caruncle (Fig. 7.4.1.41 A, D); occipital antenna present (Fig. 7.4.1.41 A, D) or absent; eyespots present or absent. Chaetiger 1 generally reduced, with or without notochaetae. Chaetiger 5 not distinctly enlarged with noto- and neuropodia often well-developed with postchaetal lamellae and spreading fascicles of capillaries (Fig.  7.4.1.41  C, F); curved row of heavy spines of two types with anterior row pennoned (Fig.  7.4.1.41  H, J), posterior row simple spines (Fig.  7.4.1.41  G, I), or single type with companion chaetae; modified chaetae often arranged in J- or U-shaped fascicles. Posterior notopodial spines or hooks present or absent. Neuropodial hooded hooks from chaetiger 8, bidentate, secondary tooth closely applied to main fang, with constriction on shaft (Fig.  7.4.1.41  K); accompanying capillaries present or absent. Branchiae first

Fig. 7.4.1.41: Pseudopolydora species. A–C, G, H, P. kempi: A, anterior end, dorsal view; B, posterior end, dorsal view; C, modified chaetiger 5, anterior view; G, simple spine from chaetiger 5; H, pennoned chaeta from chaetiger 5. D–F, I–K, P. paucibranchiata: D, anterior end, dorsal view; E, posterior end, dorsal view; F, modified chaetiger 5, anterior view; I, simple spine from chaetiger 5; J, pennoned spine from chaetiger 5; K, hooded hook. A–K, original; C, F, modified from Light (1978). Scale bars: A, B, 500 µm; D, E, 250 µm; G–J, 20 µm; K, 10 µm. C, F, not to scale. Abbreviations: br, branchia; car, caruncle; neCh, neurochaetae; noCh, notochaetae; ocAn, occipital antenna; pa, palp; pr, prostomium; pyg, pygidium.

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appear posterior to chaetiger 5 (Fig.  7.4.1.41  A, D). Pygidium enlarged or reduced, disclike (Fig. 7.4.1.41 B), collarlike (Fig. 7.4.1.41 E), or divided into lobes or small lappets. Remarks: The species of Pseudopolydora are among the least modified of the Polydora complex. The majority of the 25 species occur in the Indo-Pacific region; P. antennata and P. pulchra were described from Europe; some reports of P. antennata from global localities have now been determined to represent additional species (Simon et al. 2017). Two species, P. kempi and P. pauci­ branchiata, are common and often dominant in the tidal flats of California bays and estuaries (Blake and Woodwick, 1975; Blake and Ruff 2006), but also occur widely around the north Pacific Rim and are reported from Australia (Blake and Kudenov 1978). P. paucibranchiata has also been reported from New Zealand (Read 1975) and has been introduced into Europe (Ramberg and Schram 1982). Woodwick (1964) described three species from the Marshall Islands; Radashevsky and Hsieh (2000) described six species from Taiwan. New species from Brazil, South Africa, and Japan were recently described by Radashevsky and Migotto (2009), Simon (2009), and Simon et al. (2017). 1. Pseudopolydora achaeta Radashevsky and Hsieh, 2000. Taiwan; Kinmen Island off Mainland China; intertidal in brackish water sediments. 2. Pseudopolydora antennata (Claparède, 1869). Mediterranean Sea; North Atlantic coasts of Europe; South Africa. 3. Pseudopolydora bassarginensis (Zachs, 1933). Sea of Japan. No recent records. 4. Pseudopolydora corallicola Woodwick, 1964. Central Pacific Ocean, Marshall Islands, Eniwetok, in coral rock. 5. Pseudopolydora corniculata Radashevsky and Hsieh, 2000. Taiwan, intertidal in brackish water sediments. 6. Pseudopolydora dayii Simon, 2009. South Africa, south and southeast coasts, intertidal, forms tubes on surface of gastropods and bivalves. 7. Pseudopolydora diopatra Hsieh, 1992. Taiwan, intertidal and shallow subtidal in mud, hard surfaces, above ground tube caps of Diopatra. Fide Radashevsky and Hsieh 2000b. 8. Pseudopolydora eriyali Simon, Sato-Okoshi and Abe, 2017. South Africa, intertidal. 9. Pseudopolydora floridensis Delgado-Blas, 2008. Atlantic Ocean, Lake Worth, Florida, in sediments. 10. Pseudopolydora gigeriosa Radashevsky and Hsieh, 2000. Taiwan, intertidal in brackish water sediments. 11. Pseudopolydora glandulosa Blake and Kudenov, 1978. Australia, Queensland to Victoria, intertidal in sediment. 12. Pseudopolydora hutchingsae Simon, Sato-Okoshi and Abe, 2017. South Australia, intertidal. 13. Pseudopolydora kempi (Southern, 1921). Indian Ocean: India; Pacific Ocean: Japan, Taiwan, Australia,

Queensland to New South Wales; British Columbia to California, intertidal in soft sediments. [Neopygospio laminifera] Berkeley and Berkeley, 1954. British Columbia. 14. Pseudopolydora novaegeorgiae (Gibbs, 1971). Solomon Islands, shallow subtidal, in mud. Fide Radashevsky 1996. 15. Pseudopolydora paucibranchiata (Okuda, 1937). Pacific Ocean, widespread: California; Japan; Taiwan; Australia, Queensland and New South Wales; introduced into Europe. [Polydora orientalis Annenkova, 1937]. Sea of Japan. Fide Radashevsky 1993. 16. Pseudopolydora pigmentata Woodwick, 1964. Central Pacific Ocean, Marshall Islands, Eniwetok, in coral rock. 17. Pseudopolydora primigenia Blake, 1983. Off Ecuador, 8–10 m. 18. Pseudopolydora pulchra (Carazzi, 1893). Widely distributed in European waters. 19. Pseudopolydora reishi Woodwick, 1964. Central Pacific Ocean, Marshall Islands, Eniwetok, in coral rock in sand. 20. Pseudopolydora reticulata Radashevsky and Hsieh, 2000. Taiwan, intertidal in brackish water sediments. 21. Pseudopolydora rosebelae Radashevsky and Migotto, 2009. Brazil, subtidal, 3–8 m, on muddy-sand substrates. 22. Pseudopolydora tsubaki Simon, Sato-Okoshi and Abe, 2017. Japan, Izu-Oshima, Habu Port, intertidal. 23. Pseudopolydora uphondo Simon, Sato-Okoshi and Abe, 2017. South Africa, intertidal. 24. Pseudopolydora ushioni Simon, Sato-Okoshi and Abe, 2017. Japan, Kochi Prefecture, Uranouchi Bay, intertidal. 25. Pseudopolydora vexillosa Radashevsky and Hsieh, 2000. Taiwan, intertidal in brackish water sediments. Tripolydora Woodwick, 1964 Type species: Tripolydora spinosa Woodwick, 1964, by monotypy. Monotypic Diagnosis: Prostomium rounded anteriorly, extending posteriorly as broad caruncle to segment 3 (Fig. 7.4.1.42 A); eyespots present, usually faded; occipital antenna absent; nuchal organs a pair of ciliary bands, alongside caruncle, continuing to chaetiger 4, merging with transverse ciliary band (Fig.  7.4.1.42  A). Chaetiger 1 reduced, without notochaetae or podial lobes. Branchiae from chaetiger 2 to end of body (Fig.  7.4.1.42  A, B); shortest on chaetigers 2 to 6, reaching full size on chaetiger 7; transverse ciliary bands from between branchiae from chaetiger 4. Venter of anterior chaetigers with transverse row of two to four glandular organs. Chaetigers 4 and 6 with superior row of slender capillaries and anterior row of distinct capillaries with swollen



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Fig. 7.4.1.42: Tripolydora spinosa. A, anterior end, dorsal view; B, posterior end, dorsal view; C modified notochaetae from chaetiger 4; D, E, major spines from chaetiger 5; F, anterior row capillary notochaeta from chaetiger 7; G, posterior row notochaetae from chaetiger 7; H, fascicle of two neuropodial hooded hooks, two capillaries, and one inferior sabre chaeta; I, tridentate neuropodial hooded hook. All after Blake and Woodwick (1981). Scale bars: A, B, 200 µm; C–I, 20 µm. Abbreviations: br, branchia; car, caruncle; nuO, nuchal organ; per, peristomium; pr, prostomium; pyg, pygidium; tcb, transverse ciliary band.

or inflated wings (Fig.  7.4.1.42  C). Chaetiger 5 only slightly larger than chaetigers 4 and 6 (Fig. 7.4.1.42 A), with similar appearing noto- and neuropodial lamellae; notochaetae include an anterior row of three to four modified spines with single apical tooth and two lateral knobs appearing as a subterminal collar or flange in some angles; (Fig. 7.4.1.42 D–E); spines accompanied by superior and posterior rows of capillaries similar in appearance to those of chaetigers 4 and 6. Capillaries of anterior row of chaetiger 9 bilimbate (Fig.  7.4.1.42  F); posterior row capillaries of chaetigers 7 and 8 with wings consisting of distinct ribs (Fig. 7.4.1.42 G). Posterior notopodial spines absent. Neuropodial hooded hooks tridentate with the main fang at a right angle to the shaft, with two apical teeth closely applied (Figs. 7.4.1.4 M; 7.4.1.42 H, I), sometimes difficult to observe separately, shaft smooth, curved, with no constriction and manubrium, present from chaetiger 9; hooks accompanied by capillaries and ventral sabre chaeta (Fig. 7.4.1.42 H). Pygidium with two ventral lobes and two dorsal cirri (Fig. 7.4.1.42 B). Anterior part of digestive tract without gizzardlike structure.

Remarks: Tripolydora spinosa is an entirely unique polydorid and in several respects has similarities with the genus Microspio as suggested by Blake (1979c), Blake and Woodwick (1981), and Radashevsky (2015). These include branchiae from chaetiger 2, including chaetiger 5, and continuing to the end of the body; the presence of tridentate hooded hooks from chaetiger 9; presence of neuropodial inferior sabre chaetae, and rows of glands on anterior segments of the venter. Swollen or enlarged capillaries occur on chaetigers 4 to 6, but are reduced somewhat on chaetiger 5 where three to four enlarged notopodial spines are present. Blake (1983) noted that Microspio paradoxa had thickened capillaries arranged in a U-shape on chaetigers 4 to 5 and suggested a similarity to rows of modified spines on chaetiger 5 in polydorids. A similar undescribed species of Microspio is known from Bermuda (Blake unpublished). Articles providing descriptive data on T. spinosa include Woodwick (1964), Blake and Woodwick (1981), Hartmann-Schroder (1992), Williams (2001), and Radashevsky (2015).

82 

 7.4 Sedentaria: Sabellida/Spionida

1. Tripolydora spinosa Woodwick, 1964. Central and South Pacific Ocean associated with coral and coral rubble; Marshall Islands (type locality, Eniwetok Atoll), Cook Islands, Easter Island; Hawaiian Islands; Philippines; Australia, Great Barrier Reef; Indian Ocean, Seychelles.

Spioninae: Genera Pygospio, Microspio, and Spio Pygospio Claparède, 1863 Type species: Pygospio elegans Claparède, 1863, by monotypy. Three species

Fig. 7.4.1.43: Pygospio species. A–D, P. californica: A, juvenile, entire worm, dorsal view; B, anterior end, dorsal view; C, neuropodial hooded hook; D, pygidial lobes, posterior view. E–I, P. elegans: E, juvenile, entire worm, dorsal view; F, anterior end, dorsal view; G, neuropodial hooded hook; H, modified neuropodial “spoon” hook; I, pygidium. A, after Blake (2006); B–D, after Hartman (1936); E, after Rasmussen (1973); F, G, I after Hartmann-Schröder (1996); H, after Light (1978). Not to scale. Abbreviations: br, branchia; per, peristomium; pr, prostomium; pyg, pygidium.



Diagnosis: Prostomium conical or rounded anteriorly (Fig. 7.4.1.43 A, B), or weakly incised (Figs. 7.4.1.1 F; 7.4.1.43 E, F); frontal horns absent; occipital tentacle present or absent; eyespots present. Branchiae present posterior to chaetiger 10 (Fig. 7.4.1.1 F), fused with notopodial postchaetal lamellae; males with an additional simple pair of branchiae on chaetiger 2, not fused to notopodial lamellae (Figs. 7.4.1.1 F; 7.4.1.43 B). Notochaetae all capillaries; neurochaetae include capillaries and bidentate hooded hooks (Fig. 7.4.1.43 C, G); P.  elegans with some chaetigers having unusual spoonshaped neuropodial hooks (Fig.  7.4.1.43  H) in addition to typical bidentate hooded hooks. Pygidium with four thick, glandular lobes (Figs. 7.4.1.1 F; 7.4.1.43 A, D, E, I). Remarks: There are three valid species of Pygospio: the type species P. elegans, which is opportunistic and widely distributed throughout the northern hemisphere (Radashevsky et al. 2016b; Thonig et al. 2016), P. californica, which is known only from central California (Hartman 1936; Blake 1996), and P. muscularis from Hawaii (Ward 1981). Both P. elegans and P. californica are common in high intertidal habitats in California, with the latter species found at the highest levels of intertidal sand flats in bays and estuaries. Both species were thoroughly reviewed and redescribed by Light (1978) and may be readily distinguished on the basis of prostomial shape, form and distribution of hooded hooks, and pigment. A possible undescribed species from Oregon, USA, was identified by Radashevsky et al. (2016b) from Oregon using molecular sequences. Both P. elegans and P. californica reproduce by architomic asexual reproduction (Armitage 1979; Blake 2006). Larval development has been described for P. elegans (see Hannerz 1956; Rasmussen 1973). Pelagic larvae have been described for P. californica (Blake 2006). 1. Pygospio californica Hartman, 1936. California, intertidal. 2. Pygospio elegans Claparède, 1863. Widespread, intertidal. 3. Pygospio muscularis Ward, 1981. Hawaii, intertidal. Microspio Mesnil, 1896 Type species: Spio mecznikowianus Claparède, 1869, designated by Söderström, 1920. 20 species Synonym: Mesospio Gravier, 1911. Type species: Meso­ spio moorei Gravier, 1911, by monotypy. Fide Blake 1983. Diagnosis: Prostomium rounded (Fig.  7.4.1.44  A, E) or bilobed (deeply incised) (Fig. 7.4.1.44 G) anteriorly, frontal or lateral horns absent; eyespots present or absent; occipital antenna present or absent. Nuchal organs typically as bands lateral to caruncle; M. hartmanae with bilobed posterior extension of caruncle and nuchal organs over chaetigers 2 to 3 (Fig. 7.4.1.44 E); metameric dorsal ciliated organs

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 83

often present. Transverse ciliary bands present between bases of branchiae on some species (Fig.  7.4.1.44  E). Branchiae from chaetiger 2 (Fig. 7.4.1.44 A, E, G), limited to anterior region of body or continuing to posterior end, partly fused to bases of postchaetal notopodial lamellae. Ventral epidermal glands present or absent. Notochaetae capillaries of various types (Fig.  7.4.1.44  H–L); notopodial spines present (Fig. 7.4.1.44 D) or absent; neurochaetae include capillaries, hooded hooks, and ventral sabre chaetae; hooks bi-, tri-, or multidentate (Fig.  7.4.1.44  C, M). Pygidium with two to four anal cirri (Fig. 7.4.1.44 B, F), usually with bacillary glands. Remarks: Microspio is distinguished from Spio by having branchiae first present from chaetiger 2 instead of chaetiger 1. On the other hand, Söderström (1920) separates both genera based on the number of ciliary bands constituting the metameric dorsal ciliated organs. According to Söderström’s diagnosis, two bands are found in Microspio and four bands are found in Spio. This problem is not fully resolved and the assignment of several species to either Spio or Microspio still needs to be validated (see, e.g., Bick and Meißner 2011 for summary). Most species of Microspio have conspicuous bacillary glands on the noto- and neuropodial postchaetal lamellae and anal cirri. The genus was reviewed by Maciolek (1990), who listed 15 species as valid. Currently, 20 species are referred to Microspio. 1. Microspio africana Rullier, 1964. Atlantic Ocean, Cape Verde Islands. 2. Microspio atlantica (Langerhans, 1881). Atlantic Ocean, Madeira. 3. Microspio elegantula Blake, 1984. New Zealand, North Island, intertidal. 4. Microspio granulata Blake and Kudenov, 1978. New South Wales, Botany Bay. 5. Microspio gracilis (Hartmann-Schröder, 1962). Argentina, intertidal. Fide Blake 1983. 6. Microspio hartmanae Blake, 1983. Argentina, coarse sediments, 18–26 m. 7. Microspio kussakini Chlebovitsch, 1959. Northwest Pacific Ocean, Kuril Islands, intertidal. 8. Microspio maori Blake, 1984. New Zealand, North and South Islands, intertidal. 9. Microspio mecznikowianus (Claparède, 1869). Widespread in European waters. 10. Microspio microcera (Dorsey, 1977). Pacific Ocean, Southern California; Atlantic Ocean, off North Carolina. 11. Microspio minuta (Hartmann-Schröder, 1962). Gala­ págos Islands; Chile; intertidal to 18 m. 12. Microspio moorei (Gravier, 1911). Antarctica. Fide Blake 1983. 13. Microspio multidentata Zhou, Ji and Li, 2009. East China Sea, intertidal.

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 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.44: Microspio species. A–D, M. pigmentata: A, anterior end, dorsal view; B, posterior end, dorsal view; C, neuropodial hooded hook; D, posterior notopodial spine. E, F, M. hartmanae: E, anterior end, dorsal view; F, posterior end, dorsal view. G–M, M. paradoxa: G, anterior end, dorsal view; H, superior dorsal capillary, chaetiger 5; I, modified capillary from anterior row; J, same, posterior row; K, notched capillary notochaeta from anterior row of chaetiger 8; L, bristled capillary notochaeta from posterior row of chaetiger 8; M, tridentate hooded hook, lateral view. A–D, after Maciolek (1990); E, F, G–M, after Blake (1983). Scale bars: A, B, E, F, 200 µm; G, 300 µm; C, D, 10 µm; H–M, 20 µm. Abbreviations: anC, anal cirrus; br, branchia; car, caruncle; nuO, nuchal organ; per, peristomium; pr, prostomium; pyg, pygidium; tcb, transverse ciliary band.

14. Microspio occipitalis Hartmann-Schröder, 1983. Australia, West Australia, intertidal. 15. Microspio paradoxa Blake, 1983. Galapágos Islands, 18 m. 16. Microspio pigmentata (Reish, 1959). Pacific Ocean, Southern California. 17. Microspio profunda Maciolek, 1990. Western North Atlantic, New England to Delaware; Bahamas; 1760–3600 m. 18. Microspio rolasiana Augener, 1918. Atlantic Ocean, western Africa. 19. Microspio spinosa Blake, 1996. Pacific Ocean, California continental shelf, 90–150 m. 20. Microspio tetrabranchia Maciolek, 1990. Western North Atlantic, off North and South Carolina, 584–807 m.

Spio Fabricius, 1785 Type species: Nereis filicornis Müller, 1776, designated by Söderström, 1920. 36 species Synonyms: Paraspio Czerniavsky, 1881. Type species: Spio decoratus Bobretzky, 1870, by monotypy. Euspio McIntosh, 1915. Type species: Euspio mesnili McIntosh, 1914. Diagnosis (emended from Bick and Meißner 2011): Prostomium anteriorly rounded (Figs. 7.4.1.1 I; 7.4.1.45 G), truncate (Fig.  7.4.1.45  L), or slightly incised (Fig.  7.4.1.45  A), lacking frontal or lateral horns; eyespots present or absent; occipital antenna absent, but posterior portion of prostomium may be raised or inflated. Nuchal organ with short median and long lateral ciliary bands,



extending to chaetiger 2 or 3 (Fig. 7.4.1.45 A). Metameric dorsal ­ciliated organs usually present; transverse dorsal ciliated bands present (Figs. 7.4.1.3 G, I, J; 7.4.1.45 A, N). Branchiae present from chaetiger 1 (Fig.  7.4.1.45  A, G, L–N), continuing almost throughout the body, completely separate from or basally fused with notopodial lamella (Fig. 7.4.1.45 H), often reduced in size on chaetiger 1. Ventral epidermal glands usually present in anterior and middle chaetigers (Fig.  7.4.1.3  H). Notochaetae and anterior neurochaetae all capillaries (Fig. 7.4.1.45 I); capillaries (Fig. 7.4.1.45 C), hooded hooks (Fig. 7.4.1.45 E, K, O, P), and inferior sabre chaetae (Fig. 7.4.1.45 D, J) on middle and posterior neuropodia. Pygidium with four anal cirri (Fig. 7.4.1.45 B). Remarks: The most important reviews of Spio are by Maciolek (1990), Bick et al. (2010), Meißner et al. (2011), and Bick and Meißner (2011). Maciolek (1990) summarized the taxonomic characters of the 25 then known species of Spio. Spio is distinguished from Microspio in having branchiae first present from chaetiger 1 instead of chaetiger 2. The consistency of this character was emphasized by Blake and Kudenov (1978) and Maciolek (1990), who argued strongly for the retention of two genera largely based on the occurrence of the first pair of branchiae (but see also under remarks for Microspio). Bick et al. (2010) reviewed species of Spio from northern Europe, including records referred to the type species S. filicornis, and identified at least six species from the area, two of which were similar to S. filicornis. Meißner et al. (2011) resolved the identity of S. filicornis by collecting specimens from the type locality near Paamiut, southwest Greenland, and designating a neotype. In addition to providing a redescription of the type species, two species previously referred to S. filicornis from northern Europe in Bick et al. (2010) were described as new. Bick and Meißner (2011) redescribed several poorly known species from the northwestern Pacific. At present, 36 species of Spio are recognized. Ecologically, species of Spio are more commonly found in coastal and continental shelf depths, whereas Microspio species occur from intertidal to slope depths (Maciolek 1990). 1. Spio aequalis Ehlers, 1904. Southern Ocean, Chatham Island. 2. Spio africana (Rullier, 1964). Atlantic Ocean, Cape Verde Islands. Fide Maciolek 1990. 3. Spio armata (Thulin, 1957). Baltic Sea, Øresund, North Sea, Norwegian Sea, Arctic Ocean, subtidal in sand and clay. 4. Spio arndti Meißner, Bick and Bastrop, 2011. Western Baltic Sea. 5. Spio bengalensis Willey, 1908. Indian Ocean.

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 85

6. Spio blakei Maciolek, 1990 (replacement name for S. pacifica Blake and Kudenov, 1978, preoccupied). Australia, Queensland, New South Wales, Victoria. 7. Spio borealis Okuda, 1937. Japan. 8. Spio butleri Berkeley and Berkeley, 1954. Eastern North Pacific. British Columbia. 9. Spio celata Dalyell, 1853. Scotland. 10. Spio cirrifera (Banse and Hobson, 1968). Eastern North Pacific, Puget Sound, Washington. 11. Spio decoratus Bobretzky, 1870. North Sea, Black Sea, Mediterranean Sea, northeast Atlantic Ocean, Arctic Ocean, subtidal in coarse sediments. 12. Spio filicornis (Müller, 1776). Western Greenland (type locality). Fide Meißner et al. (2011). 13. Spio goniocephala Thulin, 1957. Baltic Sea, North Sea, Baffin Island, subtidal in mixed sediments. 14. Spio gorbunovi Averincev, 1990. Arctic Ocean, Laptev Sea. 15. Spio kurilensis Buzhinskaya, 1990. Northwest Pacific Ocean, Kuril Islands, shallow subtidal. 16. Spio limicola Verrill, 1879. Western North Atlantic, New England, Massachusetts. 17. Spio maciolekae Blake, 1996. Pacific Ocean, California continental shelf, 90–150 m. 18. Spio maculata (Hartman, 1961). Southern California. Eastern North Pacific, California to Mexico in shelf depths. 19. Spio malmgreni Sikorski in Jirkov, 2001. Arctic Ocean. 20. Spio martinensis Mesnil, 1896. Baltic Sea, North Sea, Northeast Atlantic Ocean, Arctic Ocean, subtidal in mixed sediments. 21. Spio mesnili Augener, 1914. Australia, West Australia, Sharks Bay. 22. Spio multioculata (Rioja, 1918). Spain. 23. Spio obtusa Ehlers, 1913. Antarctica, McMurdo Sound, 385 m. Species has not been recorded since original account. 24. Spio parva (Dalyell, 1853). UK. Questionable. Not reported since original account. 25. Spio pettiboneae Foster, 1971. Gulf of Mexico; off North Carolina. 26. Spio picta Zachs, 1933. Northwest Pacific Ocean, Peter the Great Bay, Sea of Japan, Sea of Okhotsk, intertidal to shallow subtidal. 27. Spio quadrisetosa Blake, 1983. Argentina, intertidal in sand. 28. Spio readi Blake, 1984. New Zealand. New Zealand, North and South Island, intertidal to 105 m. 29. Spio setosa Verrill, 1873. Western North Atlantic, New England. 30. Spio singularis Blake and Kudenov, 1978. Australia, Queensland, Moreton Bay.

86 

 7.4 Sedentaria: Sabellida/Spionida



31. Spio symphyta Meißner, Bick and Bastrop, 2011. North Sea. 32. Spio theeli (Söderström, 1920). Arctic Ocean. Fide Maciolek 1990. 33. Spio thulini Maciolek, 1990. Western North Atlantic Ocean, off New England. 34. Spio tridentata Hutchings and Turvey, 1984. Australia, South Australia. 35. Spio tzetlini Sikorski in Jirkov, 2001. Arctic Ocean. 36. Spio unidentata Chlebovitsch, 1959. Northwest Pacific Ocean, Kuril Islands, shallow subtidal. Clade Pygospiopsis, Atherospio, and Pseudatherospio, three closely related genera Pygospiopsis Blake, 1983 Type species: Pygospio dubia Monro, 1930; designated by Blake. Gender feminine. Six species Synonym: Pseudatherospio Lovell, 1994. Fide Blake and Maciolek (2018). Diagnosis (after Blake and Maciolek 2018): Prostomium longer than wide, sometimes bell-shaped, flaring anteriorly, with bilobed frontal margin (Fig. 7.4.1.46 A, D), frontal horns absent; occipital antenna present (Fig. 7.4.1.46 A, D); eyespots present or absent. Branchiae from chaetiger 1, 2, or 7, or on chaetiger 2, 2–3, 4–6, or, and resuming on chaetiger 7 (Fig. 7.4.1.46 A), continuing posteriorly; branchiae either basally (Fig.  7.4.1.46  E) or entirely fused to membranous notopodial postchaetal lamellae (Fig.  7.4.1.46  F) except for branchiae anterior to chaetiger 7 that are generally simple and free from notopodial lamellae. Interparapodial pouches and dorsal crests absent. Notochaetae all capillaries (Fig.  7.4.1.46  G). Neurochaetae include simple capillaries, some with distinct fringe of fibrils along one edge, or weakly aristate, but not heavily modified (Fig. 7.4.1.46 H). Hooks in middle and posterior chaetigers, unhooded, unidentate (Fig. 7.4.1.46 C) or weakly bidentate, shaft more or less straight and short, subapical tooth on concave side (Fig. 7.4.1.46 I); inferior sabre chaetae absent. Pygidium surrounded by ring of anal cirri (Fig. 7.4.1.46 B). Remarks: Pygospiopsis was established by Blake (1983) for Pygospio dubia Monro, a subantarctic species that differed

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 87

from Pygospio species by having unidentate unhooded instead of hooded neuropodial hooks and a pygidium surrounded by anal cirri rather than four lobes. Subsequently, Mackie and Duff (1986) Atherospio disticha from off Scotland which had modified anterior neurochaetae. These species have more or less similar prostomial shapes, an occipital antenna, modified anterior neurochaetae, branchiae that are either basally or entirely fused to notopodial lamellae, and unusual neuropodial hooded or unhooded hooks with a small tooth or knob on the concave side and subapical to the terminal shaft or main fang. In other spionids, the small tooth (teeth) is (are) superior to the main fang on the convex side. In both P. dubia and A. disticha, the shaft of these hooks is more or less straight or only gently curved. The major differences between these genera lie with branchial distribution. In Pygospiopsis dubia, slender branchiae occur on chaetigers 2 and 3, then are absent on chaetigers 4–6, with heavier branchiae basally fused to notopodial lamellae from chaetiger 7 and continuing for 9–10 chaetigers. In P. occipitalis, a species described by Blake (1996) branchiae also occur from chaetiger 2, mostly separate from the notopodial lamellae; these branchiae continue on following segments with increasing fusion with the notopodial lamellae; by chaetiger 7, the branchiae and lamellae are mostly fused along their length. In A. disticha, thickened branchiae are fully fused with the dorsal lamellae from chaetiger 7, and are present for six chaetigers; there are no branchiae anterior to chaetiger 7. The same branchial arrangement is present in A. guillei redescribed by Meißner and Bick (2005). In P. fauchaldi, a species described by Lovell 1994), branchiae are first present from chaetiger 1, continuing posteriorly to near the end of the body; these branchiae are basally fused with notopodial lamellae over most of the body, and fully fused from chaetiger 7. Blake and Maciolek (2018) described three additional species of Pygospiopsis and redefined the genus with individual species having a variety of branchial distributional patterns anterior to to chaetiger 7. Blake (1996) described a new species of Pygospiopsis, P. occipitalis from slope depths of 930 m off California. This species differed from P. dubia in having branchiae from chaetigers 2 to 12–14 without a gap between chaetigers 3 and 6. Blake and Maciolek (2018) described three new

◂ Fig. 7.4.1.45: Spio species. A–F, S. filicornis: A, anterior end, dorsal view; B, posterior end, dorsolateral view; C, posterior neurochaeta from posterior chaetiger; D, sabre chaeta from posterior chaetiger; E, neuropodial hooded hook from posterior chaetiger; F, anterior neurochaeta from same chaetiger. G, H, S. quadrisetosa: G, anterior end, dorsal view; H, right chaetiger 9, anterior view; I, capillary neurochaeta from anterior row of chaetiger 11; J, inferior sabre chaeta, K, neuropodial hooded hook. L, S. limicola, anterior end, dorsal view. M, S. pettiboneae, anterior end, dorsal view. N–P, S. singularis: N, anterior end, dorsal view; O, P, neuropodial hooded hook in frontal (O) and lateral views (P). A–F, after Meißner et al. (2011); G, H, after Blake (1983); L, M, after Maciolek (1990); N–P, after Blake and Kudenov (1978). Scale bars: A, G, 500 µm; B, M, 300 µm; H, L, 200 µm; N, 100 µm; C, D, F, 25 µm; E, I, J, 10 µm; K, O, P, 20 µm. Abbreviations: anC, anal cirrus; br, branchia; dcb, dorsal ciliary band; dCr, dorsal crest; neP, neuropodium; noL, notopodial lamella; noP, notopodium; nuO, nuchal organ; per, peristomium; pr, prostomium; tcb, transverse ciliary band.

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 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.1.46: Pygospiopsis species. A–C, P. dubia: A, anterior end, dorsal view; B, posterior end, dorsal view; C, neuropodial hook, from middle chaetigers. D–I, P. occipitalis: D, anterior end, dorsal view; E, chaetiger 5, anterior view; F, chaetiger 7, anterior view; G, capillary notochaeta from anterior chaetiger; H, aristate neurochaeta from chaetiger 5; I, two neuropodial hooks and capillary from middle body chaetiger. A–C, after Blake (1983); D–I, after Blake (1996). Scale bars: A, 500 µm; B, D, 300 µm; E, F, 100 µm; C–I, 20 µm. Abbreviations: anC, anal cirrus; br, branchia; dcb, dorsal ciliary band; neL, neuropodial lamella; noL, notopodial lamella; nuO, nuchal organ; ocAn, occipital antenna; pa, palp; per, peristomium; pr, prostomium; prob, proboscis.

species, P. antarctica, P. antennata, and P. profunda from the Antarctic Peninsula, northern California, and the U.S. Atlantic slope, respectively. These same authors referred Pseudatherospio fauchaldi to synonymy with Pygospiopsis based on the distribution of branchiae. The following six species are currently assigned to Pygospiopsis. 1. Pygospiopsis antarctica Blake and Maciolek, 2018. East Antarctic Peninsula, 385 m. 2. Pygospiopsis antennata Blake and Maciolek, 2018. off northern California, 1820 m. 3. Pygospiopsis dubia (Monro, 1930). Southern Ocean, South Georgia, 25 m; Eastern Antarctic Peninsula, 500 m. Fide Blake 1983, 2006 (larvae, Blake and Maciolek 2018). 4. Pygospiopsis fauchaldi (Lovell, 1994). Central and southern California, 197–530 m. 5. Pygospiopsis occipitalis Blake, 1996. California, off Point Arguello, 930 m. Fide Blake 1996 6. Pygospiopsis profunda Blake and Maciolek, 2018. U.S. Atlantic continental slope, 1509–2155. Atherospio Mackie and Duff, 1986 Type species: Atherospio disticha Mackie and Duff, 1986, by monotypy. Two species Diagnosis (after Meißner and Bick 2005): Prostomium deeply incised, longer than wide, posteriorly tapered

and not extended into a distinct caruncle; occipital antenna present or absent or minute process at the position of this antenna present. Nuchal organ small or indistinct. Dorsal branchiae on chaetiger 7 and following four to six chaetigers; branchiae with distal digitate process, outer branchial margin completely fused with notopodial postchaetal lamella. Parapodia biramous with well-developed postchaetal lamellae and alimbate, mostly hirsute, capillaries in noto- and neuropodia. Chaetigers 4 and 5 or only chaetiger 5 with modified chaetae in the neuropodium, these falcate and pointed or aristate spines, modified chaetae in irregular short row superior to several capillary chaetae. Postbranchial neuropodial hooks alongside capillaries; hooks uni-or bidentate, secondary tooth below main fang; hook distally with closely applied sheath. Notopodial hooks absent. Sabre chaetae absent but several capillaries in inferiormost position throughout the body. Interparapodial pouches absent. Pygidium surrounded by several pairs of lateral cirri. Remarks: See comments for Pygospiopsis. 1. Atherospio disticha Mackie and Duff, 1986. North Atlantic Ocean, west coast of Scotland, shallow subtidal, approximately 27 m. 2. Atherospio guillei (Laubier and Ramos, 1974). North Atlantic Ocean: North Sea; Mediterranean Sea; subtidal 40–100 m. Fide Meißner and Bick (2005).



Five monotypic genera with little or no affiliation with other spionids Glandulospio Meißner, Bick, Guggolz and Götting, 2014 Type species: Glandulospio orestes Meißner, Bick, Guggolz and Götting, 2014, by monotypy. Monotypic Diagnosis: Anterolateral horns arising subanteriorly from prostomial margin, posterior part of prostomium extended posteriorly as short caruncle terminating at the end of chaetiger 1; occipital antenna absent. Nuchal organs with two pairs of ciliary bands, continuing as metameric double-paired ciliary bands (= metameric dorsal ciliated organs) between transversal ciliated bands of consecutive segments. Branchiae present from chaetiger 1. Large glandular organs present in middle body chaetigers. Neuropodial hooded hooks with pair of apical teeth present in posterior chaetigers. Remarks: One species is known. This species has a somewhat tumid or expanded shape to the body due to the large glandular organs in middle body segments. In addition, the two frontal horns are located slightly ventral to the anterior margin of the prostomium. 1. Glandulospio orestes Meißner, Bick, Guggolz and Götting, 2014. Northeast Atlantic seamounts, approximately 300 m. Glyphochaeta Bick, 2005 Type species: Glyphochaeta laudieni Bick, 2005a, by original designation. Monotypic Diagnosis: Body not divided into different regions. Anterior margin of prostomium with frontal horns; posterior end forming a short caruncle extending to chaetiger 1; without occipital antenna; eyespots present. Nuchal organ as small ciliated patches on the posterior lateral margin of prostomium. Peristomium well developed. Branchiae absent. Postchaetal lamellae well developed only in the anterior body region. Dorsal ciliated crest present along dorsum. Lateral sensory organs absent. Notopodia with capillaries. Anterior neuropodia with capillaries; middle and posterior body with hooded hooks, replaced by grooved spines in some neuropodia of the middle body region; sabre chaetae absent. Some middle segments with glandular organs. Pygidium with four anal lobes. Remarks: Glyphochaeta laudieni is only known from the Norwegian Arctic in shallow subtidal depths (Bick 2005a). The genus and only species is characterized by a prostomium with frontal horns, the absence of branchiae and sabre chaetae, and the presence of unusually large grooved spines that replace hooded hooks in some middle body segments. These grooved spines are associated with glandular organs situated in the neuropodia and

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are suggested to drain or otherwise pass secretions from the glands out of the body. The author suggests that the species is likely related to Pygospio. 1. Glyphochaeta laudieni Bick, 2005a. Norwegian Arctic, Svalbard, Spitsbergen, 4 m. Spiogalea Aguirrezabalaga and Ceberio, 2005 Type species: Spiogalea vieitezi Aguirrezabalaga and Ceberio, 2005, by monotypy. Two species Diagnosis (after Peixoto and Paiva 2017): Prostomium anteriorly rounded or with short anterolateral projections, narrowing posteriorly, with caruncle; nuchal organs absent. Two chevron-shaped chitinous plates or single chitinous plate surrounding anterior part of prostomium; eyespots absent. Peristomium well developed forming posteriorly open collar that surrounds prostomium. Branchiae absent. Parapodia of first chaetiger reduced, lacking notopodial postchaetal lobe and with small neuropodial postchaetal lobe. Subsequent parapodia larger, well-developed with rounded noto- and neuropodial postchaetal lobes. Posterior notopodial lobes connected by low dorsal ridge or ridges absent. Notopodial chaetae all capillary or capillaries and multidentate hooded hooks on posterior chaetigers. Posterior neuropodia with long-shafted, multidentate hooded hooks, with complete hood. Sabre chaetae present. Pygidium morphology uncertain, possibly rounded with pair of small anal cirri. Remarks: Two species are known, both from deep water. Spiogalea is one of three spionid genera known to entirely lack branchiae. It is entirely unique in the presence of one or two large chitinous plates surrounding the anterior end of the broad prostomium. 1. Spiogalea capixaba Peixoto and Pava, 2017. Off Brazil, Espírito Santo Basin, Doce Canyon, 950 m. 2. Spiogalea vieitezi Aguirrezabalaga and Ceberio, 2005. Northeast Atlantic, Bay of Biscay 1000–1739 m. Spiophanella Fauchald and Hancock, 1981 Type species: Spiophanes pallida Hartman, 1961. Designated by Fauchald and Hancock (1981). Monotypic Diagnosis: Spionid species without branchiae and without enlarged, curved hooks in the first chaetiger. Anterior parapodia with well-developed noto- and neuropodial postchaetal lobes; median and posterior chaetigers with reduced lobes. Notopodia with capillary chaetae only; neuropodia in median and posterior chaetigers with hooded multidentate hooks. Remarks: This deep-water species, originally in the genus Spiophanes, was removed to a new genus, Spiophanella, by Fauchald and Hancock (1981) because neuropodial crook

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chaetae were absent from chaetiger 1. However, there is some question relative to the validity of this genus because despite the lack of branchiae, the type species, Spiophanes pallida, resembles other spionids. For example, Pettibone (1962) suggested that the species belonged to Prionospio. Sigvaldadóttir et al. (1997) stated that the genus “…is of doubtful status and requires further investigation.” In our review, the species superficially resembles Prionospio and Laonice species. 1. Spiophanella pallida (Hartman 1961). Pacific Ocean: Southern California and Western Mexico, 1675–2800 m. Fide Fauchald and Hancock 1981. Xandaros Maciolek, 1981b Type species: Xandaros acanthodes Maciolek, 1981b, by monotypy. Monotypic Diagnosis (emended): Prostomium anteriorly rounded, without posterior keel, lacking eyespots and occipital tentacle. Peristomium well-developed partly fused to chaetiger 1, not elaborated into wings or hood. Palps inserted at anterior dorsal junction of prostomium and peristomium. Chaetiger 1 uniramous, lacking notopodial lamellae and chaetae, neuropodial lamellae bilobed, with capillary chaetae. Branchiae from chaetiger 2, continuing to midbody; each elongate, cylindrical, crossed by numerous transverse rings providing wrinkled appearance. No interramal or interparapodial pouches. Notopodial chaetae all capillaries. Neuropodial capillaries of chaetigers 1 and 2 mostly replaced by unhooded, recurved acicular spines from chaetiger 3, these spines grading into bidentate hooded hooks by middle of body and continuing to last chaetiger; ventral sabre chaetae lacking. Pygidium with four unequal lobes. Remarks: This deep-water hydrothermal vent species has several unusual characters (Maciolek 1981b). A recent examination of additional specimens revealed that branchiae begin on chaetiger 2 instead of 4 as originally described. The branchiae themselves are crossed by numerous rings or wrinkles, which are unusual for a spionid, although a similar condition has been described in some species of Prionospio (Maciolek, 1985). 1. Xandaros acanthodes Maciolek, 1981b. Hydrothermal vents at the Galapagos Rift, 2447 m.

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habitats. Proceedings of the Biological Society of Washington 93: 947–962. Blake, J.A. (1983): Polychaetes of the family Spionidae from South America, Antarctica and adjacent seas and islands. Biology of Antarctic Seas XIV. Antarctic Research Series 39: 205–288. Blake, J.A. (1984): Four new species of Spionidae (Polychaeta) from New Zealand, with comments on the syntype of Spio aequalis Ehlers from Chatham Island. Proceedings of the Biological Society of Washington 97:148–159. Blake, J.A. (1986): A new species of Boccardia (Polychaeta: Spionidae) from the Galápagos Islands and a redescription of Boccardia basilaria Hartman from Southern California. Bulletin of the Southern California Academy of Sciences 85:16–21. Blake, J.A. (1996): Chapter 4. Family Spionidae Grube, 1850, including a review of the genera and species from California and a revision of the genus Polydora Bosc, 1802. In: Blake, J.A., Hilbig, B., & Scott, P.H. (Eds.). Taxonomic Atlas of the Santa Maria Basin and Western Santa Barbara Channel. Vol. 6. Annelida Part 3. Polychaeta: Orbiniidae to Cossuridae. Santa Barbara Museum of Natural History: 81–223. Blake, J.A. (2006): Spionida. In: Rouse, G. & Pleijel, F. (Eds.). Reproductive Biology and Phylogeny of Annelida. Volume  4 of Series: Reproductive Biology and Phylogeny, Series Editor, Jamieson, B.G.M., Science Publishers, Enfield, NH, pp. 566–638. Blake, J.A. (2017): Larval development of Polychaeta from the Northern California coast. Fourteen additional species together with seasonality of planktic larvae over a 5-year period. Journal of the Marine Biological Association United Kingdom 97(5): 1081–1133. Blake, J.A. & Arnofsky, P.L. (1999): Reproduction and larval development of the spioniform Polychaeta with application to systematics and phylogeny. In: Dorresteijn, A.W.C. & Westheide, W. (Eds.). Reproductive Strategies and Developmental Patterns in Annelids. Hydrobiologia 402: 57–106. Blake, J. A. & Arnofsky, P.L. (2000): Systematics and phylogeny of the spioniform Polychaeta. Bulletin of Marine Science 67: 657 (abstract). Blake, J.A. & Evans, J.D. (1973): Polydora and related genera (Polychaeta: Spionidae) as borers in mollusk shells and other calcareous substrates. The Veliger 15: 235–249. Blake, J.A. & Grassle, J.F. (1994): Benthic structure on the US South Atlantic Slope off the Carolinas: spatial heterogeneity in a current dominated system. Deep-Sea Research II 41: 835–874. Blake, J.A. & Kudenov, J.D. (1978): The Spionidae (Polychaeta) from southeastern Australia and adjacent areas, with a revision of the genera. Memoirs of the National Museum of Victoria 39: 171–280. Blake, J.A. & Kudenov, J.D. (1981): Larval development, larval nutrition, and growth for two Boccardia species (Polychaeta: Spionidae) from Victoria, Australia. Marine Ecology Progress Series 6: 175–182. Blake, J.A. & Maciolek, N.J. (1987): A redescription of Polydora cornuta Bosc (Polychaeta: Spionidae) and designation of a neotype. In: Fauchald, K. (Ed.). Papers on Polychaete Systematics in Honor of Marian H. Pettibone. Bulletin of the Biological Society of Washington 7: 11–15. Blake, J.A. & Maciolek, N.J. (1992): A new genus and two new species of Spionidae (Polychaeta) from hydrothermal vents at the Guaymas Basin and Juan de Fuca Ridge, with comments are a related species from the western North Atlantic. Proceedings of the Biological Society of Washington. 105: 723–732.

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Simon, J.L. (1968): Occurrence of pelagic larvae in Spio setosa Verrill 1873 (Polychaeta: Spionidae). Biological Bulletin 134: 503–515. Smith, H.L. & Gibson, G.D. (1999): Nurse egg origin in the polychaete Boccardia proboscidea (Spionidae). Invertebrate Reproduction and Development 35(3): 177–185. Söderström, A. (1920): Studien über die Polychätenfamilie Spionidae. Inaugural Dissertation, Almquist and Wicksells, Uppsala, 288 pp. Soulier, A. (1903): Revision des Annélides de la région de Cette. pt. 2. Mémoires de la Académie des Sciences et Lettres de Montpellier, Section des Sciences, 2e Sér. 3: 193–278. Southward, E.C., Schulze, A. & Gardiner, S.L. (2005): Pogonophora (Annelida): Form and function. In: Bartolomaeus T. & Purschke G., (Eds.). Morphology, Molecules, Evolution and Phylogeny in Polychaeta and Related Taxa. Springer, Netherlands: 227–251. Stock, M.W. (1965): Anterior Regeneration in Spionidae. Master of Science Thesis, University of Connecticut, Storrs, Connecticut. 91 pp. Storch, V. (1988): Integument. In: Westheide, W. & Hermans, C.O. (Eds.). The Ultrastructure of Polychaeta. Microfauna Marina, 4: 13–36. Struck, T.H. (2011): Direction of evolution within Annelida and the definition of Pleistoannelida. Journal of Zoological Systematics and Evolutionary Research 49: 340–345. Struck, T.H., Nesnidal, M.P., Purschke, G. & Halanych, K.M. (2008): Detecting possibly saturated positions in 18S and 28S sequences and their influence on phylogenetic reconstruction of Annelida (Lophotrochozoa). Molecular Phylogenetics and Evolution 48: 628–545. Struck, T.H., Paul, C., Hill, N., Hartmann, S., Hösel, C., Kube, M., Lieb, B., Meyer, A., Tiedemann, R., Purschke, G. & Bleidorn, C. (2011): Phylogenomic analyses unravel annelid evolution. Nature 471: 95–98. Surugiu, V. (2016): On the taxonomic status of the European Scolelepis (Scolelepis) squamata (Polychaeta: Spionidae), with description of a new species from southern Europe. Zootaxa 4161(2): 151–176. Syomin, V., Sikorski, A., Bastrop, R., Køhler, N., Stradomsky, B., Fomina, E. & Matishov, D. (2017): The invasion of the genus Marenzelleria (Polychaeta: Spionidae) into the Don River mouth and the Taganrog: morphological and genetic study. Journal of the Marine Biological Association of the United Kingdom 97(5): 975–984. Taghon, G.L. (1992): Effects of animal density and supply of deposited and suspended food particles on feeding, growth and small-scale distributions of two spionid polychaetes. Journal of Experimental Marine Biology and Ecology 162: 77–95. Taghon, G.L., Nowell, A.R.M. & Jumars, P.A. (1980): Induction of suspension feeding in spionid polychaetes by high particle flux. Science 210: 562–564. Tamai, K. (1981): Some morphological aspects and distribution of four types of Paraprionospio (Polychaeta: Spionidae) found from adjacent waters to western part of Japan. Bulletin of the Nansei Regulatory Fisheries Laboratory, 13: 41–53. [In Japanese, with English abstract and legends]. Tena, J., Capaccioni-Azzati, R., Torres-Gavila, F.J. & GarciaCarrascosa, A.M. (2000): Polychaetes associated with different facies of the photophilic algal community in the Chafarinas archipelago (SW Mediterranean). Bulletin of Marine Science 67: 55–72.

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Thonig, A., Knott, E.K., Kesaniemi, J.E., Hansen, B.W. & Banta, G.T. (2016): Population and reproductive dynamics of the polychaete Pygospio elegans in a boreal estuary complex. Invertebrate Biology 135(4): 370–384. Thorson, G. (1946): Reproduction and larval development of Danish marine bottom invertebrates, with special reference to the planktonic larvae in the sound (Øresund). Meddelelser fra Kommissionen for Danmarks Fiskeri- og Havunderersøgelser, Series Plankton 4: 1–523. Tzetlin, A.B. (1985): Asetocalamyzas laonicola gen. et. sp. n., a new ectoparasitic Polychaeta from the White Sea. Zoologicheskii Zhurnal 64: 296–298. [In Russian] Tzetlin, A.B. & Britayev, T.A. (1985): A new species of Spionidae (Polychaeta) with asexual reproduction associated with sponges. Zoologica Scripta 14: 177–181. Vortsepneva, E.V., Tzetlin, A.B., Purschke, G., Mugue, N., Haß-Cordes, E. & Zhadan, A. (2008): The parasitic polychaete known as Asetocalamyzas laonicola (Calamyzidae) is in fact the dwarf male of the spionid Scolelepis laonicola (comb. nov.). Invertebrate Biology 127(4): 403–416. Vortsepneva, E.V., Tzetlin, A.B. & Tsitrin, E. (2009a): Anterior muscular system of the dwarf ectoparasitic male Scolelepis laonicola (Tzetlin, 1985) (Polychaeta, Spionidae). Zoosymposia 2: 429–435. Vortsepneva, E.V., Tzetlin, A.B. & Tsitrin, E. (2009b): Nervous system of the dwarf ectoparasitic male Scolelepis laonicola (Polychaeta, Spionidae). Zoosymposia 2: 437–445. Vortsepneva, E.V., Zhadan, A.E. & Tzetlin, A.B. (2006): Spermiogenesis and sperm ultrastructure of Asetocalamyzas laonicola Tzetlin, 1985 (Polychaeta), an ectoparasite of the large spionid Scolelepis cf. matsugae Sikorski, 1994, from the White Sea. Scientia Marina 70S: 343–350. Walker, L.M. (2011): A review of the current status of the Polydora complex (Polychaeta: Spionidae) in Australia and a checklist of recorded species. Zootaxa 2751: 40–60. Ward, L.A. (1981): Spionidae (Polychaeta: Annelida) from Hawaii, with descriptions of five new species. Proceedings of the Biological Society of Washington 94: 713–730. Webster, H.E. (1879a): Annelida Chaetopoda of the Virginian coast. Transactions of the Albany Institute, New York 9: 202–269, 11 plates. Webster, H.E. (1879b): The Annelida Chaetopoda of New Jersey. New York State Museum of Natural History, Annual Report 32: 101–128. (The plates cited were not published until 1886). Weigert, A. & Bleidorn, D. (2016): Current status of annelid phylogeny. Organisms, Diversity & Evolution 6(2): 345–362. Weigert, A., Helm, C., Meyer, M. Nickel, B., Arendt, D., Hausdorf, B., Santos, S.R., Halanych, K.M., Purschke, G., Bleidorn, C. & Struck, T.H. (2014): Illuminating the base of the annelid tree using transcriptomics. Molecular Biology and Evolution 31(6): 1391–1401. Whitford, T.A. & Williams, J.D. (2016): Anterior regeneration in the polychaete Marenzelleria viridis (Annelida: Spionidae). Invertebrate Biology. 135(4): 357–369. DOI: 10.111/ivb.12148. Williams, J.D. (2001): Polydora and related genera associated with hermit crabs from the Indo-West Pacific (Polychaeta: Spionidae), with descriptions of two new species and a second polydorid egg predator of hermit crabs. Pacific Science 55(4): 429–465.

Williams, J.D. (2002): The ecology and feeding biology of two Polydora species (Polychaeta: Spionidae) found to ingest the embryos of host hermit crabs (Anomura: Decapoda) from the Philippines. Journal of the Zoological Society of London 257: 339–351. Williams, J.D. (2004): Reproduction and morphology of Polydorella (Polychaeta: Spionidae), including the description of a new species from the Philippines. Journal of Natural History 38: 1339–1358. Williams, J.D. (2007): New records and description of four new species of spionids (Annelida: Polychaeta) from the Philippines: the genera Dispio, Malacoceros, Polydora, and Scolelepis, with notes on palp ciliation patterns of the genus Scolelepis. Zootaxa 1459: 1–35. Williams, J.D. & Radashevsky, V.I. (1999): Morphology, ecology, and reproduction of a new Polydora species (Polychaeta: Spionidae) from the east coast of North America. Ophelia 51: 115–127. Wilson, D.P. (1928): The larvae of Polydora ciliata Johnston and Polydora hoplura Claparède. Journal of the Marine Biological Association of the United Kingdom 15: 567–589. Wilson, D.P. (1929): The larvae of British Sabellarians. Journal of the Marine Biological Association of the United Kingdom 16: 221–268. Wilson, W.H. (1985): Food limitation of asexual reproduction in a spionid polychaete. International Journal of Invertebrate Reproduction and Development 8: 61–65. Wilson, R.S. (1990): Prionospio and Paraprionospio (Polychaeta: Spionidae) from southern Australia. Memoirs of the Museum of Victoria 50: 243–274. Woodwick, K.H. (1960): Early larval development of Polydora nuchalis Woodwick, a spionid polychaete. Pacific Science 14: 122–128. Woodwick, K.H. (1963a): Comparison of Boccardia columbiana Berkeley and Boccardia proboscidea Hartman (Annelida, Polychaeta). Bulletin of the Southern California Academy of Sciences 62: 132–139. Woodwick, K.H. (1963b): Taxonomic revision of two polydorid species (Annelida, Polychaeta, Spionidae). Proceedings of the Biological Society of Washington 76: 209–216. Woodwick, K.H. (1964): Polydora and related genera (Annelida, Polychaeta) from Eniwetok, Majuro and Bikini Atolls, Marshall Islands. Pacific Science 18: 146–159. Woodwick, K.H. (1977): Lecithotrophic larval development in Boccardia proboscidea Hartman. In: Reish, D.J. & Fauchald, K. (Eds.). Essays on Polychaetous Annelids in Memory of Dr. Olga Hartman. Allan Hancock Foundation, University of Southern California, Los Angeles: 347–371. Worsaae, K. (2001): The systematic significance of palp morphology in the Polydora complex (Polychaeta: Spionidae). Zoologischer Anzeiger 240: 47–59. Worsaae, K. (2003): Palp morphology in two species of Prionospio (Polychaeta: Spionidae). Hydrobiologia 496: 259–267. Yokoyama, H. (1981): Larval development of a spionid polychaete Paraprionospio pinnata (Ehlers). Publications of the Seto Marine Biological Laboratory 26: 157–170. Yokoyama, H. (1996): Larvae of the spionid polychaete Paraprionospio sp. (form B) found in the plankton from Omura Bay. Bulletin of the National Research Institute of Aquaculture 25: 17–22.

7.4.2 Poecilochaetidae Hannerz, 1956 



Yokoyama, H. (2007): A revision of the genus Paraprionospio Caullery (Polychaeta: Spionidae). Zoological Journal of the Linnean Society 151: 253–284. Yokoyama, H. & Tamai, K. (1981): Four forms of the genus Paraprionospio (Polychaeta: Spionidae) from Japan. Publications of the Seto Marine Biological Laboratory 26: 303–317. Zajac, R.N. (1991): Population ecology of Polydora ligni (Polychaeta: Spionidae). I. Seasonal variation in population characteristics and reproductive activity. Marine Ecology Progress Series 77: 197–206. Zenetos, A., Gofas, S., Verlque, M., Çinar, M.E., Garcia Raso, J.E., Bianchi, C.N., Morri, C., Azzurro, E., Bilecenoglu, M., Froglia, C., et al. (2010): Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 1. Spatial Distribution. Mediterranean Marine Science 11: 381–493. Zettler, M.L. (1997): Bibliography on the genus Marenzelleria and its geographic distribution, principal topics and nomenclature. Aquatic Ecology 31: 233–258. Zottoli, R.A. & Carriker, M.R. (1974): Burrow morphology, tube formation, and microarchitecture of shell dissolution by the spionid polychaete Polydora websteri. Marine Biology 27(4): 307–316. Zrzavý, J., Říha, P., Piálek, L. & Janouškovec, J. (2009): Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evolutionary Biology 9:189: 14 pp. doi:10.1186/1471-21-48-9-189.

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serpens, then a new species found in the vicinity of Plymouth, UK. As additional species have been described, details of the external morphology, particularly of the nuchal organs, branchiae, epidermis, parapodia, and especially the chaetae, have been refined and expanded (Pilato and Cantone 1976; Read 1986; Imajima 1989; Mackie 1990; Santos and Mackie 2008). Orrhage (1964) described details of the internal morphology of P. serpens and Hannerz (1956) provided modern descriptions of larval morphology. Blake (1996) and Rouse and Pleijel (2001) provided a brief summary of poecilochaetid morphology and biology. Currently, 32 species of Poecilochaetus are recognized. As part of the present study, hundreds of specimens of the type-species, Poecilochaetus fulgoris, from deep-water in the western North Atlantic were available to us to study and illustrate a few details not heretofore available. Details of poecilochaetid morphology are presented in the following sections: a historical summary of the systematics of the family is presented in the sections on phylogeny and taxonomy. ZooBank Registration Number: urn:lsid:zoobank. org:pub:99A52A25-65C0-42ED-B49A-8F2206726199.

Morphology James A. Blake and Nancy J. Maciolek

7.4.2 Poecilochaetidae Hannerz, 1956 Introduction The Poecilochaetidae represent a small family of burrowing, bipalpate, spioniform polychaetes; there is only one genus, Poecilochaetus Claparède, recognized. The anterior end of these unusual worms is distinguished by a cephalic cage formed by the long noto- and neurochaetae arising from chaetiger 1. A ventral facial tubercle is attached to the upper lip of the mouth and usually projects forward, along with the parapodial lobes and cephalic cage. The chaetae of poecilochaetids are distinctive and diverse, including spinous, pectinate, plumose, and acicular types. The parapodia are distinctive and, together with the unusual head morphology, a peculiar trilobed nuchal organ, and elegant chaetae, provide a means of instant recognition for these polychaetes. The most important monograph on Poecilochaetus was by Allen (1904), who provided a historical review and a complete analysis of the external morphology, internal anatomy, histology, and biology of Poecilochaetus

External morphology Body shape and color. The bodies of poecilochaetids are generally elongate and thin, with up to 100 segments; they are not divided into typical thoracic and abdominal regions but distinctive changes to parapodial and chaetal morphology along the body are apparent and important (Fig. 7.4.2.1 A). There has been little study of living poecilochaetids. Allen (1904: 86) described the color of anterior segments of P. serpens as varying from “bright scarlet to deep purple-red” depending on the circulation of blood as seen through the translucent body wall; parapodia and cirri were “almost colorless.” The color of posterior segments varied from dark to white depending on pigmented cells in the intestine and genital products. Preserved specimens we have studied range from opaque white to light tan in alcohol. The body surface of most species of Poecilochaetus is relatively smooth, but may bear small epidermal papillae (Fig. 7.4.2.1 D, E), which were shown to be the external openings of what were considered to mucous-secreting glands (Allen 1904). At least four species have been reported with larger, more conspicuous papillae in anterior segments: P. fulgoris by Claparède (1875) and Hartman (1965) (Fig. 7.4.2.2 A, B), Poecilochaetus trachyderma by Read

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Fig. 7.4.2.1: Poecilochaetus serpens. A, anterior end with 21 chaetigers, dorsal view; B, posterior end, dorsal view (arrow indicates position of spines in C); C, notopodial spines from same; D, anterior end, first four chaetigers, dorsal view; E, same, ventral view. All after Allen (1904). Abbreviations: anC, anal cirrus; fT, facial tubercle; hB, heart body; neL, neuropodial lobe; noL, notopodial lobe; nuO, nuchal organ; pa, palp.

(1986), and Poecilochaetus granulatus and P. bifurcatus, both by Imajima (1989). In P. granulatus, some papillae are large and globular (Imajima 1989). Anterior segments. The prostomium and peristomium or “head” of poecilochaetids is greatly reduced and encompassed by the elongate parapodia of chaetiger 1 that bears long capillary chaetae forming a cephalic cage (Figs. 7.4.2.1 D, E; 7.4.2.2 A–C). The prostomium consists of a small spherical or elongate lobe; two pairs of eyespots are usually present or eyes may be entirely absent, when present, one pair is larger than the other one. Nuchal organs are complex and variable, consisting

of three separate structures that arise from the posterior margin of the prostomium; these may each be elongate and extend posteriorly over approximately five segments (Fig. 7.4.2.1 A, D), or there may be one long medial nuchal organ and two short lobes, or all three may be reduced to short vestigial mounds (Fig. 7.4.2.2 A, B). The peristomium is limited to the oral lips, which bear an elongate lobe that is termed a facial tubercle (Figs. 7.4.2.1 E; 2.2 C) because it is peristomial and not prostomial in origin (Mackie 1990; Blake 1996). This structure was considered a synapomorphy for Poecilochaetus by Rouse and Fauchald (1997). The ventral pharynx is short, eversible, saclike, and unarmed.



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Fig. 7.4.2.2: Poecilochaetus fulgoris, photomicrographs of specimens from US Atlantic slope, Sta. Mid-14. A, anterior end, dorsal view; B, anterior end of another specimen, dorsal view; C, anterior end, ventral view (arrow indicates neuropodial spines); D, posterior end, dorsal view. All original. Scale bars: A, C, D, 500 µm; B, 1 mm. Abbreviations: ampNo, ampullaceous notopodium; nuO, nuchal organ; fT, facial tubercle; mo, mouth; pr, prostomium.

Segmentation. All body segments are narrow and wider than long. On the majority of species, a middorsal triangular chitinous plate is present on chaetiger 9. The role of this structure is unknown. All parapodia bear elongate noto- and neuropodial postchaetal lobes (Figs. 7.4.2.3 A, B; 7.4.2.4 A–E). Generally, all postchaetal lobes are broad basally and taper apically; however, those from chaetiger 7 to 10 or 13 are long and have a distinct flask shape and are termed ampullaceous (Figs. 7.4.2.3 C; 7.4.2.4 B). The first segment with its cephalic cage of capillaries projects forward; the notopodial postchaetal lobe is typically reduced in size compared with the following notopodia. Chaetigers 2 to 6 have “normal” appearing postchaetal lobes (Figs. 7.4.2.3 A, B; 7.4.2.4 A), which are replaced by the ampullaceous lobes from chaetiger 7; after chaetigers 10 to 17, the more normal appearing lobes resume (Figs. 7.4.2.3 D, E;

7.4.2.4 C, D) and continue more or less through the middle segments. In species such as P. fulgoris, the lobes become thin and threadlike in the posterior half of the body (Fig. 7.4.2.4 E). P. bifurcatus has unique bifurcated noto-and neuropodial lobes from chaetiger 12 that follow segments with slender ampullaceous postchaetal lobes (Imajima 1989); occasional anterior notopodia with split tips have also been observed for P. fulgoris (this study). Interramal cirri have been reported for several species (Santos and Mackie 2008; Brantley 2009). These are typically elongate, slender filaments that project in a row between the noto- and neuropodial lobes. The number of interramal cirri has been reported as one in P. clavatus and four in P. tricirratus (Mackie 1990), up to 10 for P. polycirrus (Santos and Mackie 2008), and up to 22 for P. martini (Brantley 2009).

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Fig. 7.4.2.3: Poecilochaetus serpens. A, chaetiger 3, anterior view; B, chaetiger 5, anterior view; C, chaetiger 13, anterior view; D, chaetiger 18, anterior view; E, chaetiger 30, anterior view; F, featherlike chaeta; G, spinous chaeta from chaetiger 20, H, spine with feathery arista from posterior chaetiger. All after Allen (1904). Abbreviations: ampNe, ampullaceous neuropodium; ampNo, ampullaceous notopodium; br, branchiae; neL, neuropodial lobe; nePspines, neuropodial spines; noL, notopodial lobe; sO, sense organ.

Individual interramal lateral sense organs are present from chaetiger 1 and continue posteriorly (Fig. 7.4.2.3 A–C); in most species, these sense organs are absent on a few anterior segments from chaetigers 5 or 6. Allen (1904: 106) described their external appearance in anterior chaetigers (1–5 or 6) as a pear-shaped structure “protruding beyond the surface between the cirri.” In subsequent segments, they are recessed into the parapodium. The histology of these sense organs is reviewed subsequently. Branchiae. Branchiae are present on the posterior face of parapodia of some species. When present, branchiae occur from approximately chaetiger 17 and continue along most of the body. Branchiae consist of two to four fingerlike or thin

filiform lobes (Fig. 7.4.2.3 E), some of which may be branched with up to six or more filaments (Santos and Mackie 2008). Pygidium. The pygidium of Poecilochaetus species bears two, three or four anal cirri. These cirri may all be elongate or a mixture of long and short cirri (Fig. 7.4.2.1 B). Although the number and form of the anal cirri are important taxonomic characters, the nature of the anal cirri and posterior segments in general are known for fewer than half of the known species (Santos and Mackie 2008). In P. fulgoris, we have observed one long and two lateral anal cirri; however, these are often damaged and obscured by the numerous spinous chaetae arising from the crowded posterior segments (Fig. 7.4.2.2 D).

▸ Fig. 7.4.2.4: Poecilochaetus fulgoris, photomicrographs of specimens from US Atlantic slope, Sta. Mid-14. A, chaetiger 3, anterior view; B, chaetiger 11, anterior view; C, chaetiger 5, anterior view; D, chaetiger 15, anterior view; E, posterior parapodium, anterior view; F, chaetiger 3, detail of neuropodial spines; G, posterior notopodial spines (arrows denote spines where barbs are visible). All original. Scale bars: A, 100 µm; B–E, 200 µm; F, G, 50 µm. Abbreviations: ampNe, ampullaceous neuropodium; ampNo, ampullaceous notopodium; neL, neuropodial lobe; noL, notopodial lobe; sO, sense organ.



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Chaetae. The chaetae of Poecilochaetus species are complex and include (1) different kinds of capillaries with smooth, hispid, hirsute, plumose, or spinous shafts; (2) more robust chaetae that are plumose or pectinate, some with structures spiraled around along the shaft; (3) chaetae with a variety of aristae; and (4) various types of large and small spines. Mackie (1990) identified 14 distinct types of poecilochaetid chaetae. Use of the SEM by Read (1986) and Imajima (1989) has identified further complexity in these chaetae. Examples of the chaetal diversity among Poecilochaetus species are illustrated in Figs. 7.4.2.1 C, 7.4.2.3 F–H, 7.4.2.4 F, G, and 7.4.2.7 F–J. Chaetigers 2 to 3 and sometimes 4 bear a row of heavy curved neuroacicular spines (Figs. 7.4.2.3 A; 7.4.2.4 A, F). Posterior segments may also bear spines. In P. serpens, these occur in a transverse row and include heavy curved spines often with sharply curved tips (Fig. 7.4.2.1 B, C); in P. fulgoris, the spines are numerous and so thick that they conceal the parapodia and pygidium (Fig. 7.4.2.2 D); individual spines are long, narrow, and with fine tips and shafts that bear minute barbs (Fig. 7.4.2.4 G). Anatomy The primary references for internal anatomy and histology of Poecilochaetus are Allen (1904) and Orrhage (1964), both of whom studied P. serpens and used standard histological methods. To date, there have been few efforts to use the transmission electron microscope to further describe poecilochaetid anatomy. Epidermis. The cuticle of P. serpens is of variable thickness over the body and overlies a layer of cuboidal epithelial cells (Allen 1904). Gland cells lie among the epithelial cells and project above the surface as tubercles (Fig. 7.4.2.5 B–E). In some parts of the body, gland cells and tubercles are abundant. These typically are rounded cells lying among the epithelial cells and projecting through the cuticular layer (Fig. 7.4.2.5 B). Near the posterior end of the worm,

solitary gland cells open externally through a single tube (Fig. 7.4.2.5 C). The fine structure of the cuticle of poecilochaetids is generally not known due to lack of transmission electron microscope data. However, Hausen (2005) illustrated the cuticle of a larva of P. serpens; in this species, collagen fibers that are typically present in other polychaetes were entirely absent, but microvilli, presumably from gland cells, were shown to penetrate the cuticle. The nature of the adult cuticle in not known. Noto- and neuropodial lobes of P. fulgoris were observed and photographed as part of this study. All lobes exhibit glandular cells that connect basally with fibrils extending to the apex. In the ampullaceous podial lobes, the rounded base consists of thick glands that connect with a triangular-shaped group of fibrils that then narrows and continues along the lobe to a weakly expanded apex (Fig. 7.4.2.4 B). In some specimens, what seemed to be secretions were apparent on the tips of the notopodial lobes. A study of the fine structure of the parapodial lobes of species of Poecilochaetus is needed to understand the details and function of what seems to be a complex glandular morphology. Nervous system and sensory organs. The lateral sense organs lie between the noto- and neuropodia; in the anteriormost segments, they have a typical pear shape (Fig. 7.4.2.5 F) but posteriorly they are recessed and project only slightly above the body surface (Fig. 7.4.2.5 G). The histological structure of this organ was illustrated by both Allen (1904) and Orrhage (1964). Histologically, each sense organ is seen to have numerous cilia that connect internally to large sensory cells (Fig. 7.4.2.5 F, G). The nervous system of several spionids, Trochochaeta, and Poecilochaetus was well described by Orrhage (1964) and more recently reviewed by Orrhage and Müller (2005). The overall morphology of the Poecilochaetus nervous system is most similar to that of Trochochaeta and several species of Spionidae (Orrhage 1964).

▸ Fig. 7.4.2.5: Poecilochaetus serpens anatomy. A, cross-section through a midbody genital segment; B, epithelial gland cell from an anterior segment; C, gland cells and tubercle from a posterior segment; D, dorsal parapodial cirrus from a posterior segment; E, section through a parapodial cirrus, segment 20; F, lateral sense organ from an anterior segment; G, lateral sense organ from a midbody segment; H, diagram of the nervous system. A–E after Allen (1904); F–H, modified after Orrhage (1964). Abbreviations (A–G): cut, cuticle; epGlc, epidermal gland cell; latSO, lateral sense organ; lMus, longitudinal muscles; intBsin, intestinal blood sinus; neph, nephridium; noL, notopodial lobe; Sc, sensory cell; tub, tubercle; vBv, ventral blood vessel; vNc, ventral nerve cord. Abbreviations (H): Nervous system: dcvr, dorsal commissure of the ventral root ; dcdr, dorsal commissure of the dorsal root; dG, dorsal ganglia of dorsal nerves; dn, dorsal nerves; drcc, posterior (dorsal) root; LG, lateral ganglia; lnuN, left nuchal nerve; neN, neuropodial nerves; noN, notopodial nerves; nuN, nuchal nerves; Oen, esophagial nerves; Palp nerves (numbered: 1, 2, 4, 5, 6, 7); rnuN, right nuchal nerve; vcdr, ventral commissure of the dorsal root; vcvr, ventral commissure of the ventral root; vG, ventral ganglia; vnc, ventral nerve cords; vrcc, anterior (ventral) circumesophageal root.



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The example shown in Fig. 7.4.2.5 H is modified and updated from Orrhage (1964) for P. serpens. The brain consists of four transverse commissures: dorsal commissure of the ventral root (dcvr), ventral commissure of the ventral root (vcvr), dorsal commissure of the dorsal root (dcdr), and ventral commissure of the dorsal root (vcdr). Two of these (dorsal and ventral) connect with an anterior (ventral) circumesophageal root (vrcc); the other two connect to a posterior (dorsal) root (drcc). Prostomial nerves arise directly from the commissure of the ventral root (dcvr); esophageal nerves arise from the vcvr. Palp nerves (1, 2, 4, 5, 6, 7) arise from both the vrcc and drcc. Dorsal nerves (dn) arise from the dcdr whereas the nuchal nerves (nuN and InuN) arise from both the dcdr and vcdr or the posterior brain. The vrcc continues posteriorly as a pair of ventral nerve cords (vnc) that extend along the body, giving off branches to each segment with additional branches to the noto- and neuropodia (noN and neN). Digestive systems. Allen (1904) described the digestive system of P. serpens as beginning with a short, thickwalled, ventral proboscis that is nearly always retracted into the mouth on preservation. This leads to a foregut that Allen (1904) termed an esophagus followed by a gizzard, the latter being an area with heavier musculature. This section ends at chaetiger 8, in which a constriction leads to an intestine that consists of a straight tube that constricts at the junction of each segmental septum. In cross-section, Allen (1904) identified a longitudinal ciliated groove running along the midventral line of the entire intestinal tract. Allen went on to describe different types of epithelial cells and gland cells associated with the digestive tract. Coelom. The body cavity of P. serpens was described by Allen (1904) as being clearly divided by segmental septa into discrete compartments with little or no communication between them. The septa of anterior segments, however, are pushed posteriorly for several segments. Allen (1904) suggested that this flexibility of the anterior segments, septa, and coelom accommodated the protrusion and retraction of the proboscis. He also noted that the coelomic cavity extended into the nuchal organs and palps. Musculature. The musculature of P. serpens was described by Allen (1904). The body wall musculature consists of weakly developed annular rings and four well-developed longitudinal muscles. Two longitudinal muscles lie on either side of the dorsal blood vessel and the other two are on either side of the ventral nerve cord

(Fig. 7.4.2.5 A). In addition, four large bands of muscle are associated with the parapodia and chaetal sacs of each segment. One band runs down and connects to the neuropodial chaetal sac and another runs up and connects to the notopodial chaetal sac. According to Allen (1904), two other bands connect with the lateral organs (lateral sense organs) but more likely link with the parapodia because one runs downward and the other runs upward, and they are likely associated with movements of the noto- and neuropodia. Blood vascular system. The circulatory system of P. serpens was described by Allen (1904). In life, he noted that the bright red color of the blood provides rapid color changes to the worm as the filling and emptying of the larger vessels proceed. To describe the circulatory system, Allen (1904) divided the worm into three sections: (1) the anterior region of segments 1 to 11; (2) a middle region of segments 12 to 15; and (3) a posterior region continuing from segment 16. The anterior region is conspicuous with a large, thick dorsal blood vessel along which blood moves anteriorly, branching into the palps; the blood vessels of the middle region of segments 12 to 15 are further enlarged and serve as a heart body (Fig. 7.4.2.1 A), pumping the blood anteriorly; posteriorly, the intestine is surrounded by a blood sinus (Fig. 7.4.2.5 A) and with branches that connect to the branchiae and the ventral vessel. Nephridia. The nephridial morphology of P. serpens was described by Allen (1904) and summarized by Orrhage (1964) and Bartolomaeus and Quast (2005). Paired metanephridia or segmental organs occur throughout the body. The metanephridial system serves both for filtration by special cells called podocytes and in reproduction with gonoducts. In the latter instance, a nephrostome or ciliated funnel serves to collect gametes and move them to a ciliated nephridial canal for external discharge. In P. serpens, the nephridia of anterior segments (approximately 1–14) are simple nephridia that function only in filtration and are termed “head kidneys” by Bartolomaeus and Quast (2005), whereas those that follow from approximately segment 17 and posteriorly are compound organs with large genital funnels that also function in reproduction (Fig. 7.4.2.5 A).

Reproduction and development The eggs of P. serpens, and presumably all poecilochaetids, are large, yolky, discoid in shape, and have a thick membrane with distinct vesicles (Allen 1904; Hannerz 1956). Allen (1904) observed developing oocytes (Fig. 7.4.2.5 A)



7.4.2 Poecilochaetidae Hannerz, 1956 

 111

Fig. 7.4.2.6: Poecilochaetus serpens eggs and larvae. A, optical section of unfertilized egg removed from female; B, optical section of unfertilized egg after immersion in seawater; C, diagram of surface of unfertilized egg. D–F, nectochaete larva with provisional chaetae and ciliary bands: D, anterior end, ventral view; E, anterior end, dorsal view; F, posterior end, dorsal view. G, Late-stage planktic larva, dorsal view. H, I, larva ready for metamorphosis: H, anterior end, ventral view; I, anterior end, dorsal view. A–C after Allen (1904); D, E, H, I, after Hannerz (1956); G, after Thorson (1946). Abbreviations: ampNe; ampullaceous neuropodium; ampNo, ampullaceous notopodium; cilPit, ciliated pit; eyS, eyespots; gst, gastrotroch; fT, facial tubercle; neT, neurotroch; nuO; pa, palp; pr, prostomium; prT, prototroch; teT, telotroch.

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 7.4 Sedentaria: Sabellida/Spionida

and later mature eggs of P. serpens that he noted were similar to those of some spionids in having a thick membrane bearing numerous vesicles (Fig. 7.4.2.6 A), now called cortical alveoli. Upon immersion in seawater, the cytoplasm was observed to sink away from the membrane (Fig. 7.4.2.6 B) (Allen 1904). The surface of the egg was sculptured rather like a honeycomb (Fig. 7.4.2.6 C). Allen (1904) recorded the sperm as of the short-headed type. Embryology and early larval development are not known, but according to Hannerz (1956), the type of egg and sperm suggest that the entire development of P. serpens takes place in the plankton. Late stage, planktic larvae identified as P. serpens have been variously described and illustrated by Claparède (1863), Gravely (1909), Thorson (1946), Hannerz (1956), and Reddy and Mohan (1982), with Hannerz (1956) providing the most details. The larvae are distinctive, large (up to 50 segments), and longlived in the plankton (Thorson 1946; Hannerz 1956). Morphologically, the larvae of Poecilochaetus are similar to spionids in ciliation in having a prototroch, telotroch, gastrotrochs, and neurotroch with ciliated pit (Fig. 7.4.2.6 D–F), but nototrochs are absent. Provisional larval chaetae are present, but relatively short. Nuchal organs are initially patches of cilia lateral to the prostomium (Fig. 7.4.2.6 E); in late stages prior to metamorphosis, a nuchal tentacle develops with lateral cilia (Fig. 7.4.2.6 I) (Hannerz 1956). Palps also do not develop until late in development. Illustrated larvae include a nectochaete stage with all larval morphology including provisional chaetae, ciliary bands, and a well-developed ciliated vestibule (Fig. 7.4.2.6 D–F). The late-stage larva (Fig. 7.4.2.6 G) has developed palps and parapodia, but has lost the provisional chaetae and ciliary bands. The stages in Fig. 7.4.2.6 H and I are developing adult characteristics including nuchal tentacles, ampullaceous parapodia, and neuropodial spines on chaetigers 2 to 3. Metamorphosis of P. serpens larvae is induced by the presence of sand (Hannerz 1956). A living late-stage larva of Poecilochaetus anterospinus was collected from a plankton sample off Oahu, Hawaii, by Magalhães and Bailey-Brock (2015). These authors described and illustrated the larva with photomicrographs. The specimen was 7 mm long and incomplete with 29 chaetigers. In life, the body was elongate, thin, and transparent with paired green chromatophores in each segment from chaetiger 4. The prostomium was broadly rounded, with four red eyespots, one pair large and the other minute. A medial lobe of the nuchal organ was said to be as long as the palps; ampullaceous

parapodia were as described for adults. A lateral sense organ was illustrated, but no mention was made of the presence or absence of ciliary bands. Nozais et al. (1997) investigated the swimming and feeding biology of P. serpens larvae. These authors found that mucus secretion from the ciliated pit acted as a buoyancy mechanism to help suspend the larva in the water column, thus reducing energy expenditure and contributing to the long larval life characteristic of this species. They also suggested that the mucus secretion assisted in feeding of late-stage larvae before the development of adult morphology. However, no mention was made of the presence of larval cilia such as the neurotroch that lies between the ciliated pit, the source of mucus, and the mouth, and which might play an active role in feeding of late-stage larvae before settlement. Reproduction of Poecilochaetus johnsoni is dependent on temperature and takes place in spring, summer, and fall when water temperature is approximately 20°C or higher (Taylor 1966). Pelagic larvae of P. johnsoni were found in waters of Tampa Bay, FL in April, May, and August (Taylor 1966). Hannerz (1956) found the larvae abundant in waters of the Gullmar Fjord, Sweden, in July and August, and rarely as late as November.

Biology and ecology Ecology Habitat. Poecilochaetids are found in sand, mud, or mixed sediments. Taylor (1966) found P. johnsoni from coastal North Carolina and Florida in shallow silty sand sediments, sometimes in areas where marine grasses were common. At most localities, the salinities were higher than 30 practical salinity units. Taylor (1966) found juvenile commensal pinnotherid crabs in burrows of P. johnsoni in both Florida and North Carolina populations. Although the majority of species are from shallow, nearshore habitats, a few such as P. fulgoris are from deep water. As part of the U.S. Atlantic Continental Slope and Rise Program (ACSAR), P. fulgoris was identified from several stations from off New England to off the Carolinas, but was particularly abundant at two stations (Mid-3 and Mid-14) off New Jersey and Delaware in depths of 2055 and 1500 m, respectively, and one station off Massachusetts (North-5) in 2065 m (Maciolek et al. 1987a,b). All samples were collected with a 0.25 m² box core from which 0.09 m² of sediment was used for benthic analysis and sieved through a 300 µm mesh. At Sta. Mid-3, P. fulgoris ranked 7th, with 169 specimens



representing 2.2% of the entire fauna in 18 replicates collected over a 2-year period. At Sta. Mid-14, P. fulgoris ranked 10th, with 110 specimens representing 1.8% of the total fauna in 12 replicates collected over a 2-year period. At Sta. North-5, P. fulgoris ranked 14th, with 79 specimens or 1.5% of the total fauna in 18 replicates collected over a 2-year period. The sediment at each of the two mid-Atlantic stations consisted of silt and clay, but had a relatively high sand component (ca. 25%) for deep-sea muds. Station North-5 had more than 50% sand content. Details of the benthic communities and fauna at these stations and others in the program are found in Maciolek et al. (1987a,b). Behavior Burrowing and feeding. Allen (1904) described the U-shaped tubes of P. serpens. The tubes are lined with a layer of fine sediment and mucus. Allen observed how living animals burrow in the sediment by placing worms between two plates of glass. The worm burrows with its head end by using the parapodial cirri and cephalic chaetae of the first segment to excavate its way through the sediment. The burrowing activities continued until a U-shaped tube had been formed. Water moved through the tube and the worms constantly moved their bodies in an undulatory fashion and moved the parapodia and chaetae in fanlike motions. Allen observed that the numerous featherlike bristles in the posterior part of the animal played an important role in maintaining water movement in the tube. When the worms reversed their direction in the tube, the direction of the current flow immediately reversed as well. While in their tubes, poecilochaetids extend their palps into the overlying water. Allen (1904) observed that the palps of P. serpens were either extended some distance from the tubes or were drawn closer into a number of loose coils. He did not, however, actually observe any specimens feeding but did identify diatom frustules in their guts. According to Fauchald and Jumars (1979), poecilochaetids use their palps in suspension feeding on small algae and diatoms in the water or in deposit feeding from the surface of the sediment. The ability to switch feeding modes from suspension to deposit feeding is now well-known for spionids (Taghon et al. 1980; Dauer et al. 1981) and depends on currents and water-borne particle flux. High flux and flow stimulate a switch to suspension feeding, whereas quiescent conditions are conducive to deposit feeding. It is likely that poecilochaetids have the same ability (Jumars et al. 2015).

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Phylogeny and taxonomy Phylogeny Morphological studies. Rouse and Fauchald (1997) developed the first cladistic-based family-level phylogeny of polychaetes using morphological characters. They established a phylogeny in which the polychaete families were organized into six basic clades. The Poecilochaetidae were grouped with six other families into a clade termed the Spionida. Other families assigned to the Spionida were Apistobranchidae, Spionidae, Trochochaetidae, Longosomatidae (genus Heterospio), Magelonidae, and Chaetopteridae. The first phylogenetic analysis of spioniform genera using morphology was by Sigvaldadóttir et al. (1997). These authors used 25 adult morphological characteristics of the type species of 28 spionid genera as part of a parsimony analysis. P. serpens was included, but was used as an outgroup taxon rather than an ingroup taxon and as such was basal in the analysis. Blake and Arnofsky (1999), as part of a review of the reproduction and larval development of spioniform polychaetes, developed a preliminary phylogenetic analysis of 36 genera of Spionidae, Apistobranchidae, Trochochaetidae, Poecilochaetidae, Heterospionidae (= Longosomatidae), and Uncispionidae using 38 characters. Cossura and Cirrophorus were used as outgroups. Among the 38 characters, 14 were reproductive and developmental in nature. The results of this analysis clearly showed that the classification of Spionidae was paraphyletic in that there were two major clades consisting of the subfamily Spioninae and a larger clade consisting of all remaining spionid genera and the genera Heterospio, Poecilochaetus, Trochochaeta, and Uncispio. A minor third clade consisting of the enigmatic genus Pygospiopsis (including Atherospio) was distinct. Apistobranchus behaved as an outgroup in this analysis and does not belong in the order Spionida. An expanded phylogenetic analysis using additional characters and taxa including the magelonids and chaetopterids was later developed by Blake and Arnofsky (2000: Abstract). This analysis added further support to the preliminary results of Blake and Arnofsky (1999) and demonstrated that reproductive and developmental data, when used together with adult morphology, provide a robust suite of characters to better understand the interrelationships of spioniform polychaetes. However, these analyses, although demonstrating that reproductive modes and larval morphology are important in understanding spioniform phylogeny, did not include

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a sufficiently large suite of adult morphology, including chaetal and parapodial characters, to fully characterize genera such as Poecilochaetus, which, although similar to spionids in terms of egg and larval morphology, differs considerably when adult morphology is considered. Rouse and Pleijel (2001) developed a “polychaete metatree” based on a variety of sources. In that effort, Poecilochaetus was again placed into Spionida with the following taxa: Apistobranchus, Chaetopteridae, Spionidae sensu stricto, Magelona, Heterospio, Trochochaeta, and Uncispio. The Spionida was a sister group to the Terebellida, which includes the cirratuliform and terebelliform families. Eibye-Jacobsen (2006) developed the first phylogenetic analysis of Poecilochaetus using 34 morphological characters. The analysis included 26 ingroup species of Poecilochaetus and two outgroup taxa, Apistobranchus tullbergi and Trochochaeta multisetosa. The results suggested that Poecilochaetus was a well-defined monophyletic group and that Trochochaeta was a sister group. Poecilochaetus was found to be divided into two major subgroups or clades: (1) the first clade included species with the body covered by numerous papillae, lacking a notopodial postchaetal lobe on chaetiger 1, with a vestigial middorsal nuchal organ, and lacking a dorsal chitinous plate on chaetiger 9; (2) the second clade consisted of smooth-bodied species with a notopodial lobe on chaetiger 1, an elongate middorsal nuchal organ and a dorsal chitinous plate present on chaetiger 9. Molecular studies. There have been relatively few studies of Poecilochaetus among the numerous studies published on polychaete phylogeny using molecular data. When Poecilochaetus gene sequences have been used, they have always been recovered in a clade with Spionidae and Trochochaeta, thus agreeing with morphological studies. A molecular phylogeny by Rousset et al. (2007) used more than 250 sequences with two ribosomal genes (18S rDNA and 28S rDNA), histone H3, and one mitochondrial gene (16S rDNA). The 217 taxa that were included in the analysis were all required to have an 18S rDNA sequence and at least two other gene sequences. The results of this analysis did not recover any evidence of monophyly of the Spionida as defined by Rouse and Fauchald (1997). Apistobranchus, Chaetopteridae, Magelona, and Spionidae were in different parts of the tree and with different relationships. Apistobranchus was actually near the base of the tree. The genera of the Spionidae and Poecilochaetus, however, formed a sister clade to one that included genera of the Sabellidae.

Struck et al. (2008) presented an analysis of 18S rRNA and 28S rRNA sequences in two different maximum likelihood trees. In these analyses, the genera of Spionidae (Polydora, Prionospio, and Scolelepis), Poecilochaetus, and Trochochaeta occurred in a clade with Sabellaria. In both examples, Apistobranchus and Chaetopterus were unrelated to the spionids, thus not supporting a monotypic Spionida sensu Rouse and Fauchald (1999). Zrzavý et al. (2009) developed an analysis that combined morphological and molecular characters to assess annelid phylogeny. They used 93 morphological characters and six genes (18S, 28S, and 16S rRNA, EF-I α, H3, and COI). Unfortunately, the results were presented only at the family or genus level. Spionidae, Poecilochaetus, and Trochochaeta formed a clade that grouped with Sabellidae and Sabellariidae in all of the analyses. Apistobranchus, Chaetopterus, and Magelona were in different parts of the trees. Capa et al. (2012) evaluated the relationship of Sabellariidae with other polychaetes using both morphological data and DNA sequences. The molecular analyses using 18S rDNA, 28S rDNA, and EF-1 α confirmed the monophyly of Sabellariidae as well supported, together with a sister-group relationship with the order Spionida that included Polydora sp., Trochochaeta sp. and P. serpens. Taxonomic history The poecilochaetids were assigned to the Disomidae by Mesnil (1897), a small family that included only two genera: Disoma and Poecilochaetus. This arrangement was subsequently recognized and followed by most workers for more than 50 years. Hannerz (1956), as part of a study of larval development of spioniform polychaetes from Swedish waters, determined that Poecilochaetus larvae were sufficiently different from larvae of Disoma and the spionids to warrant establishment of a separate family, the Poecilochaetidae. Pettibone (1963) determined that Disoma Örsted, 1843, was preoccupied in the Protozoa and resurrected the next available name, Trochochaeta Levinsen, 1883, to replace it and renamed the family Trochochaetidae. The Spionidae, Trochochaetidae, and Poecilochaetidae have been used as distinct spioniform families by all subsequent workers except Day (1967), who included Poecilochaetus in the Trochochaetidae. The first species of Poecilochaetus to be described was P. fulgoris Claparède 1875, which was dredged from 1450 m in the Atlantic off France. This species remained poorly known until it was redescribed from collections in deep water off North and South America by Hartman (1965). The second reported species was P. serpens by Allen (1904)



from various shallow water localities around Europe. Allen (1904) also provided a detailed account of the morphology, internal anatomy, and aspects of the mode of life of this species. The third species was P. tropicus Okuda (1935) from Palau in the central Pacific (see also Okuda, 1937). P.  serpens has subsequently been reported from the Solomon Islands by Gibbs (1971, as a new subspecies: P.  serpens honiarae) and from Japan by Imajima (1989). The fourth species discovered was P. johnsoni by Hartman (1939) from Southern California. Hartman provided a key to the four species known at that time. Milligan and Gilbert (1984) have since reported P. johnsoni from North Carolina, whereas Taylor (1966) reported them from Florida and the Gulf of Mexico, although specimens from those localities exhibited variability from the original account. In the 80 years since Hartman (1939) described P. johnsoni, the number of named species of Poecilochaetus has increased from four to 32. Species have been described worldwide. Important articles include Hartman (1965) on species from deep water in the western North Atlantic; Pilato and Cantone (1976) on a review of the family and a new species from Sicily; Read (1986) on three new deep-sea species from off New Zealand; Kitamori (1965), Miura (1988), and Imajima (1989) on 11 species from Japan (10 new). An article by Miura (1989), which included descriptions of two new Japanese species, appeared in print 3 days after Imajima (1989) had already described and named the same taxa. Other species have been described by Levenstein (1962) from the Tonga Trench, Nonato (1963) from Brazil, Rullier (1965) from West Africa, Gallardo (1968) from Vietnam, Hartmann-Schröder (1980) from northwestern Australia; Mackie (1990) from the vicinity of Hong Kong, China; and de Leon-Gonzales (1992) from western Mexico. More recently, new species have been described by Santos and Mackie (2008) from Brazil; Brantley (2009) from Southern California, and Magalhães et al. (2014) from Hawaii. Laubier and Ramos (1973) described Elicodasia mirabilis, an aberrant poecilochaetid genus and species from the Mediterranean coast of Spain. Mackie (1990), however, proposed that the head of E. mirabilis was actually the posterior end of a species of Poecilochaetus, most likely P. fauchaldi Pilato and Cantone, 1976. Mackie (1990) also suggested that P. gallardoi was the posterior end of P. paratropicus. Taxonomy Poecilochaetus Claparède in Ehlers, 1875 Type species: Poecilochaetus fulgoris Claparède, 1875, by monotypy.

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Synonym: Elicodasia Laubier and Ramos, 1973: Type species: Elicodasia mirabilis Laubier and Ramos, 1973, by monotypy. Fide Mackie 1990. Diagnosis (modified after Imajima 1989 and Blake 1996): Prostomium small, rounded, two pairs of eyespots (Figs. 7.4.2.1 A; 7B); prominent facial tubercle projecting from dorsal lip of mouth (Figs. 7.4.2.1 E; 7.4.2.2 C; 7.4.2.7 A); one to three tentaculiform nuchal organs extending posteriorly (Figs. 7.4.2.1 D; 7.4.2.7 B) or nuchal organs reduced to short lobes or knobs (Fig. 7.4.2.2 A, B). Two long, grooved palps present (Fig. 7.4.2.1 A). First parapodia directed anteriorly, bearing elongated postchaetal lobes, with long chaetae forming cephalic cage (Figs. 7.4.2.1 D, E; 7.4.2.2 A–C; 7A, B). Chaetigers 2 to 3 or 4 with thick, curved spines in neuropodia (Figs. 7.4.2.1 E; 7.4.2.4 A, F; 7.4.2.7 A, C). Flasklike (ampullaceous) postchaetal lobes present on some anterior parapodia from chaetiger 7 to 10 or 17 (Figs. 7.4.2.2 A, B; 7.4.2.3 C; 7.4.2.4 E; 7.4.2.7 D). Thin, filiform, or branched branchiae on posterior sides of some middle and posterior parapodia (Fig. 7.4.2.3 E), or branchiae entirely absent. Simple chaetae of numerous types in middle and posterior parapodia: plumose, hispid, and knobbed with arista either simple or plumose. Last 20 or so parapodia modified, with notopodial spines (Figs. 7.4.2.1 B, C; 7.4.2.4 G; 7.4.2.7 I, J). Remarks. The majority of species of Poecilochaetus occur in intertidal to shallow subtidal depths 10,000 m). The majority of species have relatively limited geographic distributions. However, this might be due to lack of sampling rather than a high degree of local endemism. P. serpens is a European species but has been recorded more widely, but in this case it likely has been misidentified in some locations such as India. P. johnsoni has been recorded from all three coasts of North America (Taylor 1966; Milligan and Gilbert 1984; Blake 1996). Poecilochaetus fulgoris, the type species, was originally described from the northeastern Atlantic off France in 1190 to 1325 m by Claparède (1875) and redescribed by Hartman (1965) from off New England in slope and abyssal depths of 1000 to 5000 m. As part of the ACSAR program (1983–1987), hundreds of specimens were collected from the US Atlantic continental slope from off New England to South Carolina in depths of 1000 to 3000  m (Blake et  al. 1987; Maciolek et al. 1987a,b). As noted in the Biology section, the species was most abundant at a few stations in the 1500 and 2000 m depth

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Fig. 7.4.2.7: Poecilochaetus johnsoni. A, anterior end, ventral view; B, anterior end, dorsal view; C, chaetiger 3, anterior view; D, chaetiger 10, anterior view; E, chaetiger 15, anterior view; F, neuropodial spine from chaetiger 2; G, spinous chaeta; H, plumose chaeta; I, J, spines from posterior parapodia. After Blake (1996). Abbreviations: ampNe, ampullaceous neuropodium; ampNo, ampullaceous notopodium; fT, facial tubercle; mo, mouth; neL, neuropodial lobe; noL, notopodial lobe; nuO, nuchal organ; pr, prostomium. Arrows denote location of anterior neuropodial spines.

ranges. The morphology of the ACSAR specimens generally agrees with the redescription provided by Hartman (1965), but differences or additions to the description of the nuchal organs, the neuropodial spines on chaetigers 2 to 4, and the spines in far posterior chaetigers can be made. P. fulgoris has the surface of the body covered with numerous papillae (Fig. 7.4.2.2 A, B), some large. Hartman (1965) assumed the medial nuchal tentacle had been lost and that a base or scar was all that remained. In reality, the medial nuchal organ is a low rounded mound or vestigial structure. In addition, two lateral vestigial curved areas are believed to represent two lateral nuchal organs. Thus, all three nuchal organs are vestigial. Hartman (1965) illustrated the anterior neuropodial spines as sharply curved and tapering to a fine tip. In contrast, in our specimens, the spines, although curved, taper to a

bluntly rounded tip (Fig. 7.4.2.4 F). The posterior spines are numerous and provide the entire posterior end of the worms with a spinous appearance in which the parapodia and pygidium are obscured (Fig. 7.4.2.2 D). The individual spines are long, narrow, and terminate in a narrow, blunt tip; each spine is covered with short barbs (Fig. 7.4.2.4G). The noto- and neuropodial cirri of posterior segments are long and thin (Fig. 7.4.2.4 E) and because the posteriormost segments are narrow and crowded against the pygidial segment, the actual number of anal cirri seems to be more numerous than the three reported. However, one long ventral anal cirrus and at least two lateral cirri of variable length are present. The morphology of P. serpens as described by Allen (1904) and P. fulgoris as described by Hartman (1965) and this study represent opposite ends of the



morphological diversity observed in the genus. In P. serpens, the anterior end is dominated by the three long tentacular nuchal organs, a body that has a relatively smooth cuticle with only small tubercles visible externally, and a row of large curved notopodial spines in posterior chaetigers, in which the parapodia and anal cirri are clearly visible. In contrast, P. fulgoris has only vestigial nuchal organs, a body covered with numerous papillae, and numerous narrow, elongate posterior spines in both noto- and neuropodia that entirely cover and conceal the parapodia and anal cirri. P. johnsoni has nuchal organs that are intermediate between these two species in having one long medial and two short lateral lobes (Fig. 7.4.2.7B). Elicodasia mirabilis is believed to be described from the posterior end of a species of Poecilochaetus, most likely P. fauchaldi Pilato and Cantone, 1976 (Mackie 1990). If confirmed, then the species name of E. mirabilis is the senior synonym of Poecilochaetus fauchaldi. Mackie (1990) also suggested Poecilochaetus sp. A of Gallardo (1968) which was named P. gallardoi by Pilato and Cantone (1990) was also a posterior end, likely belonging to Gallardo’s P. paratropicus. Neither of these potential synonymies has been confirmed, but are here noted in brackets within the species in the subsequent list. At present, 31 species and one subspecies of Poecilochaetus are recognized. Of these, only four species were known prior to 1962; the remaining 28 species were described between 1962 and 2015. 1. Poecilochaetus anterospinus Magalhães, Bailey-Brock, and Santos, 2015. Off Oahu, Hawaii, 40 to 65 m. 2. Poecilochaetus australis Nonato, 1963. Brazil, intertidal. 3. Poecilochaetus bermudensis Hartman, 1965. North Atlantic, off Bermuda, 1000 m. 4. Poecilochaetus bifurcatus Imajima, 1989. Japan, Izu-Oshima, 30 to 75 m. 5. Poecilochaetus clavatus Imajima, 1989. Japan, off Honshu, 70–80 m. [Poecilochaetus branchiatus Miura, 1989]. Published 3 days after Imajima (1989). 6. Poecilochaetus elongatus Imajima, 1989. Japan, 10 to 110 m. 7. Poecilochaetus exmouthensis Hartmann-Schröder, 1980. Western Australia, intertidal. 8. Poecilochaetus fauchaldi Pilato and Cantone, 1976. Mediterranean, Sicily, 15 to 30 m. [Elicodasia mirabilis Laubier and Ramos, 1973]. Suggested posterior end. Fide Mackie 1990.

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9. Poecilochaetus fulgoris Claparède in Ehlers, 1875. North Atlantic, widespread in slope and abyssal depths, 1000 to 5000 m. 10. Poecilochaetus granulatus Imajima, 1989. Japan, 15 to 120 m. 11. Poecilochaetus hystricosus Mackie, 1990. China, Hong Kong, 13 to 21 m. 12. Poecilochaetus ishikariensis Imajima, 1989. Japan, off Hokkaido, 84 to 88 m. 13. Poecilochaetus japonicus Kitamori, 1965. Japan, 5 to 20 m. 14. Poecilochaetus johnsoni Hartman, 1939. Central and Southern California, intertidal to 90 m; North Carolina; Florida; Gulf of Mexico, to 189 m. 15. Poecilochaetus koshikiensis Miura, 1988. Japan, 200 m. 16. Poecilochaetus magnus Imajima, 1989. Japan, 10 m. [Poecilochaetus toshiomarae Miura, 1989]. Published 3 days after Imajima (1989). 17. Poecilochaetus martini Brantley, 2009. Southern California, 13 to 61 m. 18. Poecilochaetus modestus Rullier, 1965. West Africa, off Togo, 82 m. 19. Poecilochaetus multibranchiatus Leon-Gonzalez, 1992. W. Mexico, Baja California, 160 m. 20. Poecilochaetus paratropicus Gallardo, 1968. Vietnam, 9 to 43 m. [Poecilochaetus gallardoi Pilato and Cantone, 1976]. Suggested posterior end. Fide Mackie 1990. 21. Poecilochaetus perequensis Santos and Mackie, 2008. Brazil, intertidal to 15 m. 22. Poecilochaetus polycirratus Santos and Mackie, 2008. Brazil, intertidal. 23. Poecilochaetus serpens Allen, 1904. England, intertidal. 24. Poecilochaetus serpens honiarae Gibbs, 1971. Solomon Islands, intertidal. 25. Poecilochaetus spinulosus Mackie, 1990. China, Hong Kong, intertidal. 26. Poecilochaetus tokyoensis Imajima, 1989. Japan, low water. 27. Poecilochaetus trachyderma Read, 1986. New Zealand, 477 to 515 m. 28. Poecilochaetus tricirratus Mackie, 1990. China, Hong Kong, 18 to 20. 29. Poecilochaetus trilobatus Imajima, 1989. Japan, 5 to 20 m. 30. Poecilochaetus tropicus Okuda, 1937. Solomon Islands; Southern Japan; intertidal. 31. Poecilochaetus vietnamita Gallardo, 1968. Vietnam, 19 m. 32. Poecilochaetus vitjazi Levenstein, 1962. Tonga Trench, 10,415 to 10,687 m.

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 7.4 Sedentaria: Sabellida/Spionida

References Allen, E.J. (1904): The anatomy of Poecilochaetus Claparède. Quarterly Journal of Microscopical Science, new series, London 48: 79–151, pls. 7–12. Bartolomaeus, T. & Quast, B. (2005): Structure and development of nephridia in Annelida and related taxa. In: Bartolomaeus, T. & Purschke, G. (Eds.), Morphology, Molecules, Evolution, and Phylogeny in Polychaeta and Related Taxa. Hydrobiologia 535/536: 139–165. Blake, J.A. (1996): Chapter 5. Family Poecilochaetidae. In: Blake, J.A., Hilbig, B. & Scott, P.H. (Eds.). Taxonomic Atlas of the Santa Maria Basin and Western Santa Barbara Channel. Vol. 6. Annelida Part 3. Polychaeta: Orbiniidae to Cossuridae. Santa Barbara Museum of Natural History 225–232. Blake, J.A. & Arnofsky, P.L. (1999): Reproduction and larval development of the spioniform Polychaeta with application to systematics and phylogeny. In: Dorresteijn, A.W.C. & Westheide, W. (Eds.). Reproductive Strategies and Developmental Patterns in Annelids. Hydrobiologia 402: 57–106. Blake, J.A. & Arnofsky, P.L. (2000): Systematics and phylogeny of the spioniform Polychaeta. Bulletin of Marine Science 67: 657 (abstract). Blake, J.A., Hecker, B., Grassle, J.F., Brown, B., Wade, M., Boehm, P., Baptiste, E., Hilbig, B., Maciolek, N., Petrecca, R., Ruff, R.E., Starczak, V. & Watling, L.E. (1987): Study of biological processes on the U.S. South Atlantic slope and rise. Phase 2. Prepared for the U.S. Department of the Interior, Minerals Management Service, Washington, D.C., OCS Study MMS 86-0096: Volume 1. Executive Summary, ii + 58 pp.; Final Report. ii + 414 pp. and 13 Appendices. https://www.boem. gov/ESPIS/4/4698.pdf. Brantley, C.A. (2009): A new species of Poecilochaetus (Polychaeta: Poecilochaetidae) from coastal waters off Southern California. Zoosymposia 2: 81–89. Capa, M., Hutchings, P. & Peart, R. (2012): Systematic revision of the Sabellariidae (Polychaeta) and their relationships with other polychaetes using morphological and DNA sequence data. Zoological Journal of the Linnean Society 164: 245–284. Claparède, E. (1863): Beobachtungen über Anatomie und Entwicklungsgeschichte wirbelloser Thiere an der küste von Nomandie angestellt. Leipzig, vii + 120 pp., 18 plates. Claparède, E. (1875): Annelids of the Lightning and Porcupine expeditions. In: Ehlers, E. (ed.), Beiträge zur Kenntniss der Verticalverbreitung der Borstenwürmer im Meere. Zeitschrift für Wissenschaftliche Zoologie 25: 2–15. Dauer, D.M., Maybury, C.A. & Ewing, R.M. (1981): Feeding behavior and general ecology of several spionid polychaetes from the Chesapeake Bay. Journal of Experimental Marine Biology and Ecology 54: 21–38. Day, J.H. (1967): A monograph on the Polychaeta of Southern Africa. British Museum of Natural History, Publication No. 656: 1–878. de Leon-Gonzales, J.A. (1992): Soft bottom polychaetes from the western coast of Baja California Sur, Mexico. II. Poecilochaetidae. Cahiers de Biologie Marine 33: 109–114.

Ehlers, E. (1875): Beiträge zur Kenntniss der Verticalverbreitung der Borstenwürmer im Meere. Zeitschrift für wissenschaftliche Zoologie. 25: 1–102, plates I–IV. Eibye-Jacobsen, D. (2006): A preliminary phylogenetic analysis of Poecilochaetidae (Annelida: Polychaeta) at the species level. Marine Ecology 26: 171–180. Fauchald, K. & Jumars, P.A. (1979): The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology Annual Review 17: 193–284. Gallardo, V.A. (1968): Polychaeta from the Bay of Nha Trang, South Viet Nam. Naga Report 4: 35–279. Gibbs, P.E. (1971): The polychaete fauna of the Solomon Islands. Bulletin of the British Museum of Natural History (Zoology) 21: 101–211. Gravely, F.H. (1909): Polychaete larvae of Port Erin. LMBC Memoirs, No. 19, in Transactions of the Biological Society of Liverpool 23: 575–653. Hannerz, L. (1956): Larval development of the polychaete families Spionidae Sars, Disomidae Mesnil and Poecilochaetidae n. fam. in the Gullmar Fjord (Sweden). Zoologiska Bidrag från Uppsala 31: 1–204. Hausen, H. (2005): Comparative structure of the epidermis in polychaetes (Annelida). In: Bartolomaeus, T. & Purschke, G. (Eds.), Morphology, Molecules, Evolution, and Phylogeny in Polychaeta and Related Taxa. Hydrobiologia 535/536: 25–35. Hartman, O. (1939): New species of polychaetous annelids from Southern California. Allan Hancock Pacific Expeditions 7: 157–172. Hartman, O. (1965): Deep-water benthic polychaetous annelids off New England to Bermuda and other North Atlantic areas. Allan Hancock Foundation Publications, Occasional Paper 28: 1–378. Hartmann-Schröder, G. (1980): Die Polychaeten der tropischen Nordwestküste Australiens (zwischen Port Samson im Norden und Exmouth im Süden). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 77: 42–110. Imajima, M. (1989): Poecilochaetidae (Annelida, Polychaeta) from Japan. Bulletin of the National Science Museum, Series A (Zoology) 15: 61–103. Jumars, P.A., Dorgan, K.M. & Lindsey, S.M. (2015): Diet of worms emended: an update of polychaete feeding guilds. Annual Review of Marine Science 7: 497–520 + Supplemental Appendix A. Family-by-Family Updates: A1–A350 + Supplemental Table of Guild Characteristics: 1–14. Kitamori, R. (1965): Two new species of rare families, Disomidae and Paralacydonidae (Annelida: Polychaeta). Bulletin of the Tokai Regional Fisheries Laboratory 44: 41–44. Laubier, L. & Ramos, J. (1973): A new genus of Poecilochaetidae (Polychaetous annelids) in the Mediterranean: Elicodasia mirabilis. Proceedings of the Biological Society of Washington 86: 69–78. Levenstein, R.Y. (1962): The polychaetes from three abyssal trenches in the Pacific Ocean. Zoologisches Zhurnal 41: 1142–1148 [in Russian]. Mackie, A.S.Y. (1990): The Poecilochaetidae and Trochochaetidae (Annelida: Polychaeta) of Hong Kong. In: Morton, B. (Ed.), Proceedings of the Second International Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 1986. Hong Kong University Press, pp. 337–362.



Maciolek, N.J., Grassle, J.F., Hecker, B., Boehm, P.D., Brown, B., Dade, R.B., Steinhauer, W.G., Baptiste, E., Ruff, R.E. & Petrecca, R. (1987a): Study of biological processes on the US Mid-Atlantic slope and rise. Final Report prepared for US Department of the Interior, Minerals Management Service, Washington, DC, OCS Study MMS 87-0050: Volume 1. Executive Summary, iii + 44 pp.; Vol. 2. Final Report, ii + 310 pp. + Appendices A–M. https://www.boem.gov/ESPIS/4/4722.pdf. Maciolek, N.J., Grassle, J.F., Hecker, B., Brown, B., Blake, J.A., Boehm, P.D., Petrecca, R., Duffy, S., Baptiste, E. & Ruff, R.E. (1987b): Study of biological processes on the US North Atlantic slope and rise. Final Report prepared for US Department of the Interior, Minerals Management Service, Washington, DC, OCS Study MMS 87-0051: Vol. 1. Executive Summary, iii + 39 pp.; Vol. 2. Final Report, iii + 362 pp. + Appendices A–L. https:// www.boem.gov/ESPIS/4/4725.pdf. Magalhães, W.F., Bailey-Brock, J.H. & Santos, C.S.G. (2015): A new species and two new records of Poecilochaetus (Polychaeta: Poecilochaetidae) from Hawaii. Journal of the Marine Biological Association of the United Kingdom 95: 91–100. Mesnil, F. (1897): Études de morphologie externe chez les Annélides. II. Remarques complémentaires sur les Spionidiens. La famille nouvelle des Disomidiens. La place des Aonides (sensu Tauber, Levinsen). Bulletin Scientifique de la France et de la Belqique 30: 83–100, 1 pl. Milligan, M.R. & Gilbert, K.M. (1984): Family Poecilochaetidae Hannerz, 1956. In: Uebelacker, J.M. & Johnson, P.G. (eds.) Taxonomic guide to the polychaetes of the northern Gulf of Mexico. Vol. II. Final Report to the Minerals Management Service, contract No. 14-12-0001-29091. Barry A. Vittor & Associates, Inc. Mobile, AL. pp. 9–1 to 9–7. Miura, T. (1988): Poecilochaetus koshikiensis, a new polychaete species from Shimo-Koshiki Island, Japan. Proceedings of the Biological Society of Washington 101: 671–675. Miura, T. (1989): Two new species of the genus Poecilochaetus (Polychaeta, Poecilochaetidae) from Japan. Proceedings of the Japanese Society of Systematic Zoology 39: 8–19. Nonato, E. (1963): Poecilochaetus australis n. sp. (Annelida, Polychaeta). Neotropica 9: 17–26. Nozais, C., Duchêne, J.C. & Bhaud, M. (1997): Control of position in the water column by the larvae of Poecilochaetus serpens, (Polychaeta): the importance of mucus secretion. Journal of Experimental Marine Biology and Ecology 210: 91–106. Örsted, A.S. (1843): Annulatorum danicorum conspectus, Fascicle 1. Maricolae. Copenhagen, 1–52. Okuda, S. (1935): Poecilochaetus tropicus n. sp., a remarkable sedentary polychaete from the South Seas. Proceedings of the Imperial Academy of Japan 11: 289–291. Okuda, S. (1937): Polychaetous annelids from the Palau Islands and adjacent waters, the South Sea Islands. Bulletin of the Biogeographical Society of Japan 7: 257–315. Orrhage, L. (1964): Anatomische und morphologische Studien über die Polychätenfamilien Spionidae, Disomidae, und Poecilochaetidae. Zoologiska Bidrag från Uppsala 36: 335–405.

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Orrhage, L. & Müller, M.C.M. (2005): Morphology of the nervous system of Polychaeta (Annelida). In: Bartolomaeus, T. & Purschke, G. (Eds.), Morphology, Molecules, Evolution and Phylogeny in Polychaeta and Related Taxa. Hydrobiologia 535/536: 79–111. Pettibone, M.H. (1963): Marine polychaete worms of the New England Region. Bulletin of the United States National Museum 227(1): 1–356. Pilato, G. and Cantone, G. (1976): Nouve specie de Poecilochaetus e considerazione sulla famiglia dei Poecilochaetidae (Annelida, Polychaeta). Animalia, Catania 3: 29–63. Read, G.B. (1986): New deep-sea Poecilochaetidae (Polychaeta: Spionidae) from New Zealand. Journal of Natural History 20: 399–414. Reddy, V.P. & Mohan, P.C. (1982): On the occurrence of larval stages of Poecilochaetus johnsoni Hartman, 1939 (Polychaeta: Trochochaetidae) in the plankton off Waltair coast. Mahasagar Bulletin of the National Institute of Oceanography 15(4): 243–246. Rouse, G.W. & Fauchald, K. (1997): Cladistics and polychaetes. Zoologica Scripta 26: 139–204. Rouse, G.W. & Pleijel, F. (2001): Polychaetes. Oxford University Press, London, 1–354. Rousset, V., Pleijel, F., Rouse, G.W., Erséus, C. & Siddall, M. (2007): A molecular phylogeny of annelids. Cladistics 23: 41–63. Rullier, F. (1965): Contribution à la faune des Annélides Polychètes du Dahomey et du Togo. Cahiers Océanographique 3: 5–66. Santos, C.S.G. & Mackie, S.Y. (2008): New species of Poecilochaetus Claparède, 1875 (Polychaeta, Spionida, Poecilochaetidae) from Paranaguá Bay, southeastern Brazil. Zootaxa 1790: 53–68. Sigvaldadóttir, E., Mackie, A.S.Y & Pleijel, F. (1997): Generic interrelationships within the Spionidae (Annelida: Polychaeta). Zoological Journal of the Linnean Society 119: 473–500. Struck, T.H., Nesnidal, M.P., Purschke, G. & Halanych, K.M. (2008): Detecting possibly saturated positions in 18S and 28S sequences and their influence on phylogenetic reconstruction of Annelida (Lophotrochozoa). Molecular Phylogenetics and Evolution 48: 628–545. Taghon, G.L., Nowell, A.R.M. & Jumars, P.A. (1980): Induction of suspension feeding in spionid polychaetes by high particle flux. Science 210: 562–564. Taylor, J.L. (1966): A Pacific polychaete in Southeastern United States. Quarterly Journal of the Florida Academy of Sciences 29: 21–26. Thorson, G. (1946): Reproduction and larval development of Danish marine bottom invertebrates, with special reference to the planktonic larvae in the sound (Øresund). Meddelelser fra Kommissionen for Danmarks Fiskeri- og Havunderersøgelser, Series Plankton 4: 1–523. Zrzavý, J., Říha, P., Piálek, L. & Janouškovec, J. (2009): Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evolutionary Biology 9:189 doi:10.1186/1471-21-48-9-189.

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James A. Blake and Nancy J. Maciolek

7.4.3 Trochochaetidae Pettibone, 1963 Introduction The family Trochochaetidae contains a single genus, ­Trochochaeta, of burrowing spioniform polychaetes that are global in distribution. Similar to closely related species of Poecilochaetus, they possess a pair of palps and a cephalic cage on the anterior end comprised of parapodia and long chaetae that project forward. However, in Trochochaeta, the first two segments project forward (Fig.  7.4.3.1  A,  B) rather than only one segment as in Poecilochaetus. Trochochaetids have three unique kinds of chaetae: (1) large neuropodial spines on segments 2 and/or 3 (Fig. 7.4.3.2  B,  C), (2) neuropodial spines and capillaries on thoracic segments from chaetiger 4 that assist in movement (Fig. 7.4.3.1  E–G), and (3) eversible posterior notopodial spines on some species (Fig. 7.4.3.1 D). Trochochaetids have elongate, fragile bodies with up to 200 segments that fragment easily upon collection; because of this fragility and a general rarity in samples, the family is not well known. Most species are found offshore in shelf depths; Trochochaeta watsoni, found on the US Atlantic coast, is a deep-water species. At present, 12 species are known. Species of Trochochaeta were previously included in the genus Disoma Örsted, 1843. Pettibone (1963) determined that Disoma was preoccupied in the Protozoa and referred the polychaetes previously included in Disoma to Trochochaeta Levinsen, 1883 and at the same time established the family Trochochaetidae. Pettibone (1976) published a more extensive review of the family, including a review of five species and a description of one new species. Gilbert (1984), Mackie (1990), Fauchald and Rouse (1997), Rouse (2001), Alcantara and Solis-Weiss (2011), and Radashevsky et al. (2018) have subsequently published brief reviews of the family. In the present review, available information on the morphology, biology, and systematics is presented. A relatively large collection of the North Atlantic deep-water species, Trochochaeta  watsoni, is available to us together with specimens of T. multisetosa (Fig. 7.4.3.3  A–C) and T. pettiboneae (Fig. 7.4.3.4) from offshore New England and specimens of T.  franciscana from the eastern Pacific (Figs. 7.4.3.1; 7.4.3.2; 7.4.3.3  E–I). These materials provided an opportunity to compare and illustrate details of several species, some of which are poorly known. ZooBank Registration Number: urn:lsid:zoobank.org: pub:C483105E-11B7-491F-9957-92D7A99734D8.

Morphology External morphology Body shape. The body of trochochaetids is divided into a short anterior thoracic region (ca. 10–20 segments) and a long abdominal region (ca. 60–150 segments) indistinctly separated by transitional segments (Fig. 7.4.3.5  A). The prostomium is reduced and, together with the palps and mouth, is located between and somewhat compressed by the two forwardly directed anterior segments. The anterior abdominal segments entirely lack notopodia; far posterior abdominal segments, however, may have emergent clusters of notopodia that bear spines or these are absent. The pygidium bears a terminal anus surrounded by either papillae or cirri. The color of living specimens has not been recorded. In alcohol, specimens observed by various investigators are white, tan, or yellowish; sometimes with parapodia or glandular areas appearing brown against the light body (Dean 1987; this study). Anterior segments. The prostomium is elongate, oval, or fusiform, and either flattened, rounded, or weakly bilobed on the anterior margin (Figs. 7.4.3.1 A, B; 7.4.3.4 A; 7.4.3.5 B, C). A mid-dorsal crest (Fig. 7.4.3.1 A) is present or absent and may extend posteriorly as a narrow caruncle for one or more segments; ciliated nuchal organs are present alongside the caruncle or dorsal crest; two to four small eyespots are present (Fig. 7.4.3.1 A) or entirely absent; a small occipital antenna may be present (Fig. 7.4.3.5 B) or absent. The peristomium is largely limited to the pharynx and mouth (Fig. 7.4.3.1 B), but extends laterally and serves as a base for the prostomium. The pharynx is an eversible, unarmed, lobed sac. The palps arise from the dorsal part of the peristomium between the prostomium and the first segment; they are elongate, cylindrical, and have a ciliated ventral groove (Figs. 7.4.3.1 A, B; 7.4.3.3 A). Palps are easily detached during collection. Chaetae. The chaetae of Trochochaeta species include capillaries of various kinds and spines that are either smooth, aristate, or fibrillated. The different kinds of chaetae in trochochaetids are often limited to certain regions of the body and associated with certain parapodia as described in the preceding sections. The first segment has long, capillary noto- and neurochaetae that form the anteriorly directed cephalic cage (Figs. 7.4.3.1 A, B; 7.4.3.5 B, C). Chaetae of segment 2 also project anteriorly but are usually not as long and, in most cases, the notochaetae are absent. Capillaries are present in the notopodia and neuropodia of subsequent thoracic segments and abdominal neuropodia. These capillaries



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Fig. 7.4.3.1: Trochochaeta franciscana. A, anterior end, dorsal view; B, anterior end, ventral view; C, two posterior segments, ventral view; D, posterior end with pygidium, dorsal view; E–G, neuropodial acicular chaetae from chaetiger 17, E, new, unworn aciculum; F, emergent aciculum, partially worn; G, worn aciculum; H, thoracic capillary chaeta. Modified after Hartman (1947). Abbreviations: anC, anal cirrus; anPap, anal papilla; ipGP, interparapodial genital pouch; neL, neuropodial lobe; noL, notopodial lobe; pa, palp; per, peristomium; pr, prostomium; Seg, segment.

are either smooth, serrated (Fig. 7.4.3.4 E), or have lateral fringes of thin spinelets or heavier fringes. Some capillaries are thick and taper to aristate-like tips (Fig. 7.4.3.4 I). Several species of Trochochaeta have heavy spines on chaetiger 2 (Fig. 7.4.3.3 E, H), but these are not as heavy as those on chaetiger 3. All known species of Trochochaeta have heavy spines on chaetiger 3, usually accompanied with a few thin capillaries. The spines range in color from golden to dark brown or nearly black (Figs. 7.4.3.3  I; 7.4.3.4  G; 7.4.3.5  I). These spines are usually weakly curved and taper to a blunted tip. Thoracic neuropodia from chaetiger 4 include capillaries (Fig. 7.4.3.1 H) and spines that are straight or weakly curved and have a smooth shaft; others are reported with a cloak of fibrils (Fig. 7.4.3.1  E–G). These thoracic

neuropodial spines typically begin on chaetiger 4 and continue for few or many subsequent thoracic segments. T. pettiboneae was observed to have narrow curved spines, straight, blunt-tipped spines, and thick, curved capillaries in which the tip tapers abruptly, almost appearing aristate (Fig. 7.4.3.4 I). The spines of T. watsoni are curved with a fringe on the convex side and taper to an aristate tip (Fig. 7.4.3.6 K, L) (this study). Notochaetae are typically absent from abdominal segments except for those species in which sharply pointed spines are present in stellate or fan-shaped arrays (see above). Neurochaetae include capillaries and sharply pointed spines, some with thin aristate tips (Figs. 7.4.3.3 D; 7.4.3.5 M). Orrhage (1971) described the ultrastructure of the heavy spines from chaetiger 3 of T. multisetosa.

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In cross-section, the spines are composed of numerous longitudinal canals that are largest in diameter in the center, and smaller and more numerous around the periphery. Optically, this accounts for the darker border and lighter center or core of the spines. Dark walls that have several microsized canals that appear as small holes line the main canals, which in turn surround each longitudinal canal. Thorax. The thoracic region consists of 10 to 25 segments including two enlarged anterior segments with elongate noto- and neuropodial lobes and chaetae that project forward and surround the prostomium and peristomium; the following segments have well-developed noto- and neuropodia, sometimes with modified podial lobes and with chaetae of various kinds. The parapodia of segment 1 are lateral to the prostomium with the noto- and neuropodia projecting anteriorly and dorsally and bearing long capillary noto- and neurochaetae (Figs. 7.4.3.1 A, B; 7.4.3.4 A; 7.4.3.5 A–C); the postchaetal lobes are subconical (Fig. 7.4.3.2 A) and have erroneously been referred to as tentacular cirri. The second segment is close to the first, and ventrally contributes to the lower lip of the mouth (Figs.  7.4.3.1  B; 7.4.3.5  C). The biramous parapodia are shifted laterally and ventrally, partially supporting the mouth region; the postchaetal lobes are similar to those of the first segment; notochaetae are present or absent; the neuropodia have fanshaped bundles of capillary neurochaetae that are either smooth (Fig. 7.4.3.4 D) or serrated (Fig. 7.4.3.4 E); sometimes, heavy acicular spines are present (Figs. 7.4.3.2 B; 7.4.3.3 E). The third segment has short postchaetal lobes, with those of some species having multilobed or serrated borders (Fig.  7.4.3.2  C). Notochaetae are all capillaries; neurochaetae include a row of heavy acicular spines and a few capillaries (Figs. 7.4.3.2 C; 7.4.3.3 F; 7.4.3.4 F; 3.5 H). The heavy projecting acicular spines of the neuropodia of chaetiger 3 and sometimes chaetiger 2 are diagnostic (Figs. 7.4.3.3 H, I; 7.4.3.4 G; 7.4.3.5 I). The fourth segment and following thoracic segments have capillary notochaetae. The postchaetal lobes are oval or platelike, with their margins either entire (Figs. 7.4.3.4 H; 7.4.3.5 J) or multilobed (Figs. 7.4.3.2 D, E; 7.4.3.3 G). The presence or absence of multilobed parapodia is an important taxonomic character. The notopodial lobes gradually become smaller posteriorly and the notochaetae decrease in number and may be absent on a few transitional segments. The neuropodial lobes from chaetiger 4 are short, subcylindrical, and bear limbate capillary chaetae and various types of heavier spinous neurochaetae. These spines may be straight or curved and covered with fibrils

that may be worn to various degrees (Figs.  7.4.3.1  E–G; 7.4.3.4 I; 7.4.3.5 J–L). Weitbrecht (1984) found the thoracic neuropodial spines from chaetiger 4 to assist the worms in their movements within the tubes (see section on Musculature for details of this process). Distinctive raised and thickened glandular pads occur on Trochochaeta pettiboneae in defined patterns on anterior thoracic segments (Fig. 7.4.3.4 A). They are on both the dorsal (Fig.  7.4.3.4  D) and ventral surfaces, between segments, and on notopodial lamellae (Dean 1987; this study). These glandular pads are tan to brown against a lighter background body color on preserved specimens. Imajima (1989) described similar structures for T. japonica. Abdomen and pygidium. The body wall of the post-­ thoracic segments is thinner and more fragile than that of the thoracic segments. Because of this, the abdominal

Fig. 7.4.3.2: Trochochaeta franciscana, parapodia. A, chaetiger 1, anterior view; B, chaetiger 2, anterior view; C, chaetiger 3, anterior view; D, chaetiger 4, anterior view; E, chaetiger 17, anterior view; F, ventral view of two posterior neuropodia. Modified after Hartman (1947). Abbreviations: ipGP, interparapodial genital pouch; NeL, neuropodial lobe; NeP, neuropodium; NoL, notopodial lobe.



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Fig. 7.4.3.3: Trochochaeta multisetosa from Massachusetts Bay. A, anterior end, dorsal view; B, posterior end, dorsal view; C, array of five posterior notopodial spines; D, two posterior parapodia in dorsal view. T. franciscana from British Columbia: E, chaetiger 2, anterior view; F, chaetiger 3, anterior view; G, chaetiger 6, anterior view; H, spinous capillary and blunttipped acicular spine from chaetiger 2; I, acicular spine from chaetiger 3. All original. Abbreviations: anC, anal cirrus; eso, esophagus; giz, gizzard; int, intestine; neL, neuropodial lamella; neP, neuropodium; noL, notopodial lobe; pa, palp.

segments are often lost during collection and handling. Complete specimens are rarely collected. The notopodial lobes and notochaetae are usually absent in the anterior abdominal segments but are sometimes represented by small papillae. The neuropodial lobes are also reduced, but bear a few heavy acicular and capillary neurochaetae (Figs. 7.4.3.1 C; 7.4.3.3 D). The postchaetal lamellae of each abdominal segment are reduced to short fingerlike lobes (Fig. 7.4.3.3 D). Membranous interparapodial pouches similar to those of spionids such as Laonice spp. extend between the neuropodia of most abdominal segments. These were described and illustrated (e.g., Figs. 7.4.3.1 C; 7.4.3.2 F) by Hartman (1947) for Trochochaeta franciscana (as Disoma franciscanum).

We have observed these same structures on T. watsoni (Fig. 7.4.3.5 D, E). Notopodia reappear in the posterior abdominal segments in some species in the form of thick mounds bearing dark, pointed acicular spines. When withdrawn, only the tips of the spines project but they are visible through the thin body wall. When extended, the spines are arranged in a stellate or wheel-like array in T. franciscana (Fig. 7.4.3.1 D) and T. multisetosa (Fig. 7.4.3.3  C). These spines were the basis for the name Trochochaeta, which was named and illustrated by Levinsen (1883: 2: fig. 6) for a specimen, named T. sarsi, that was later identified as the posterior end of Disoma multisetosum by Michaelsen (1897: 41). In other species, such as T. pettiboneae and T. carica, the everted

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Fig. 7.4.3.4: Trochochaeta pettiboneae from Massachusetts Bay. A, anterior end, dorsal view; B, posterior end, dorsal view; C, notopodial acicular spines (arrows point to individual spines); D, chaetiger 2, anterior view; E, serrated neurochaetae from chaetiger 2; F, chaetiger 3, anterior view; G, detail of acicular spines and thin capillaries from chaetiger 3; H, chaetiger 8, anterior view; I, detail of spines and aristate chaetae from chaetiger 8. All original. Abbreviations: anC, anal cirrus; neL, neuropodial lobe; neP, neuropodium; noL, notopodial lobe; pr, prostomium.

spines are displayed in a spreading fascicle or fan shape (Fig. 7.4.3.4  C) rather than a circular array (Dean 1987; Buzhinskaja and Jørgensen 1997; this study). These spines are entirely absent in the deep-water species, T.  watsoni (this study), and perhaps other species for which the posterior ends have not been observed. The posterior end is cylindrical, with a simple pygidium that bears a variable number of papillae (Fig. 7.4.3.1 D) or anal cirri. In T. multisetosa from Massachusetts Bay, 5 to 8 thick stubby lobes are present (Fig. 7.4.3.3 B); in T. pettiboneae from New England, 4 to 10 fingerlike anal cirri have been observed (Fig. 7.4.3.4 B); in T. watsoni from off the US Atlantic coast in deep water, 6 to 8 cirriform lobes surround the anal opening (Fig. 7.4.3.5 F, G). The number of anal cirri is size related, with increasing numbers of

cirri in larger specimens. Ventrally, on the body segments, there may be a few short retractile papillae, sometimes referred to as branchiae, on either side of the median line (Figs. 7.4.3.1 C; 7.4.3.2 F). Ciliated lateral organs similar to those found in several genera of Spionidae also occur in Trochochaeta (Orrhage 1964). There are, however, no additional details available except that these are presumably spionid-like ciliated pits or papillae located between the noto- and neuropodia (Rullier 1951). Anatomy Musculature. Weitbrecht (1984) described the musculature of Trochochaeta franciscana (as T. multisetosa) in detail. Dorsal and ventral longitudinal muscles extend



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along the entire body; the dorsal longitudinal muscles are exceptionally broad and well developed in the thoracic region although the oblique muscles are poorly developed (Fig. 7.4.3.6 A). There are three pairs of longitudinal muscles in the thoracic region: one pair is dorsal; the other two pairs are ventral (Fig. 7.4.3.6 A). There are four pairs of oblique muscles in each segment, with two pairs passing from the ventral nerve cord to the body wall anterior and posterior to the notopodium (Weitbrecht 1984). Weitbrecht (1984) described in detail the musculature of the thoracic neuropodia and how these muscles control the movement of the neuropodial spines of thoracic segments. While alive, the worms were observed with the parapodia moving in waves from posterior to anterior or in a step-by-step walking gait. She observed that during the backward parapodial stroke, only the dorsal-most neuropodial spine was protruded and then retracted. Weitbrecht (1984: fig. 4) described the thoracic neurochaetae of T. franciscana as arranged in three vertical rows: rows 1 and 3 are outer rows of capillaries; row 2 is a central vertical row of heavy straight spines. As chaetae wear and are lost, they are replaced and the chaetae move or shift in the parapodium from their point of origin to the site where they are lost. The anterior capillaries originate ventrally, the posterior ones dorsally, and the chaetae shift through the parapodium in opposite directions. The central row of spines originates in the dorsal part of the ramus. The dorsal-most spine is the movable spine, which, in living animals, slides in and out relative to the other chaetae. Six muscles (Weitbrecht 1984: fig. 6) control the position of the movable spine. The type of moveable spine and associated “walking” described for T. franciscana by Weitbrecht (1984) has not been reported for other polychaetes. However, other burrowing worms such as species of the orbiniid genus Leodamas might be good candidates for having a similar function because they have large neuropodial spines that are arranged in multiple vertical rows (Blake 2017). In T. franciscana, the abdominal muscles following the thoracic segments become smaller and simpler; in addition, notopodia are lost and the neurochaetae are reduced to a few capillaries and a few spines (Weitbrecht

1984). In the posterior-most segments, the notopodia reappear bearing clusters of spines. Posterior abdominal notopodia contain four to seven flattened spines and are surrounded by two concentric sheaths of muscle tissue (Weitbrecht 1984: fig. 10A). The spine clusters are everted by the contraction of the muscle sheaths, which causes the spines to twist as they emerge from the parapodium; they are then locked rigidly into position by their wedgelike cross-sections (Weitbrecht 1984: fig. 10B). The entire notopodium is elevated with the spines arranged in a stellate wheel (Figs. 7.4.3.1 C; 7.4.3.3 C). Weitbrecht (1984) believed that the spines were everted only once because they were always unworn, all of the same size, and there were no retractor muscles to return the spines to the inverted state. She speculated that the everted spines might serve as a protective anchoring device or possibly to support reproduction because gametes are found only in the posterior segments. Digestive system. There is little published information on the digestive system of trochochaetids. There is a proboscis interpreted by Orrhage (1964) as a simple axial proboscis and verified by Purschke and Tzetlin (1996). Examination of several juveniles and other specimens of Trochochaeta watsoni from off the US Atlantic coast revealed that this species has a simple narrow esophagus that extends from the pharynx through the thoracic segments. Upon entering the anterior abdominal segments, it changes to an enlarged hindgut filled with fine sediment particles (Fig. 7.4.3.5 A); this intestine extends to the anal opening. Specimens of T. franciscana from British Columbia and T. multisetosa from Massachusetts Bay have a muscular gizzardlike structure between the esophagus and intestine in the anterior abdominal segments (Fig.  7.4.3.3  A). This structure is barrel-shaped in T.  franciscana and bulbous in T. multisetosa; muscles encircle each. Several spionid genera have a similar gizzardlike structure in the digestive tract (Blake et al. 2019). Excretory system and nephridia. Information on the segmental organs or nephridia of Trochochaeta is limited but available to some extent from Orrhage (1964) and

◂ Fig. 7.4.3.5: Trochochaeta watsoni from US Atlantic continental slope off Delaware, 2050 m. A, anterior end, dorsal view; B, anterior

end of another specimen, dorsal view; C, same, ventral view; D, posterior segments, ventrolateral view; E, posterior segments, ventral view; F, posterior end, dorsal view (arrow points to neuropodial lobe and acicular spines; G, posterior end, ventral view (arrow indicates neuropodial lobe); H, chaetiger 3, anterior view; I, neuropodial acicular spines and capillaries from chaetiger 3; J, neuropodium from chaetiger 6, anterior view; K, aristate spines from J, dorsal view; L, same lateral view; M, acicular spines and serrated capillaries from posterior neuropodia (arrows point to spines). All original. Abbreviations: anC, anal cirrus; eso, esophagus; int, intestine; ipGP, interparapodial genital pouch; pr, prostomium; neL, neuropodial lobe; noL, notopodial lobe; Seg, segment.



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Weitbrecht (1984). Metanephridia in Trochochaeta have been observed only in abdominal segments (Orrhage 1964; Bartolomaeus and Quast 2005). Nephridia of anterior segments, if present, may be limited to an excretory function because gametes have been observed only in posterior abdominal segments. Weitbrecht (1984) noted that segmental organs were greatly enlarged in posterior abdominal segments. The lateral parts of the far abdominal segments were filled with enlarged genital ducts and the median parts by the gut. Blood vascular system. The only comments regarding the circulatory system of trochochaetids are by Weitbrecht (1984), who, as part of her study of the musculature of T. franciscana, noted that dorsal and ventral blood vessels were prominent in the thoracic segments (Fig. 7.4.3.6  A). The overall circulatory system is probably similar to that of spionids. Nervous system. The nervous system of Trochochaeta multisetosa and several spionids was well described by Orrhage (1964) and more recently reviewed by Orrhage and Müller (2005). The example shown in Fig. 7.4.3.6  B for T. multisetosa (as Disoma multisetosa) is modified and updated from Orrhage (1964). The following account is nearly identical to that presented for Spionidae and Poecilochaetidae (Orrhage 1964; Blake and Maciolek 2019; Blake et al. 2019). The brain of Trochochaeta, similar to that of spionids and Poecilochaetus, consists of four transverse commissures: dorsal commissure of the ventral root (dcvr); ventral commissure of the ventral root (vcvr); dorsal commissure of the dorsal root (dcdr); and ventral commissure of the dorsal root (vcdr). Two of these (dorsal and ventral) connect with an anterior (ventral) circumesophageal root (vrcc); the other two connect to a posterior (dorsal) root (drcc). Prostomial nerves arise directly from the dcvr; esophageal nerves arise from vcvr. Palp nerves (1, 2, 5, 6, 7) arise from both the vrcc and drcc. Dorsal nerves arise from the dcdr whereas the nuchal nerves arise from both the dcdr and vcdr or the posterior brain. The vrcc continues posteriorly as a pair of ventral nerve cords that extend along the body, giving off branches to

each segment with additional branches to the noto- and neuropodia. Gametes. The reproductive biology of Trochochaeta is poorly known. Buzhinskaja and Jørgensen (1997) obtained sexually mature males and females of T. carica from Arctic locations in the Kara and East Siberian Sea. All sexual products were in abdominal segments 20 to 21: females had eggs in 20 to 30 anterior abdominal segments with 8 to 10 eggs per segment; males had sperm in most of the abdominal segments. Weitbrecht (1984) also found gametes of T. franciscana (as T. multisetosa) limited to abdominal segments. Hannerz (1956) and Hartman (1947) described the eggs of T. multisetosa from Sweden and T. franciscana from California, respectively, as discoid with a thick membrane and membrane vesicles (= cortical alveoli) (Fig. 7.4.3.7 A). Hannerz (1956) reported the eggs of T. multisetosa to be 200 to 250 µm in diameter. Sperm were reported with a short head and triserrated acrosome together with a length of 5.5 to 5.7 µm. Buzhinskaja and Jørgensen (1997) described T. carica as having large yolky eggs without membrane vesicles and diameters of 447 to 650 µm (Fig.  7.4.3.7  I); sperm with large heads measured 3.3 µm in diameter. Blake (2006) reported coelomic oocytes of T. franciscana as 80 to 100 µm in diameter. Reproduction and development Planktotrophic larval development. Both Trochochaeta multisetosa and T. franciscana are reported to have planktotrophic larvae (Hannerz 1956; Blake and Arnofsky 1999; Blake 2006). The most complete sequence of developments is for T. franciscana by Blake and Arnofsky (1999) and Blake (2006). The planktic larvae of Trochochaeta species are distinctive among spioniform larvae in having unusually long provisional chaetae on chaetiger 1 (Hannerz 1956; Blake and Arnofsky 1999; Blake 2006). In T. franciscana, they extend up to three to four times the body length in the early three- to four-chaetiger larvae (Fig. 7.4.3.7  B). With continued growth, body length catches up with

◂ Fig. 7.4.3.6: Coelom and nervous system of Trochochaeta species. A, T. franciscana cross-section through anterior thoracic segment

showing septa, reduced coelom, muscles, esophagus, and blood vessels. B, T. multisetosa, diagram of the nervous system. A, modified after Weitbrecht (1984); B, modified after Orrhage (1964). Abbreviations A: circM, circular muscle; dbv, dorsal blood vessel; dLm, dorsolateral muscles; eso, esophagus; latVLm, lateral ventrolateral muscle; midVLm, middle ventrolateral muscles; obliqueM, oblique muscle; transMbands, transverse muscle bands; vbv, ventral blood vessel. Abbreviations, B: Nervous system: dcvr, dorsal commissure of the ventral root; dcdr, dorsal commissure of the dorsal root; dG, dorsal ganglia of dorsal nerves; dn, dorsal nerves; drcc, posterior (dorsal) root; lG, lateral ganglia; neN, neuropodial nerves; noN, notopodial nerves; nuN, nuchal nerves; Oen, esophageal nerves; Palp nerves (numbered: 1, 2, 5, 6, 7); vcdr, ventral commissure of the dorsal root; vcvr, ventral commissure of the ventral root; vG, ventral ganglia; vnc, ventral nerve cords; vrcc, anterior (ventral) circumesophageal root.



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the long chaetae (Fig. 7.4.3.7 D). Both T. franciscana and T. multisetosa larvae have a large peristomial umbrella, similar to that of some spionids (Hannerz 1956; Blake 2006). The peristomial umbrella bears the prototroch and more or less surrounds the anterior end of the larva (Fig. 7.4.3.7 B, C). The prototroch is composed of powerful long cilia on the anterior side of the umbrella and shorter, posteriorly directed cilia on the posterior side (Hannerz 1956; Blake and Arnofsky 1999; Blake 2006). The pattern of cilia of T. franciscana larvae is similar to those of spionid larvae (Blake 2006). A neurotroch extends posteriorly from the mouth and ends in a ciliated pit on chaetiger 2. Both of these structures develop early and persist throughout development (Fig. 7.4.3.7  C, D). Gastrotrochs begin to develop by the four- to six-segment stage. Initially, there are two widely separated cells of cilia on chaetiger 2 lateral to the ciliated pit. From chaetiger 3, the gastrotrochs eventually include four patches or cells of cilia across the venter of each segment at least through chaetiger 11; chaetigers 12 to 17 have only a single pair of ciliated cells (Fig. 7.4.3.7 D). Larvae of T. multisetosa apparently have gastrotrochs limited to a single pair along the body (Hannerz 1956: fig. 51D). Nototrochs are entirely absent in both species. The telotroch consists of several groups of cilia that entirely surround the pygidial segment. The palps first appear at the 10- to 12-chaetiger stage. The right palp develops ahead of the left palp. This situation persists through metamorphosis (Fig. 7.4.3.7  D, E). The reason for such an unequal rate of palp development is unknown but occurs in both T. franciscana and T. multisetosa (Hannerz 1956; Blake 2006). The larval development of T. franciscana proceeds from a small three-chaetiger larva (Fig. 7.4.3.7 B, C: 210 μm long), to the eight-segment or four-chaetiger stage (440 μm long), the 11- to 12-chaetiger (780 μm long), and the fully developed 17-chaetiger larva (Fig. 7.4.3.7 D: 1.02 mm long). In the transition to the adult, modified notochaetae of chaetiger 3 and brush-tipped chaetae on chaetigers four to seven are similar to those of the adults and are present in the largest planktic larvae (Fig. 7.4.3.7 D). Details of the development of these larvae were described and illustrated by Blake and Arnofsky (1999) and Blake (2006).

A juvenile of T. franciscana that metamorphosed in culture had 16 chaetigers (Fig. 7.4.3.7  E). This specimen was characterized by having a contracted body shape; most of the prototroch was lost with only a few short cilia remaining. The palps were elongated, but still unequal in length. All of the body ciliation had been lost. The mouth, with a reduction of the peristomial umbrella, appeared as an opening between two lateral lips. The pygidium was a simple expanded lobe. Careful inspection showed that chaetiger 2 bore modified spines (Fig. 7.4.3.7 G). Chaetiger 3 was evident, with its large modified spines (Fig. 7.4.3.7 H). Notochaetae of the thoracic segments were simple capillaries at this stage; neurochaetae were the characteristic brush-tipped spines and fringed capillaries characteristic of the adult (Fig. 7.4.3.7 F). Lecithotrophic larval development. Buzhinskaja and Jørgensen (1997) collected 21-setiger larvae from the adult tubes of Trochochaeta carica and concluded that the development was entirely lecithotrophic. The larvae were large, measuring 1.7 to 1.8 mm long (Fig. 7.4.3.7  J), and had long provisional chaetae on several segments, a large peristomial umbrella, and a single palp present, on the right side as in T. franciscana. The pygidial segment was enlarged and divided into four lobes (Fig. 7.4.3.7  J). Cilia were not observed. Spines of chaetigers 2 and 3 were similar to those of adults (Fig. 7.4.3.7 K–M). Direct larval development. Collections of Trochochaeta watsoni from continental slope sediments off the US Atlantic coast include several larval and postlarval forms that suggest the development is either lecithotrophic or nonpelagic. A postlarval form collected in November 1985 from Sta. 6 off Delaware in 2050 m is short, thick, and fusiform in shape (Fig. 7.4.3.8 A, B). The specimen has 12 chaetigers, measures 643 μm long and 310 μm wide across the middle. There are no ciliary bands. The prostomium is truncate on the anterior margin; the peristomium extends ventrally and encompasses the mouth. There is no evidence of a medial antenna or nuchal organ at this stage. Palps are present with the right one longer and better developed

◂ Fig. 7.4.3.7: Reproductive biology of Trochochaeta. A–H, T. franciscana eggs and larvae: A, unfertilized egg with cortical alveoli;

B, 3-chaetiger larva, dorsal view; C, same ventral view; D, 17-chaetiger larva, ventral view; E, 16-chaetiger newly metamorphosed juvenile postlarva, dorsal view; F, brush-tipped spines and fringed capillaries from thoracic neuropodia; G, neuropodial spines from chaetiger 2; H, neuropodial spines from chaetiger 3. I–K, T. carica eggs and larvae I, unfertilized egg; J, 21-segment larva, ventral view; K, acicular spine from chaetiger 2; L, acicular spine from chaetiger 3; M, detail of provisional chaeta from larva. A, after Hartman (1947); B–H, after Blake (2006); I–M, after Buzhinskaja and Jørgensen (1997). Abbreviations: cilP, ciliated pit; eyS, eyespot; gsT, gastrotroch; neT, neurotroch; nuO, nuchal organ; pa, palp; per, peristomium; pr, prostomium; prT, prototroch; pyg, pygidium.



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Fig. 7.4.3.8: Trochochaeta watsoni postlarva from US Atlantic continental slope off Delaware, 2050 m. A, entire worm, dorsal view; B, same, ventral view (arrow indicates neuropodial acicular spine of chaetiger 3); C, pygidium, dorsal view; D, same, ventral view; E, detail of neuropodial acicular spine of chaetiger 3 (arrow). All original. Abbreviations: pa, palp; pyg, pygidium.

than the left one as observed for other Trochochaeta larvae (see above). The first parapodium bears fingerlike notoand neuropodial lobes and long curved capillary chaetae, all of which are directed anteriorly. Notopodia of chaetigers 2 to 12 bear short fingerlike lobes. Notochaetae are all capillaries; capillaries are also present in all neuropodia but with heavy neuropodial spines present in chaetiger 3 (Fig.  7.4.3.8  E) and curved geniculate spines present in the neuropodia of chaetigers 4 to 6. The pygidium is large and bulbous in shape (Fig. 7.4.3.8 A–D) with a prominent anal vestibule; numerous small papillae that appear to be the external tips of bacillary glands are present around the anal opening; two short fingerlike dorsal cirri are also present. The digestive track includes a lobed intestine extending from the pharynx to the posterior end (Fig. 7.4.3.8 A, B). The gut is complete, but there is no evidence of sediment or other particles along its length. Other larvae in the same collections along the US Atlantic slope are similar in appearance and size. Smaller stages of development compared with the 12-setiger stage

were not observed, but not all samples have been examined. The lack of provisional chaetae and any residual ciliary bands typical of trochochaetid and other spioniform larvae suggest that the development is direct and likely takes place in the tubes of adults. Later stages of postmetamorphic juveniles suggest that the entire thoracic region including the prostomium, nuchal organs, and occipital antenna differentiate initially followed by a narrow, and undifferentiated abdominal region. Further study of these larvae and juveniles will be published later (Blake unpublished).

Biology and ecology Trochochaetids inhabit soft sediments ranging from nearshore to continental slope depths. They seem to be tube builders; Thulin (1921) described the tubes of Trochochaeta multisetosa as being complex, both U-shaped and branched.

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We have no examples of trochochaetids being dominant or indicator species in any benthic infauna program we have managed. In surveys conducted along the US Atlantic coast in slope depths, T. watsoni was present at most stations in depths from 1500 to 3000 m, but was not among the dominants in any samples. Gilbert (1984: 8-2) also noted that “The trochochaetids are not known to be dominant anywhere.” Feeding has not been observed. Jumars et al. (2015) hypothesized that trochochaetids, similar to spionids, use their palps for both surface deposit feeding and suspension feeding.

Phylogeny and taxonomy Taxonomic history Mesnil (1897) established the family Disomidae to include Disoma multisetosum (Örsted 1843) and Poecilochaetus ­fulgoris Claparède, 1875. He considered that the family was intermediate between the Spionidae and Chaetopteridae. Allen (1904), as part of his monograph on Poecilochaetus serpens, supported Mesnil’s concept of the family Disomidae but considered it to be closer to the Spionidae because of the similar egg types found in some spionid genera and the nature of the palps. Hannerz (1956) noted similarities between the larvae of Spionidae and Disomidae but, based on differences in larval and adult morphology, removed Poecilochaetus from Disomidae and established a separate family Poecilochaetidae, leaving Disomidae with a single genus, Disoma. Subsequent workers have supported this arrangement. However, Pettibone (1963) determined that Disoma was preoccupied in the Protozoa and referred the polychaetes previously included in Disoma to Trochochaeta Levinsen, 1883 and at the same time established the family Trochochaetidae. Pettibone (1976) published a more extensive review of the family including a description of five species, one of which was new. At the species level, new species of Trochochaeta have been described by Birula (1897), Fauvel (1916, 1932), Hartman (1947, 1974), Pettibone (1976), Dean (1987), Imajima (1989), Hernández-Alcántara and Solís-Weiss (2011), and Bochert and Zettler (2013). Phylogeny Molecular studies. There have been few studies of Trochochaeta among the numerous publications on polychaete phylogeny using molecular data. When Trochochaeta gene sequences are used, they always resolve into a clade

with Spionidae and Poecilochaetus, thus agreeing with morphological studies. Struck et al. (2008) presented an analysis of 18S rRNA and 28S rRNA sequences in two different maximum likelihood trees. In these analyses, the genera of Spionidae (Polydora, Prionospio, and Scolelepis), Poecilochaetus, and Trochochaeta occurred in a clade with Sabellaria. Zrzavý et al. (2009) developed an analysis that combined morphological and molecular characters to assess annelid phylogeny. They used 93 morphological characters and six genes (18S, 28S, and 16S rRNA, EFIα, H3, and COI). The results were presented at the family or genus level and Trochochaeta together with Spionidae and Poecilochaetus formed a clade that could be grouped with Sabellidae and Sabellariidae. Capa et al. (2012) evaluated the relationship of Sabellariidae with other polychaetes using both morphological data and DNA sequences. The molecular analyses using 18S rDNA, 28S rDNA, and EF-1α confirmed the monophyly of Sabellariidae as well supported, as well as a sister-group relationship with the order Spionida, including Polydora sp., Trochochaeta sp., and P. serpens. Morphological studies. Rouse and Fauchald (1997) developed the first cladistic-based family-level phylogeny of polychaetes using morphological characters. The Trochochaetidae were grouped with six other families into a clade termed the Spionida. Other families assigned to the Spionida were Apistobranchidae, Spionidae, Poecilochaetidae, Longosomatidae (genus Heterospio), Magelonidae, and Chaetopteridae. Blake and Arnofsky (1999) developed a preliminary phylogenetic analysis of 36 genera of Spionidae, Apistobranchidae, Trochochaetidae, Poecilochaetidae, ­Heterospionidae (=Longosomatidae), and Uncispionidae using 38 characters. Cossura and Cirrophorus were used as outgroups. Among the 38 characters, 14 were reproductive and developmental in nature. The results of this analysis clearly showed that the classification of Spionidae was paraphyletic in that there were two major clades consisting of the subfamily Spioninae and a larger clade consisting of all remaining spionid genera and the genera Heterospio, Poecilochaetus, Trochochaeta, and Uncispio. A minor third clade consisting of the enigmatic genus Pygospiopsis (including Atherospio) was distinct. Apistobranchus behaved as an outgroup in this analysis and does not belong in an order Spionida. Rouse and Pleijel (2001) developed a “polychaete metatree” based on a variety of sources. In that effort, ­Trochochaeta was again placed into Spionida with the



­following taxa: Apistobranchus, Chaetopteridae, Spionidae sensu stricto, Magelona, Heterospio, Poecilchaetus, and ­Uncispio. Taxonomy Family Trochochaetidae Pettibone, 1963 Disomidae Mesnil, 1897 (in part). Disomididae. Chamberlin, 1919 (in part). Diagnosis: Same as genus (see below). Remarks: The family Trochochaetidae (then Disomidae) of Mesnil (1897) and Chamberlin (1919), included Disoma Örsted (or Disomides Chamberlin) and Poecilochaetus Claparède. Hannerz (1956) referred the latter genus to a separate family, Poecilochaetidae. Both families show relationships to the Spionidae, in which some of the species were grouped earlier. Following Pettibone (1963), the family Trochochaetidae includes the single genus, Trochochaeta. Trochochaeta Levinsen, 1883 Type species: Trochochaeta sarsi Levinsen, 1883 = Trochochaeta multisetosa (Örsted 1844) (type by monotypy) Synonyms: Disoma Örsted, 1843. Type species: Disoma multisetosum Örsted, 1843, by monotypy; preoccupied by Ehrenberg, 1831, in Protozoa (see Neave 1939) = Trochochaeta multisetosa (Örsted 1843). Thaumastoma Webster and Benedict, 1884. Type species: Thaumastoma singulare Webster and Benedict, 1884, by monotypy, =Trochochaeta multisetosa (Örsted 1843). Nevaya McIntosh, 1911. Type species: Nevaya whiteavesi McIntosh, 1911, by monotypy = Trochochaeta multisetosa (Örsted 1843). Disomides Chamberlin, 1919. New name for Disoma Örsted, preoccupied. Diagnosis (modified from Pettibone 1976): Body long, slender, subcylindrical, with numerous segments, divided into two more-or less-distinct regions: short thoracic and long abdominal, changing gradually with some transitional segments. Prostomium small, fusiform, with median crest and caruncle extending posteriorly on the first segment or beyond, with or without small occipital antenna, with or without two to four small eyes. Pair of long spioniform palps (readily deciduous) with longitudinal groove, lateral to the prostomium. Parapodia of anterior two segments closely apposed, directed anteriorly and somewhat enclosing prostomium, tentacular palps and ventral mouth; with or without notochaetae on segment 2. Proboscis eversible as thin-walled lobulated sac. Parapodia of thoracic region biramous, with simple capillary notochaetae and neurochaetae; with well-developed subtriangular to lamelliform

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postchaetal lobes, with margins entire or serrated; fanshaped group of heavy acicular neurochaetae on segment 3 and sometimes also on segment 2. Beginning on segment 5, some neurochaetae stouter, of various types: straight, lanceolate, acicular, smooth, spiny or hairy, curved subdistally with hairy limbate borders and fine tips. Abdominal region more slender, thin-walled, with notopodia lacking anteriorly; neuropodia with few capillary and acicular neurochaetae and subconical to digitiform postchaetal lobes, extending posteriorly as thin flanges. Posterior abdominal region with notopodia in the form of low mounds and a few dark acicular spines, sometimes forming stellate structures; or notochaetae entirely absent. Pygidium thick, collarlike, slightly lobulate or with circle of anal cirri, and with terminal anus. Tube long, cylindrical, formed of fine mud particles cemented together by secreted fibers. Remarks: As part of our study of specimens from offshore New England for this review we were able to confirm the suggestion by Buzhinskaja and Jørgensen (1997) that Trochochaeta carica was limited to Arctic seas and that specimens identified as T. carica by Pettibone (1976) from the western North ­Atlantic are in fact the same as T. pettiboneae described by Dean (1987). The posterior ends and pygidial cirri are illustrated for the first time for T. watsoni, based on specimens from the US Atlantic slope; there are no posterior notopodial spines in the specimens examined. We have also found minute specimens that suggest they are postlarval forms that likely developed directly in the tubes of adults. The discovery that some species of Trochochaeta have an enlarged gizzardlike structure between the esophagus and intestine similar to those of certain spionid genera is an additional morphological character that can be used in a phylogenetic assessment of trochochaetids and spionids. Another spionid-like structure we have observed in Trochochaeta species is a neuropodial membranous pouch or flange that is similar to the interparapodial genital pouches described for certain spionid genera such as Laonice, Prionospio, and Spiophanes (see Blake et al. 2019). Hartman (1947) described the same structure in her description of T. franciscana (as D. franciscanum). In the following species list, 6 of the 12 known species of Trochochaeta were described prior to 1950. Of the more recently named species, two were described in the 1970s, two in the 1980s, and two more in 2011 and 2013. The rate of new species discoveries is thus relatively low and the genus is relatively small. However, we are aware of at least three undescribed species: one in the Gulf of Mexico

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and another in Southeast Asia, both from deep water; Trochochaeta sp. A of Gilbert (1984) is another undescribed species from the Gulf of Mexico in shelf depths. 1. Trochochaeta ankeae Bochert and Zettler, 2013. Southwest Atlantic, off Angola, 84 m. 2. Trochochaeta carica (Birula, 1897). Arctic waters, eastern Siberia, Kara Sea, Bering Sea. Buzhinskaja and Jørgensen (1997) referred records from eastern Canada to New England by Pettibone (1976) to T. pettiboneae. 3. Trochochaeta cirrifera (Hartman, 1974). Arabian Sea, 36 m. 4. Trochochaeta diverapoda (Hoagland, 1920). Philippines, 37 m; China, Hong Kong, low water. 5. Trochochaeta franciscana (Hartman, 1947). Eastern Pacific, Washington to California, low water. 6. Trochochaeta japonica Imajima, 1989. Japan, 30 to 91 m; recently reported from Brazil, and believed to be introduced (Radashevsky et al. 2018). 7. Trochochaeta kirkegaardi Pettibone, 1976. Off west Africa, 44 to 175 m. 8. Trochochaeta mexicana Hernández-Alcántara and Solis-Weiss, 2011. Western Mexico, 40 m. 9. Trochochaeta multisetosa (Örsted, 1844). Widespread in the eastern North Atlantic, European waters, intertidal to 700 m; New England, 25 to 200 m. 10. Trochochaeta orissae (Fauvel, 1932). Off east and southwest coasts of India, 4 to 55 m. 11. Trochochaeta pettiboneae Dean, 1987. US Atlantic coast, Eastern Canada to New England; Gulf of Maine, 116 to 138 m. 12. Trochochaeta watsoni (Fauvel, 1916). Western North Atlantic in slope depths, 530 to 3753 m. References Allen, E.J. (1904): The anatomy of Poecilochaetus Claparède. Quarterly Journal of Microscopical Science, new series, London 48: 79–151, 7–12. Bartolomaeus, T. & Quast, B. (2005): Structure and development of nephridia in Annelida and related taxa. In: Bartolomaeus, T. & Purschke, G. (Eds.), Morphology, Molecules, Evolution, and Phylogeny in Polychaeta and Related Taxa. Hydrobiologia 535/536: 139–165. Blake, J.A. (2006): Spionida. pp. 566–638, In: Rouse, G. and F. Pleijel, Editors, Reproductive Biology and Phylogeny of Annelida. Volume 4 of Series: Reproductive Biology and Phylogeny, Ed. B.G.M. Jamieson. Science Publishers, Enfield, New Hampshire. Blake, J.A. (2017): Polychaeta Orbiniidae from Antarctica, the Southern Ocean, the abyssal Pacific Ocean, and off South America. Zootaxa, 4218: 1–145.

Blake, J.A. & Arnofsky, P.L. (1999): Reproduction and larval development of the spioniform Polychaeta with application to systematics and phylogeny. In: Dorresteijn, A.W.C. & Westheide, W. (Eds.). Reproductive Strategies and Developmental Patterns in Annelids. Hydrobiologia 402: 57–106. Blake, James A. & Maciolek, N.J. (2019): 7.4.2. Poecilochaetidae Hannerz, 1956. pp. 103–119, In: Purschke, G., Böggemann, M. & Westheide, W. (Eds.), Handbook of Zoology. Annelida. Volume 2: Annelida Basal groups and Pleistoannelida, Sedentaria II. i–x, 1–460. De Gruyter, Berlin. Published on line 2018. Blake, James A., Maciolek, N.J. & Meißner, K. (2019): 7.4.1. Spionidae Grube, 1850. pp. 1–103, In: Purschke, G., Böggemann, M. & Westheide, W. (Eds.), Handbook of Zoology. Annelida. Volume 2: Annelida Basal groups and Pleistoannelida, Sedentaria II. i–x, 1–460. De Gruyter, Berlin. Published on line 2017. Birula, A. (1897): Researches on biology and zoogeography, chiefly in Russian Seas, collected by Dr. A.C. Botkin in 1895 in the Gulfs of Yenisey and Ob. Annuaire du Musée Zoologique de L’Académie Impériale des Sciences de St. Pétersburg 2: 78–116 [In Russian]. Bochert, R. & Zettler, M.L. (2013): A record of the genus Trochochaeta (Polychaeta) in the southern hemisphere with description of a new species. Journal of the Marine Biological Association of the United Kingdom 93(4): 967–972. Buzhinskaja, G.N. & Jørgensen, L.L. (1997): Redescription of Trochochaeta carica (Birula, 1897) (Polychaeta, Trochochaetidae) with notes on reproductive biology and larvae. Sarsia 82(1): 69–75. Capa, M., Hutchings, P. & Peart, R. (2012): Systematic revision of the Sabellariidae (Polychaeta) and their relationships with other polychaetes using morphological and DNA sequence data. Zoological Journal of the Linnean Society 164: 245–284. Chamberlin, R.V. (1919): The Annelida Polychaeta. Memoirs of the Museum of Comparative Zoology at Harvard College 48: 1–514, plates 1–80. Dean, D. (1987): Trochochaeta pettiboneae, a new species (Polychaeta: Trochochaetidae) from the Gulf of Maine with additional comments on T. carica. Bulletin of the Biological Society of Washington 7: 46–49. Fauchald, K. & Rouse, G.A. (1997): Polychaeta systematics: past and present. Zoologica Scripta 26: 71–138. Fauvel, P. (1916): Deux polychètes nouvelles (Disoma watsoni n. sp. et Hyallinecia brementi n. sp.). Bulletin de l’Institut Océanographique 316: 1–10. Fauvel, P. (1932): Annelida Polychaeta of the Indian Museum, Calcutta. Memoirs of the Indian Museum, Calcutta 12(1): 1–262, 9 plates. Gilbert, K.M. (1984): Chapter 8. Family Trochochaetidae Pettibone, 1963. In: Uebelacker, J.M. & Johnson, P.G. (Eds), Taxonomic Guide to the Polychaetes of the Northern Gulf of Mexico. Volume 5: 8.1–8.4. Barry A. Vittor & Associates, Inc. Hannerz, L. (1956): Larval Development of the Polychaete Families Spionidae Sars, Disomidae Mesnil, and Poecilochaetidae n. fam. in the Gullmar Fjord (Sweden). Zoologiska Bidrag från Uppsala 31: 1–204, 57 figures.



Hartman, O. (1947): Disoma franciscanum, a new marine annelid from California. Journal of the Washington Academy of Science 37(5): 160–169, 3 figures. Hartman, O. (1974): Polychaetous annelids of the Indian Ocean including an account of species collected by members of the International Indian Ocean Expeditions, 1963–1964 and a catalogue and bibliography of the species from India. Journal of the Marine Biological Association of India 16: 191–252. Hernández-Alcántara, P. & Solís-Weiss, V. (2011): Trochochaeta mexicana, a new species from an unusual family of Polychaeta, with comments on the world distribution of Trochochaetidae. Journal of the Marine Biological Association of the United Kingdom 91(2): 403–413. Hoagland, R.A. (1920): Polychaetous annelids collected by the United States fisheries steamer “Albatross” during the Philippine expedition of 1907–1909. Bulletin of the United States National Museum 100: 603–635, plates 46–52. Imajima, O. (1989): A new species of Trochochaeta (Polychaeta, Trochochaetidae) from Japan. Bulletin of the National Science Museum, Series A (Zoology) 15(3): 139–146. Levinsen, G.M.R. (1883): Systematisk-geografisk Oversigt over de nordiske Annulata, Gephyrea, Chaetognathi og Balanoglossi, Part II. Videnskabelige Meddelelser fra den Dansk Naturhistorisk Forening i Kjøbenhavn, 1883: 92–350, plates 2–3. Mackie, A.S.Y. (1990): The Poecilochaetidae and Trochochaetidae (Annelida: Polychaeta) of Hong Kong. In: Morton, B. (Ed.), Proceedings of the Second International Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 1986. Hong Kong University Press, pp. 337–362. McIntosh, W.C. (1911): Notes from the Gatty Marine Laboratory, St. Andrews, 2: On Nevaya whiteavsi, a form with certain relationships to Sclerocheilus Grube, from Canada. Annals and Magazine of Natural History, series 8, 7: 149–151, plate 5. Mesnil, F. (1897): Études de morphologic externe chez les Annélides; Remarques complémentaires sur les Spionidiens; La famille nouvelle des Disomidiens; La place des Aonides (sensu Tauber, Levinsen). Bulletin Scientifique de la France et de la Belgique, 30: 83–100, plate 3. Michaelsen, W. (1897): Die Polychaetenfauna der Deutschen Meere, Einschliesslich der benachbarten und verbindenden Gebiete. Wissenschaftliche Meeresuntersuchungen (Kiel and Leipzig), new series 2(1): 1–216, plate 1. Neave, S.A. (1939): Nomenclator Zoologicus. Vol. 2, 1025 pp. Zoological Society, London. Orrhage, L. (1964): Anatomische und morphologische Studien über die Polychätenfamilien Spionidae, Disomidae, und Poecilochaetidae. Zoologiska Bidrag från Uppsala 36: 335–405. Orrhage, L. (1971): Light and electron microscope studies of some annelid chaetae. Acta Zoologica, Stockholm 52: 157–169. Orrhage, L. & Müller, M.C.M. (2005): Morphology of the nervous system of Polychaeta (Annelida). In: Bartolomaeus, T. & Purschke, G. (Eds.), Morphology, Molecules, Evolution and Phylogeny in Polychaeta and related Taxa. Hydrobiologia 535/536: 79–111.

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Örsted, A.S. (1843): Maxicolae. Part 1 of Annulatorum Danicorum Conspectus. 52 pp., 7 plates. Copenhagen. Örsted, A.S. (1844): Zur Classification der Annulaten, mit Beschreibung einiger neuer oder unzulänglich bekannter Gattungen und Arten. Archiv fur Naturgeschichte 10(1): 99–112, plates 2–3. Pettibone, M.H. (1963): Marine polychaete worms of the New England Region. Bulletin of the United States National Museum 227(1): 1–356. Pettibone, M.H. (1976): Contribution to the polychaete family Trochochaetidae Pettibone. Smithsonian Contributions to Zoology 230: 1–21. Purschke, G. & Tzetlin, A.B. (1996): Dorsolateral ciliary folds in the polychaete foregut: structure, prevalence and phylogenetic significance. Acta Zoologica, Stockholm 77(1): 33–49. Radashevsky, V.I, Rizzo, A.E. & Peixoto, A.J.M. (2018). First record of Trochochaeta japonica (Annelida: Spionidae) in Brazil with identification key to species of the genus. Zootaxa 4462(4): 566–578. Rullier, F. (1951): Étude morphologie, histologie et physiologique de l’organe nucal chez les Annélides Polychètes Sédentaires. Annales de l’institute Océanographique 25: 207–341. Radashevsky, V.I., Rizzo, A.E. & Peixoto, A.J.M. (2018). First record of Trochochaeta japonica (Annelida: Spionidae) in Brazil with identification key to species of the genus. Zootaxa 4462(4): 566–578. Rouse, G.A. (2001): Chapter 69. Trochochaeta Örsted, 1843a. In: Rouse, G.W. & Pleijel, F. (Eds.), Polychaetes. Oxford University Press, London, pp. 273–275. Rouse, G.W. & Fauchald, K. (1997): Cladistics and polychaetes. Zoologica Scripta 26: 139–204. Rouse, G.W. & Pleijel, F. (2001): Polychaetes. Oxford University Press, London, pp. 354. Struck, T.H., Nesnidal, M.P., Purschke, G. & Halanych, K.M. (2008): Detecting possibly saturated positions in 18S and 28S sequences and their influence on phylogenetic reconstruction of Annelida (Lophotrochozoa). Molecular Phylogenetics and Evolution 48: 628–545. Thulin, G. (1921): Biologisch-faunistische Untersuchungen aus dem Öresund. Über Cossura longocirrata Webster und Benedict und über die Röhren von Disoma multisetosum. Lunds Universitets Årsskrift, new series, 17(10): 1–14, 17 figures. Webster, H.E. & Benedict, J. (1884): The Annelida Chaetopoda from Provincetown and Wellfleet, Massachusetts. Annual Report of the Commisioner of Fish and Fisheries for 1881. pp. 699–747, plates 1–8. Weitbrecht, B.E. (1984): Muscular anatomy of Trochochaeta multisetosum (Polychaeta; Trochochaetidae). In: Hutchings, P.A. (Ed.), Proceedings of the First International Polychaete Conference, Sydney. The Linnaean Society of New South Wales, 401–412. Zrzavý, J., Říha, P., Piálek, L. & Janouškovec, J. (2009): Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evolutionary Biology 9: 189 14 pp. doi:10.1186/1471-21-48-9-189.

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James A. Blake and Nancy J. Maciolek

7.4.4 Uncispionidae Green, 1982 Introduction The Spionida or spioniform polychaetes are currently grouped into four families: Poecilochaetidae, Spionidae, Trochochaetidae, and Uncispionidae. These taxa are treated in this handbook as separate chapters by Blake et al. (2019), Blake and Maciolek (2019a,b), and the present chapter. The Apistobranchidae and Longosomatidae, which historically have been included with the ­spioniform polychaetes, are treated elsewhere in the handbook (Blake and Petti 2019; Blake and Maciolek 2019c). The Uncispionidae is the smallest and rarest of the spioniform groups currently classified as a separate family. They are characterized by having (1) anteriorly directed parapodia and chaetae of the first chaetiger forming a cephalic cage similar to that of poecilochaetids; (2) bidentate neuropodial hooded hooks similar to those of spionids along most of the body; (3) enlarged, “giant” curved hooks in far posterior segments that are unique among spioniform polychaetes; and (4) unusual oral lobes on the dorsal and ventral lips of the mouth. The first records of these unusual worms were by Hartman (1965) and Hartman and Fauchald (1971), who reported posterior fragments of unusual polychaetes from deep-water off northeastern South America and New England, respectively. These fragments had unusually large posterior bifid hooks, somewhat similar to the hooded hooks of spionids. Hartman (1965) termed these fragments “?spionid”. The first formal description of an uncispionid was by Fauchald and Hancock (1981) of a single specimen from deep water off Oregon. This species was named Uncopherusa bifida and was thought by these authors to belong to the Flabelligeridae. Green (1982) subsequently described a new genus and species, Uncispio hartmanae from southern California that was similar to Uncopherusa bifida. She recognized the affinity of these worms to the spionids and suggested that they constituted a separate spioniform

family that she named the Uncispionidae. Darbyshire and Mackie (2011) described the third uncispionid species, Uncispio reesi from the southern Irish Sea. The most recent account of these rare and unusual spioniform polychaetes is by Blake and Maciolek (2018), based on new deep-sea collections from off North America and Southeast Asia. These authors described two additional species of Uncopherusa: U. papillata from Southeast Asia off Brunei and U. cristata from off Louisiana in the Gulf of Mexico; two new species of Uncispio: U. greenae from off New England and U. hamata from off Louisiana in the Gulf of Mexico; and a new genus and species, Rhamphispio tridentata from New England to South Carolina along the US Atlantic continental slope. To date, the family consists of three genera and eight species, of which most are rare and consist of only a few specimens. In preparing this chapter, we drew on the previous accounts of Uncopherusa bifida, Uncispio hartmanae, and U. reesi and the new taxa we described. We have also examined types from each of the previously described species as well as the fragments recorded by Hartman (1965) and Hartman and Fauchald (1971). Morphology External morphology The bodies of uncispionids are elongate and slender (Fig. 7.4.4.1 D), with or without enlargement of a few anterior segments. In general, these worms are fragile and fragment readily: unless samples are handled with great care, the posterior end is more often lost than retained. The anterior segments may be somewhat dorsoventrally flattened, becoming more cylindrical in middle segments. Darbyshire and Mackie (2011) reported living specimens of Uncispio reesi with a light green color; the new species from off North America and Brunei are light tan or opaque white in alcohol with no particular body pigmentation. The prostomium is narrow, rounded, or blunt on the anterior margin (Fig. 7.4.4.1 A, D); eyes are absent; nuchal organs have not been observed. A short occipital antenna is present (Fig. 7.4.4.1 A) or absent (Fig. 7.4.4.1 D); when present, it arises at a level between the notochaetae of

▸ Fig. 7.4.4.1: Uncispionidae morphology: A, B, Rhamphispio tridentata, anterior end, dorsal view; B, posterior end, left lateral view.

C, D, Uncopherusa papillata, C, anterior end, ventral view of oral structures; D, anterior end, dorsal view of first 11 chaetigers; E, F, Uncispio hartmanae, E, chaetiger 6 with branchiae; F, chaetiger 31, with spinous capillary; G, posterior end, dorsal view. A–D, after Blake and Maciolek (2018); E–G, after Green (1981), not to scale. Abbreviations: anC, anal cirrus; aOrL, anterior oral lobe; br, branchia; eso, esophagus; int, intestine; lOrL, lateral oral lobe; noSp, notopodial spines; ocAn, occipital antennae; pap, papillae; per, peristomium; phrx, pharynx; pOrL, posterior oral lobe; pr, prostomium. Arrows (B, G) denote enlarged posterior spines.



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chaetiger 1. Palps are typically lost; when present, they arise lateral to the prostomium and have a distinct ventral groove. The peristomium is reduced, extended laterally, and merged with the neuropodial p ­ ostchaetal lobes of chaetiger 1 (Fig. 7.4.4.1 A); it surrounds the mouth ventrally. The pharynx is partially eversible, and has two rounded ciliated lobes, called the anterior oral lobes, emerging from the dorsal lip of the mouth (Figs. 7.4.4.1 A, C and 7.4.4.2 B); each lobe bears a small laterally directed fingerlike process. When extended, the pharynx may also have a pair of short lateral lobes and a midventral lobe (Fig. 7.4.4.1 C) (Darbyshire and Mackie 2011, Blake and Maciolek 2018). Parapodia are biramous throughout, with those of chaetiger 1 shifted dorsally and directed anteriorly (Figs. 7.4.4.1 A, C, D and 7.4.4.2 A, B). The podial lobes of chaetiger 2 are short, conical, and may also be shifted dorsally (Fig. 7.4.4.1 A). Subsequent parapodia have short, rounded notopodia and longer lamellate neuropodia, or podial lobes reduced to low mounds (Fig. 7.4.4.1 A, D). The neurochaetae of chaetiger 1 are elongated thickened capillaries that produce the cephalic cage (Figs. 7.4.4.1 A, D and 7.4.4.2 A, B). In species of Uncispio and Rhamphispio, notochaetae of chaetiger 1 are also elongate and part of the cage (Figs. 7.4.4.1 A and 7.4.4.2 A, B); in species of Uncopherusa, the first notochaetae include a group of heavy acicular spines that are sometimes accompanied by thin, short capillaries that produce an armature posterior to the prostomium (Figs. 7.4.4.1 D and 7.4.4.3 A, B). R. tridentata has an enlarged chaetiger 3 that bears heavy crested neurochaetae similar to those found in species of Trochochaeta (Figs. 7.4.4.1 A, 7.4.4.2 A, B, and 7.4.4.3 E) (Blake and Maciolek 2018). Some species of Uncispio are also noted to have neurochaetae with curved limbate crests on chaetiger 3, but these chaetae are relatively small and the actual segment is not enlarged relative to chaetigers 2 and 4 (Darbyshire and Mackie 2011). All other chaetae are simple capillaries or hooks. Notochaetae from chaetiger 3 are typically short capillaries with a fringe of fibrils along one edge, or the fibrils are absent or inconspicuous (Fig. 7.4.4.3 C, D); longer spinose capillaries (Figs. 7.4.4.1 F and 7.4.4.3 H) may also be present in middle chaetigers (Green 1982, Darbyshire and Mackie 2011). In the posterior notopodia of R. tridentata, longshafted bidentate hooded hooks have been observed on some specimens (Fig. 7.4.4.1 B) (Blake and Maciolek 2018). Neurochaetae of anterior chaetigers are short capillaries with a fringe of fibrils along one edge (Fig. 7.4.4.3 F, G); these may be greatly enlarged on chaetiger 3 (Fig. 7.4.4.3 E) as previously noted; these fringed chaetae are in two rows until bidentate hooded hooks begin at about chaetiger 8 or 9. The hooded hooks range from having relatively straight shafts (Figs. 7.4.4.2 C and 7.4.4.3 I, L) to ones that are strongly

Fig. 7.4.4.2: Rhamphispio tridentata morphology. A, anterior end, dorsal view; B, anterior end, ventral view; C, neuropodial hooded hook; D, large modified posterior hook; E, posterior end, right lateral view; F, middle body segments with paired ovaries. All after Blake and Maciolek (2018). A, E, stained with Shirlastain A; B, stained with methyl green. Abbreviations: anC, anal cirrus; br, branchiae; eso, esophagus; int, intestine; ocAn, occipital antenna; ov, ovary; phrx, pharynx. Arrows (E) denote enlarged posterior spines.

sigmoid (Fig. 7.4.4.3 J, K), sometimes with a sigmoid shape (Fig. 7.4.4.3 K). The apical tooth is slightly thinner than the main fang in most species; however, the hooks of Uncopherusa papillata have the apical tooth longer than the main fang (Fig. 7.4.4.3 L). The neuropodial hooks of the posteriormost segments are enlarged and modified, typically with one or two lateral teeth emerging from the shaft below a large curved tip (Figs. 7.4.4.2 D and 7.4.4.4 A, C–E); the accessory teeth may be missing or reduced on the posteriormost hooks (Fig. 7.4.4.4 B, F); the remnant of a hood is usually present. Uncispio hamata has no accessory teeth on any of the enlarged hooks that occur over 10 of the posteriormost chaetigers (Blake and Maciolek 2018). Uncopherusa bifida has up to six posterior segments with modified hooks; other species have two to three posterior segments with modified hooks. In all species, the penultimate segment typically has the largest hooks.



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7.4.4.2 B). These glandular areas stain conspicuously with MG (Fig. 7.4.4.2 B) and may have a secretory function. Additional MG staining is evident ventrally in a V-shaped area posterior to the mouth extending to the anterior margin of chaetiger 3 (Fig. 7.4.4.2 B). There is no comparable staining pattern on the dorsal surface. Uncopherusa papillata did not retain any stain. Sense organs have not been reported for any uncispionid and none were observed in any of our specimens.

Fig. 7.4.4.3: Uncispionidae chaetae. A, B, notopodial spines of chaetiger 1 (Uncopherusa papillata); C, D, notopodial capillaries of chaetiger 3 (Rhamphiospio tridentata); E, large neuropodial crested spines from chaetiger 3 (R. tridentata); F, G, neuropodial fringed capillaries of anterior chaetigers (R. tridentata); H, spinose notopodial capillary from middle segment (Uncispio hartmanae); I–L, hooded hooks: I, (?spionid of Hartman); J, K (R. tridentata); L, U. papillata. A–G, J, K, after Blake and Maciolek (2018); H, after Green (1982), not to scale; I, after Hartman (1965), not to scale.

The branchiae of most uncispionids are short and straplike (Figs. 7.4.4.1 A, D and 7.4.4.2 A), typically fused basally to notopodial lobes (Fig. 7.4.4.1 D) but sometimes not; branchiae are first present from chaetigers 5 or 9 and continue for 2, 3, or up to 22 segments. Darbyshire and Mackie (2011) reported that branchiae of Uncopherusa bifida were small and limited to chaetiger 5. Uncopherusa papillata has rounded, oval-shaped branchiae from chaetigers 8 or 9 through chaetigers 14 or 15 (Fig. 7.4.4.1 G); these are free from the notopodial lamellae. The posterior end of all genera has a terminal anus surrounded by four to eight digitiform lobes (Figs. 7.4.4.1 B, G and 7.4.4.2 E). Darbyshire and Mackie (2011) found conspicuous glandular patches that stained with methyl green (MG) posterior and ventral to some anterior parapodia in Uncispio reesi. We have observed Rhamphispio tridentata to have thickened glandular cells extending from the dorsolateral surface of 10 to 12 anterior segments as a ring around the venter of each segment (Figs. 7.4.4.1 A and

Anatomy There is nothing published regarding the internal anatomy of any uncispionid apart from observations of an eversible ciliated proboscis or pharynx (Darbyshire and Mackie 2011, Blake and Maciolek 2018). Our observations of both Rhamphispio tridentata and Uncopherusa papillata suggest that there is a narrow esophagus extending from the pharynx through at least the first two to three chaetigerous segments; thereafter, an intestine or hindgut fills each segment (Figs. 7.4.4.1 A and 7.4.4.2 B). The intestine narrows in far posterior segments prior to the anal opening. Blake and Maciolek (2018) described ovaries of R. ­tridentata as paired sacs in middle segments that originated from the anterior septa and extended posteriorly about half way along individual segments (Fig. 7.4.4.2 F).

Biology and ecology Habitat. Uncispionids are found in continental shelf and slope depths and seem to prefer sediments with some percentage of clay. Green (1982) reported Uncispio hartmanae from light-brown hard-clay sediment with pebbles. Darbyshire and Mackie (2011) reported that the majority of their Uncispio reesi specimens occurred in a boulder-clay habitat, but also where this substrate was mixed with coarser sediment. Both of those species are from shelf depths: Uncispio hartmanae was found at 222 m off southern California and U. reesi from 137 to 171 m in the southern Irish Sea. In contrast, Uncopherusa bifida (2860 m, off Oregon, USA), Uncopherusa papillata (1725 m, off Brunei, Island of Borneo), Uncispio cristata (955 m, Gulf of Mexico), Uncispio greenae (2110 m, off New England), Uncispio hamata (825 m, Gulf of Mexico), and Rhamphispio tridentata (800–2160 m, US Atlantic continental slope) are from deep-water habitats where they occur in fine-grained sediments of silt and clay (Blake and Maciolek 2018). Behavior No information is available regarding tube morphology or burrow structure of uncispionids. However, the presence of large modified neuropodial hooks in posterior chaetigers

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Fig. 7.4.4.4: Uncispionidae modified posterior spines. A, B, (?spionid of Hartman); A, spine from penultimate segment; B, spine from last segment; C, penultimate spine (Uncispio greenae); D–F, Rhamphispio tridentata; D, E, penultimate spines in different views; F, spine from last segment. A, B, after Hartman (1965), not to scale; C–F, after Blake and Maciolek (2018).

suggests that these chaetae play a role in anchoring the worms within their tubes or burrows. Jumars et al. (2015) suggested that the presence of these hooks might indicate tube building and discrete motility. The presence of a pair of grooved spionid-like palps and an eversible ciliated axial proboscis suggests to us that these worms feed on particles at the sediment–water interface. Darbyshire and Mackie (2011) observed sediment in the gut of the holotype of Uncispio hartmanae. Our specimens of U. greenae, Rhamphispio tridentata, and Uncopherusa papillata all have fine silt particles in their intestine. The anterior, posterior, and lateral lobes associated with the upper and lower lips of the mouth suggest a role in particle selection for feeding and possibly building. Similar to other spioniforms, a pair of tube ­ palps with a ventral ciliated groove likely serves in the initial capture of particles that are then transported toward the mouth along the ciliated groove. The ciliated pair of anterior oral lobes likely plays an important role in further selecting and manipulating particles into the oral opening. Based on the appearance of different specimens of Uncopherusa papillata and Rhamphispio tridentata, it seems as if the pharynx is capable

of expansion and contraction, resulting in the mouth opening being reduced or greatly enlarged. There does not seem to be a distinct, separate proboscis everted, but more likely changes with the configuration of the pharynx as particles are manipulated and ingested. Study of living specimens and histological studies are required to fully understand the structure of the pharynx and the role of these unusual oral structures.

Reproduction and development The eggs of Uncispio reesi have a thick, honeycombed membrane containing prominent cortical alveoli (Darbyshire and Mackie 2011); this type of egg morphology also occurs in species of Poecilochaetus, Trochochaeta, and several genera of Spionidae such as Malacoceros, Dispio, and Aonides (Blake and Arnofsky 1999, Blake 2006). Darbyshire and Mackie (2011) recorded egg diameters of 100 to 120 µm in diameter for U. reesi. Blake and Maciolek (2018) observed eggs in three species: Rhamphispio tridentata, Uncispio hamata, and U. cristata. All had thin membranes and cortical alveoli were not observed. Paired ovaries were observed in



R. tridentata where eggs were in paired sacs; oocytes having a diameter of 40 to 50 µm were released into the coelom. The holotype of U. hamata was observed to have oocytes of about 60 µm in diameter, but these were few. U. cristata had a pair of extremely large, rounded eggs up to 180 µm in diameter in individual segments. Nothing is known about uncispionid reproductive biology or embryology and larval development. However, the egg with thick membranes and cortical alveoli reported by Darbyshire and Mackie (2011) for Uncispio reesi suggest that gametes of that species are probably dispersed in the water column and development occurs in the plankton. Related species of Spionidae, Poecilochaetus, and Trochochaeta having similarly sized eggs with thick membranes have planktic larvae (Hannerz 1956, Blake and Arnofsky 1999, Blake 2006, Blake and Maciolek 2019a,b). However, larvae having characteristics of uncispionids have not been identified in coastal plankton. The thin-membraned eggs observed by Blake and Maciolek (2018) were from deep-water species in which direct or lecithotrophic development is more likely.

Phylogeny and taxonomy Phylogeny Blake and Arnofsky (1999), as part of a review of the reproduction and larval development of spioniform polychaetes, developed a preliminary phylogenetic analysis using 38 characters of 36 genera of Spionidae, Apistobranchidae, Trochochaetidae, Poecilochaetidae, Longosomatidae, and Uncispionidae. Cossura and Cirrophorus were used as outgroups. Among the 38 characters, 14 were reproductive and developmental in nature. The results of this analysis clearly demonstrated that the classification of Spionidae was paraphyletic in that there were two major clades consisting of the subfamily Spioninae and a larger clade consisting of all remaining spionid genera and the genera Heterospio, Poecilochaetus, Trochochaeta, and Uncispio. A minor third clade consisting of the enigmatic genus Pygospiopsis (including Atherospio) was distinct. The close relationship of Uncispio with Poecilochaetus and Trochochaeta demonstrated by Blake and Arnofsky (1999) was largely based on the unique egg morphology of these genera and certain Spionidae in which the egg membranes are thick, honeycombed, and have prominent cortical alveoli. An expanded phylogenetic analysis using additional characters and taxa, including the magelonids and chaetopterids, was later developed as part of a presentation at the Sixth International Polychaete Conference

7.4.4 Uncispionidae Green, 1982 

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in Curitiba, Brazil, in August 1998 (Blake and Arnofsky 2000). This analysis added further support to the preliminary results of Blake and Arnofsky (1999) and demonstrated that reproductive and developmental data, when used together with adult morphology, provide a robust suite of characters to interpret the interrelationships of spioniform polychaetes. However, these analyses, whereas demonstrating that reproductive modes and larval morphology are important in understanding spioniform phylogeny, did not include a sufficiently large suite of adult morphology, including chaetal and parapodial characters, to fully characterize genera such as Poecilochaetus, Trochochaeta, and Uncispio. Although similar to spionids in terms of egg and larval morphology, these taxa differ considerably when adult morphology is considered. We continue to use these three taxa at the family level, but acknowledge their close similarity to Spionidae, and in particular the subfamily Nerininae. Rouse and Pleijel (2001) developed a “polychaete ­ nalysis, metatree” based on a variety of sources. In that a Uncispio was placed in the Spionida with the following taxa: Apistobranchus, Chaetopteridae, Spionidae sensu stricto, Magelona, Heterospio, Trochochaeta, and Poecilochaetus. The Spionida was a sister group to the Terebellida, which includes the cirratuliform and terebelliform families. Recent studies, however, have indicated that Heterospio is more correctly referred to cirratuliform rather than spioniform polychaetes (Blake and Maciolek 2019c). To date, there have been no phylogenetic studies of uncispionids using molecular sequence data. Taxonomic history The first discovery of an uncispionid was by Hartman (1965), who recorded a posterior fragment of a polychaete from deep water off northeastern South America that had unusual, greatly enlarged, posterior bifid hooks. Hartman recognized this worm as spionid-like and thus termed the fragment “?spionid”. An additional record of “?spionid, unknown” from abyssal depths between New England and Bermuda was mentioned by Hartman and Fauchald (1971). The first described species of an uncispionid was Uncopherusa bifida by Fauchald and Hancock (1981) from deep water off Oregon, USA. At the time, it was referred to the family Flabelligeridae largely because of the anterior-projecting cephalic cage and because the body, which was encrusted with sediment, was said to have papillae on the surface. However, spionid-like neuropodial hooded hooks were present together with enlarged, modified hooks in posterior para­podia similar to those observed earlier by Hartman (1965).

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Green (1982) subsequently described a similar-appearing species from shelf depths off southern California that she referred to a new genus and species, Uncispio hartmanae. After evaluation of her new species and comparison with Uncopherusa  bifida, she established a new family, the Uncispionidae, for these unusual worms. After the study by Green (1982), there were no published observations of uncispionids until Blake and Arnofsky (1999) and Blake (2006) referred to an undescribed species of Uncispio from deep water in the northwest Atlantic that had modified neuropodial spines in chaetiger 3. Read (2004) listed Uncopherusa sp. A in a checklist of polychaetes from New Zealand but no details of this species have been published. Brief summaries of the Uncispionidae were provided by Fauchald and Rouse (1997), Rouse and Pleijel (2001), and Jumars et al. (2015). Darbyshire and Mackie (2011) described Uncispio reesi from shallow-water habitats in the southern Irish Sea and examined and redescribed U. hartmanae and Uncopherusa bifida. Sufficient specimens of their new species were available to allow several aspects of the biology of these worms to be described. During deep-water surveys of the US Atlantic and Gulf coasts and off Brunei, Island of Borneo, in the South China Sea, five additional species of these unusual spioniform polychaetes were found. These five species, including one new genus, were described by Blake and Maciolek (2018): Uncopherusa papillata, Uncopherusa cristata, Uncispio greenae, Uncispio hamata, and Rhamphispio tridentata. Type specimens of the three previously described species were also examined. Genera diagnoses Family Uncispionidae Green, 1982 Diagnosis (after Blake and Maciolek 2018): Small, slender polychaetes with palps inserted dorsally at the junction between the pro- and peristomium (postectal prostomial margins). Occipital antenna present or absent. Peristomium dorsally expanded with lateral wings, extended ventrally encompassing mouth; separate pair of large ciliated peristomial lobes typically located on dorsal lip of mouth anterior to prostomium; a separate unpaired lobe on the ventral lip visible if extruded; a pair of lobes present or absent lateral to expanded pharyngeal area ventral to mouth opening. Parapodia biramous with reduced, simple postchaetal lobes. Branchiae present on some anterior and middle chaetigers, basally fused or separate from notopodial lobes. Chaetae simple, including capillaries (smooth, with fringe of fibrils, or spinose), bidentate hooded hooks, and enlarged, modified hooks on two or more posterior

neuropodia. Neuropodial capillaries of chaetiger 1 long, thick, directed anteriorly forming cephalic cage; notopodia of chaetiger 1 with shorter, thin capillaries or with thick spines (genus Uncopherusa). Chaetiger 3 enlarged with heavy crested spinous chaetae in neuropodia (genus Rhamphispio) or chaetiger 3 not expanded and chaetae not modified. Terminal anus surrounded by up to eight digitate lobes or cirri. Remarks: The presence of long capillaries that arise from chaetiger 1 and form the cephalic cage, bidentate hooded hooks in the neuropodia, and large modified neuropodial hooks in far posterior neuropodia are diagnostic and likely synapomorphies for species of Uncispionidae. The presence of enlarged crested neuropodial spines in chaetiger 3 of Rhamphispio tridentata suggests a close relationship with the genus Trochochaeta. However, the latter genus lacks hooded hooks. To date, only eight species of Uncispionidae are known, five from deep water and three from shelf depths. Six of the eight described species are known only from one to three specimens. Uncopherusa Fauchald and Hancock, 1981 Type species: Uncopherusa bifida Fauchald and Hancock, 1981 by monotypy. Diagnosis (emended by Blake and Maciolek 2018): Cephalic cage formed from neurochaetae of chaetiger 1; notopodia of chaetiger 1 with acicular spines and few companion capillaries. Occipital antenna present or absent. Chaetae include smooth and fringed capillaries, acicular spines; bifid neuropodial hooded hooks, and enlarged posterior neuropodial hooks. Some parts of body covered with numerous small glandular papillae, or body smooth. Anus surrounded by four short lobes. Remarks: Uncopherusa bifida is known from a single specimen collected off Oregon in deep water (Fauchald and Hancock 1981). Two specimens of a second species, U. papillata, were collected off Brunei in the South China Sea and a single specimen of a third species, U. cristata, was collected from off Louisiana in the Gulf of Mexico (Blake and Maciolek 2018). These species differ from Uncispio and Rhamphispio in having the cephalic cage formed by only the neurochaetae, rather than both notoand neurochaetae. The notochaetae of chaetiger 1 of the three species of Uncopherusa consist of short, thick, acicular spines accompanied by a few short companion ­capillaries. In U. bifida, the spines are in transverse rows; in U. papillata, the spines are in curved rows forming a rosette; in U. cristata, the spines are arranged in diagonal rows directed posteriorly. Previously, the generic



definition of Uncopherusa included reference to the number of posterior chaetigers with modified neuropodial hooks, but new species of Uncispio required the removal of this character from the diagnoses (see below). In their description of U. bifida, Fauchald and Hancock (1981) reported that the anterior segments were papillate and encrusted with sand, as were subsequent parapodial bases and the entire posterior end, but subsequent observers did not confirm the presence of papillae on the holotype, instead describing it as smooth (Darbyshire and Mackie 2011). However, as part of our observations on the new U. papillata from off Brunei, numerous small papillae were observed on anterior segments and elsewhere on the body. At present, three species of Uncispionidae, all from deep water, are referred to Uncopherusa. 1. Uncopherusa bifida Fauchald and Hancock, 1981. Eastern Pacific, off Oregon, USA, 2860 m. 2. Uncopherusa cristata Blake and Maciolek, 2018. Gulf of Mexico, off Louisiana, USA, 955 m. 3. Uncopherusa papillata Blake and Maciolek, 2018. South China Sea, off Brunei, Island of Borneo, 1725 m. Uncispio Green, 1982 Type species: Uncispio hartmanae Green, 1982 by ­monotypy. Diagnosis (emended by Blake and Maciolek 2018): Body somewhat flattened dorsoventrally, cylindrical medially; three distinct regions defined by chaetae and branchiae sometimes apparent. Occipital antenna present or absent. Cephalic cage formed by smooth capillaries of both notoand neuropodia of chaetiger 1. Some anterior chaetigers with short limbate capillaries with one edge bearing fringe of fine fibrils. Median notopodia with or without long, spinose capillaries in addition to short, haired capillaries. Median neuropodia with bidentate hooded hooks and inferior bundle of long, curved, smooth capillaries. Posterior notopodia with simple fringed capillaries or long smooth capillaries with thick shafts and bent tips; neuropodial bidentate hooded hooks present. Posterior neuropodia with enlarged modified hooks. Anus terminal with up to eight anal cirri. Remarks: The four known species of Uncispio differ from Uncopherusa in that both the noto- and neurochaetae of chaetiger 1 are long and form the cephalic cage instead of only the neurochaetae. Previously, Uncispio and Uncopherusa were said to differ in the number of posterior chaetigers with enlarged modified hooks: Uncispio was limited to two chaetigers with modified hooks whereas Uncopherusa had up to six. One of the new species,

7.4.4 Uncispionidae Green, 1982 

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U. hamata, however, has up to 10 posterior chaetigers with modified hooks, precluding the use of the number of posterior chaetigers with hooks as a generic character. Furthermore, R. tridentata has three posterior chaetigers with modified hooks. To date, four species of Uncispionidae are referred to Uncispio. 1. Uncispio greenae Blake and Maciolek, 2018. Western North Atlantic, off New England, USA, 2110 m. 2. Uncispio hamata Blake and Maciolek, 2018. Gulf of Mexico, off Louisiana, USA, 825 m. 3. Uncispio hartmanae Green, 1982. Eastern Pacific, off Santa Cruz Island, CA, USA, 222 m. 4. Uncispio reesi Darbyshire and Mackie, 2011. Northeast Atlantic, west of Anglesey, Wales, UK, 137 to 171 m.

Rhamphispio Blake and Maciolek, 2018 Type species: Rhamphispio tridentata Blake and Maciolek, 2018, by monotypy. Diagnosis (after Blake and Maciolek 2018): Chaetiger 1 with both noto- and neuropodial capillary chaetae directed forward forming a cephalic cage. Occipital antenna present. Chaetiger 3 greatly enlarged, with wide, curved, spinous golden capillaries with fimbriated crest in neuropodia. Neuropodia with bidentate hooded hooks in median and posterior chaetigers; notopodia with capillary chaetae in anterior and median chaetigers and bidentate hooded hooks in far posterior chaetigers. Hirsute or spinous capillary notochaetae absent. Enlarged modified hooks or spines with two lateral teeth present in posterior neuropodia. Pygidium with four anal cirri. Remarks: Rhamphispio differs from both Uncopherusa and Uncispio in having an expanded chaetiger 3 that bears enlarged crested spinous neurochaetae, notopodial hooded hooks in far posterior chaetigers, and enlarged posterior neuropodial hooks with two lateral teeth or flanges, which imparts a tripartite appearance to the hooks. The enlarged chaetiger 3 and large modified spines are reminiscent of similar modifications to chaetiger 3 found in species of Trochochaeta, suggesting the close relationship of the Uncispionidae to the Trochochaetidae. Smaller limbate neurochaetae occur on chaetiger 3 and subsequent anterior chaetigers in other uncispionids (Darbyshire and Mackie 2011, this study) but these are not large and spinous as in R. tridentata. At present, only a single species is known. 1. Rhamphispio tridentata Blake and Maciolek, 2018. Western North Atlantic, off New England and North Carolina, USA, 800 to 2160 m.

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References Blake, J.A. (2006): Spionida. In: Rouse G.W., Pleijel F. (Eds.), Reproductive biology and phylogeny of Annelida. Enfield, USA: Science Publishers. pp. 565–638. Blake, J.A. & Arnofsky, P.L. (1999): Reproduction and larval development of the spioniform Polychaeta with application to systematics and phylogeny. In: Dorresteijn A.W.C. & Westheide W. (Eds.), Reproductive strategies and developmental patterns in annelids. Hydrobiologia 402: 57–106. Blake, J. A. & Arnofsky, P. L. (2000): Systematics and phylogeny of the spioniform Polychaeta. Bulletin of Marine Science 67: 657 (abstract). Blake, J.A. & Maciolek, N.J. (2018): New species and records of Uncispionidae and Pygospiopsis (Polychaeta, Spionida) from deep-water off the East and West Coasts of North America, the Antarctic Peninsula, and Southeast Asia. Zootaxa 4450(2): 151–195. Blake, James A. & Maciolek, N.J. (2019a): 7.4.2. Poecilochaetidae Hannerz, 1956. pp. 103–119, In: Purschke, G., Böggemann, M. & Westheide, W. (Eds.), Handbook of Zoology. Annelida. Volume 2: Annelida Basal groups and Pleistoannelida, Sedentaria II. i–x, 1–460. De Gruyter, Berlin. Published on line 2018. Blake, James A. & Maciolek, N.J. (2019b): 7.4.3. Trochochaetidae Pettibone, 1963. pp. 120–135, In: Purschke, G., Böggemann, M. & Westheide, W. (Eds.), Handbook of Zoology. Annelida. Volume 2: Annelida Basal groups and Pleistoannelida, Sedentaria II. i–x, 1–460. De Gruyter, Berlin. Published on line 2018. Blake, James A. & Maciolek, N.J. (2019c): 7.3.1.9. Longosomatidae Hartman, 1944. pp. 457–465, In: Purschke, G., Böggemann, M. & Westheide, W. (Eds.), Handbook of Zoology. Annelida. Volume 1: Annelida Basal groups and Pleistoannelida, Sedentaria I. i–xii, 1–480. De Gruyter, Berlin. Published on line 2018. Blake, James A., Maciolek, N.J. & Meißner, K. (2019): 7.4.1. Spionidae Grube, 1850. pp. 1–103, In: Purschke, G., Böggemann, M. & Westheide, W. (Eds.), Handbook of Zoology. Annelida. Volume 2: Annelida Basal groups and Pleistoannelida, Sedentaria II. i–x, 1–460. De Gruyter, Berlin. Published on line 2017. Blake, James A. & Petti, M.A.V. (2019): 5.1 Apistobranchidae. pp. 133–134, In: Purschke, G., Böggemann, M. & Westheide, W. (Eds.), Handbook of Zoology. Annelida. Volume 1: Annelida Basal groups and Pleistoannelida, Sedentaria I. i–xii, 1–480. De Gruyter, Berlin. Published on line 2014. Darbyshire, T. & Mackie, A.S.Y. (2011): Review of Uncispionidae (Annelida: Polychaeta) with the description of a new species of Uncispio. Italian Journal of Zoology 78(S1): 65–77. Fauchald, K. & Hancock, D.R. (1981): Deep-water polychaetes from a transect off central Oregon. Allan Hancock Monographs in Marine Biology 11: 1–73. Fauchald, K. & Rouse, G. (1997): Polychaete systematics: past and present. Zoologica Scripta 26(2): 71–138. Green, K.D. (1982): Uncispionidae, a new polychaete family (Annelida). Proceedings of the Biological Society of Washington 95: 530–536. Hannerz, L. (1956): Larval development of the polychaete families Spionidae Sars, Disomidae Mesnil and Poecilochaetidae n. fam. in the Gullmar Fjord (Sweden). Zoologiska Bidrag från Uppsala 31: 1–204. Hartman, O. (1965): Deep-water benthic polychaetous annelids off New England to Bermuda and other North Atlantic areas. Occasional Papers of the Allan Hancock Foundation 28: 1–378. Hartman, O. & Fauchald K. (1971): Deep-water benthic polychaetes off New England to Bermuda and other North Atlantic areas. Allan Hancock Monographs in Marine Biology 6: 1–327.

Jumars, P.A., Dorgan, K.M. & Lindsey, S.M. (2015): Diet of worms emended: an update of polychaete feeding guilds. Annual Review of Marine Science 7: 497–520 + Supplemental Appendix A. Family-by-Family Updates: A1–A350 + Supplemental Table of Guild Characteristics: 1–14. Read, G.B. (2004): Checklist of New Zealand Polychaeta species. Available online at: www.annelida.net/nz/Polychaeta/ References/NZPolySpeciesListV2.htm. Rouse, G.W. & Pleijel, F. (2001): Polychaetes. Oxford, UK: Oxford University Press. 354 pp.

María Capa and Pat Hutchings

7.4.5 Sabellariidae Johnston, 1865 Introduction Sabellariidae Johnston, 1865, is a well-defined and highly specialized group of marine annelids commonly known as honeycomb or sandcastle worms. They live in characteristic tubes of cemented sand grains, other mineral or biogenic particles such as Foraminifera (Kirtley 1994), sometimes attached to one another forming large reefs that can extend over several kilometers. They cannot survive out of their tubes and are unable to build new ones if removed from them. Sabellariids have a well-developed operculum with rows of golden paleae that can seal the entrance of the tube when the animal withdraws into it (Figs. 7.4.5.1 A, B and 7.4.5.2 A, C). Both structures, tube and operculum, provide protection from desiccation, silt deposition, and predators. The monophyly of Sabellariidae has been assessed, and relies on synapomorphies such as the presence of an operculum formed by the head and two anterior segments, a pair of peristomial palps, nuchal organs located at the base of palps, a building organ, oral filaments originating from segment 1 (not the peristomium), paleae on the anterior segments, uncini without a rostrum or main fang and without a handle or manubrium, segmental branchiae inserted dorsally on the parapodia and an expansion of the gut in the abdomen called the “proventriculus” (Capa et al. 2012, Hutchings et al. 2012, Helm et al. 2018a). There are currently 132 nominal species (Hutchings et  al. 2012, Capa et  al. 2015, Faroni-Perez et  al. 2016) belonging to 12 genera, considered monophyletic in most but not in all cases (Capa et  al. 2012, Hutchings et  al. 2012). Sabellaria Lamarck, 1812, Idanthyrsus Kinberg, 1867, and Lygdamis Kinberg, 1867 represent more than half of all the species described in the family. In contrast, Gunnarea Johansson, 1927, Paraidanthyrsus Kirtley, 1994, and Bathysabellaria Lechapt and Gruet, 1993 include only one or two known species each. Members of this family have been reported from all



major oceans and seas. Most described sabellariids live in intertidal or shallow depths but there are some genera and species restricted to the continental shelf or the deep sea. Although most genera seem to be broadly distributed or cosmopolitan, the species distribution and ecological niche seems to be geographically restricted and with bathymetric limitations, driven by abiotic factors required for settlement and tube-building (e.g., water temperature, water movement, availability of consolidated substrate and types, and abundance of sediment) (Kirtley 1994, Bastida-Zavala and Becerril-Tinoco 2009). The best studied species are mainly gregarious and intertidal. These are characterized by a long life span, very high fecundity, and high dispersal capability of larvae which remain in the plankton for long periods (Giangrande 1997, McCarthy et  al. 2003). In gregarious species, larval settlement is induced by the presence of conspecific reefs (Pawlik 1988a,b). Some fossil tubes from Mexico, Chile, and the USA, from the Cambrian (more than 550 million years old), have been attributed to members of this family (Caline et  al. 1988, Pohler 2004). Recognizable sabellariid fossil tubes have been reported from the Pleistocene rocks in Chile (Philippi 1887, Kirtley and Tanner 1967).

Morphology Body shape Sabellariids are medium-sized annelids, with adults measuring 2 to 5 cm long. They have compact and wide bodies. Live animals are often pigmented brown or green with conspicuous red, brown, or green branchiae due to blood pigments (Fig. 7.4.5.1 A, B). Their segmented body is divided into four specialized regions: operculum, parathorax, abdomen, and caudal region. A review of the diverse terminology used to describe the various morphological features of the family has been undertaken (Capa et al. 2012), and the names proposed have been followed herein. The operculum is the most characteristic feature of this group of annelids, and it is a complex and specialized structure formed by the fusion of the head (prostomium and peristomium), and the first two chaetigers (thorax) (Figs. 7.4.5.1 A, B and 7.4.5.2 A, C). It consists of two head outgrowths as fleshy lobes which distally bear rows of simple chaetae, the paleae, and are surrounded by appendages called opercular papillae (Figs. 7.4.5.1 A, B and 7.4.5.2 A, C). The opercular lobes range from completely fused (Bathysabellaria, Neosabellaria Kirtley, 1994 and Phragmatopoma Mörch, 1863) to completely separated (Gesaia Kirtley, 1994, Idanthyrsus, Lygdamis, Mariansabellaria Kirtley, 1994, Paraidanthyrsus, Phalacrostemma

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Marenzeller, 1895, and Sabellaria), with the intermediate condition and a deep groove on the ventral margin and a fused dorsal margin (Gunnarea and Tetreres Caullery, 1913). The distal end of the operculum, or the disc, is oriented perpendicular or obliquely to the longitudinal axis of the body (Fig. 7.4.5.2 A). On the ventral and inner side of each opercular lobe, other simple (unbranched) or compound (branched) appendages, the tentacular or oral filaments may be inserted (Figs. 7.4.5.1  C and 7.4.5.2  C). Tentacular (oral) filaments are ciliated and often grooved proximally, and are involved in the transport of food particles to the mouth and sediment particles to the ventral area for tube construction (Dales 1952, Orrhage 1978, Dubois et  al. 2005, Riisgård and Nielsen 2006). In species of Phalacrostemma, the oral filaments are replaced by elongate buccal flaps or oral plates or by apophyseal ridges along the margins of the buccal cavity (Kirtley 1994, Capa et al. 2012). A pair of grooved, ciliated, and contractile (Treadwell 1926, Faroni-Perez pers. comm.) palps is present (Orrhage 1978, Orrhage and Eibye-Jacobsen 1998, Orrhage and Müller 2005). The prostomium has been defined as a narrow ridge fused laterally to the first chaetiger (Dales 1952, Fauchald 1977) in species with completely separated opercular lobes and it is represented externally by a triangular area on the anterior ventrum between fused opercular stalks, between the mouth opening and the beginning of the oral filaments (Lechapt and Kirtley 1996). An unpaired appendage, referred to as the median organ (Capa et al. 2015, Faroni-Perez et al. 2016, Helm et  al. 2018a, Meyer et  al. 2018), is present at the dorsal junction of the opercular lobes, when these are not completely fused (Kirtley 1994) or at the base of the operculum, in the anterior midline of prostomium, in Bathysabellaria spinifera Lechapt and Kirtley, 1996 with fused lobes, and is considered a prostomial structure (Lechapt and Kirtley 1996). The opercular paleae are simple chaetae (often referred to as capillaries or spines) with a proximal shaft, attached to the muscular tissue (Ebling 1945, Kirtley 1994), and a distal exposed, and generally ornamented blade. Paleae consist of an inner core, striated longitudinally, and a clear, homogeneous outer layer referred to as thecae with more or less packed fibers or microtubules (Ebling 1945, Kirtley 1994), thicker in the shaft than on the blade. In some paleae, an alveolar structure can be observed, consisting of gas-filled cavities arranged in longitudinal and transverse rows. The chaetogenesis of paleae occur in two separate chaetigerous sacs on each lobe (Ebling 1945, Dales 1952, Orrhage 1978), each forming two distinct series of paleae; the outer and inner rows (Wilson 1929, Hartman 1944), corresponding to the chaetae from the first two anterior highly modified segments. Larval paleae are all

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Fig. 7.4.5.1: Photographs of live specimens. A, Lygdamis giardi (McIntosh, 1885), dorsal view, from Lizard Island, Australia, showing the four specialized regions; B–D, Idanthyrsus australiensis (Haswell, 1883), from Sydney, Australia; B, anterior end, dorsal view; C, anterior end, ventral view; D, posterior end, ventral view. Photos A, A. Semenov; B–D, modified from Capa et al. (2012). Abbreviations: br, branchiae; ip, inner paleae; ll, lateral lobes (notopodial lobes chaetiger 2); mo, median organ; nch, notochaetae; nh, nuchal hooks; nut, notopodial unicinal tori; of, oral filaments; op pap, opercular papillae; opa, outer paleae; pa, paleae.

similar in shape but intermediate forms are produced in juvenile stages until metamorphosis (Wilson 1929, Eckelbarger 1976, Eckelbarger and Chia 1976). During settlement, the chaetal sacs rotate and the paleae that were located on the innermost side become the outer paleae and vice versa, the chaetae sacs enlarge to form the opercular stalks continuing as separated lobes or else fusing together partially or completely (Fauchald 1977, Lechapt and Kirtley 1996). Even though adults possess two rows of paleae, the orientation of their distal blades sometimes gives animals the appearance of presenting three concentric rows of paleae, the inner and the median rows formed in the inner chaetigerous sac (Kirtley 1994). In those cases (Neosabellaria, Phragmatopoma, and Sabellaria species), the blades of the “median” and inner rows are directed outwards and inwards, respectively. The outer paleae are generally arranged in facing semicircles on each side, but in species of Phalacrostemma, they display a bispiral arrangement

(Kirtley 1994). Opercular paleae are replaced during metamorphosis and subsequent adult growth changing their shape during ontogeny (Dales 1952, Gruet 1991). In larval stages (features retained in some adults), paleae have been classified as choanothecae, hemithecae, and platythecae depending on the shape of the section of the blade (for a description of different types, see Kirtley 1994). Adults show a great diversity in number, shape, and size of paleae, and the terminology used for describing the different morphologies in the literature is highly variable (Fig.  7.4.5.2 A, D–F). They display variation in the angle of the longitudinal axis of blades, and shafts (from straight to geniculate), the shape of the blade (flat, concave, or cylindrical), the shape of the lateral and distal margins (smooth or denticulate), and most of the possible combination of these conditions can be found in some sabellariids, with up to four different paleae morphologies being present within a species (when two types of “middle” paleae can be found in addition to the outer and



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Fig. 7.4.5.2: A, Operculum, top view, Sabellaria lungalla Hutchings et al., 2012; B, nuchal spines (hooks) and palps of Lygdamis augeneri Kirtley, 1994; C, anterior end, ventral view of I. australiensis (Haswell, 1883); D–F, outer paleae; D, L. giardi (McIntosh, 1885); E, Phalacrostemma maloga Hutchings et al., 2012; F, Idanthyrsus nesos Hutchings et al., 2012; G, parathoracic notopodia of I. australiensis; H, abdominal uncini of I. australiensis, frontal view; I, abdominal uncini of L. giardi, lateral view; J, details of abdominal neurochaetae of I. australiensis.

inner paleae). Most sabellariids bear stout and cylindrical chaetae on the dorsal edge of the opercular lobes, called nuchal spines, with straight or bent distal pointed tips (also known as nuchal hooks; Fig. 7.4.5.1 A, B), and with a more or less developed limbation on the inner or outer margin of the hooks (Fig. 7.4.5.2 B). They are formed in the sacs of the opercular paleae, and are therefore considered as derived from chaetiger 1 (Orrhage 1978). Ventrally, on both sides of the building organ, the neuropodia of chaetiger 1 is provided with conical cirri, and capillary neurochaetae. The neuropodia of the second thoracic segment bears cirri, and bundles of capillary neurochaetae with thecae that make them appear as bipinnate (as referred to by Kirtley 1994). Dorsal cirri (one to three), referred herein as lateral lobes may be present in this segment, between the noto- and neuropodia (Fig. 7.4.5.1 A, B). Branchiae can be present or absent on segment 2. Three or four parathoracic segments follow the thorax. They are provided with notopodia as enlarged lobes, and conical neuropodia. Although chaetae in neuropodia are smaller in size, notopodia bear retractile stout chaetae

with lanceolate tips and cylindrical capillary chaetae alternating in one row (e.g., Kieselbach and Hausen 2008) (Fig. 7.4.5.2 G). In some genera, the lanceolate chaetae are frayed or have denticulate tips. Neuropodia show higher variation between taxa and some species have both lanceolate chaetae and capillaries whereas others only bear capillaries or lanceolate chaetae. All segments have paired conical branchiae (Fig. 7.4.5.1 A, B), provided with transverse rows of cilia. Glandular areas are present on the ventrum of this parathoracic region, and they produce adhesive substances for tube building (Vovelle 1965, Wang et al. 2010). An abdominal region follows the parathoracic segments. This region can be easily separated by the presence of uncini in the notopodia. Some authors indicate an absence of lanceolate neurochaetae, and only the presence of capillaries in this region, although a gradual change has been observed in some species (Kieselbach and Hausen 2008). Abdominal segments are biramous, with notopodia as transverse tori, with a single row of pectinate uncini with two rows of similar-sized denticles

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pointing anteriorly, diminishing in width posteriorly (Fig. 7.4.5.2 H, I), and neuropodia bearing conical ventral cirri, and fascicles of capillary chaetae arranged in one or two rows with two separated formation sites (Kieselbach and Hausen 2008) (Fig. 7.4.5.2 J). Dorsal parapodial branchiae are present on abdominal segments; in some species, they are restricted only to anterior abdominal segments whereas in others they are present to the caudal region and decrease in size posteriorly (Fig. 7.4.5.1 A, B). The cauda is an apparently unsegmented body region (see Wilson 1929 for a different viewpoint). It is a smooth and cylindrical tube that is curved along the ventral surface of the abdomen where feces are evacuated through its distal anus (Fig. 7.4.5.1 D). Few studies have been undertaken on the internal morphology of Sabellariidae and available information is scant and patchy. The cuticle of Sabellaria vulgaris Verrill, 1873 lacks any collagenous orthogonal grid of thick fibrils (Storch 1988) as found in many other polychaetes. Myogenesis has been studied in Sabellaria alveolata (Linneaus, 1767) by Brinkmann and Wanninger (2008). In the early trochophore stage, the first muscles appear in close proximity to the chaetal sacs. Then, pharyngeal musculature starts to form and the muscles of the chaetal sacs develop and later two longitudinal muscles start to differentiate on the dorsal side and two on the ventral side, with the onset of elongation in the hyposphere. In the metatrochophore, additional pharyngeal and chaetal sac muscles develop followed by the formation of transversal thorax muscles on the ventral side. Premetamorphic larval stages already have a complex musculature consisting of prominent chaetal sac muscles that are interconnected by muscular bands. Two dorsal and two ventral longitudinal strands run along the body and, in addition, the parathoracic segments bear transverse and oblique muscles and the pygidium is provided with circular musculature (Brinkmann and Wanninger 2008). The gut is a straight tube running from mouth to anus, including cauda, with a broadened structure referred as to “proventriculus” (Kirtley 1994) in anterior abdominal segments. Adults lack a buccal organ (Dales 1962), although it is not known if it is present during development (Rouse 2001). The axial proboscis is non muscular, and lack dorsolateral folds (Purschke and Tzetlin 1996). The gut is provided with absorptive and serous gland cells, which are thought to secrete proteolytic enzymes into the lumen of the gut (Michel 1988). Circular muscles surround the pharynx (Brinkmann and Wanninger 2008). The circulatory system has been described as closed and without a heart body (Eisig 1887, Fauchald and Rouse 1997, but see Eckelbarger 1979, for a different opinion). Some confusion

has taken place in this regard, probably due to the interpretation of the intravasal chlorogogen gland (Eisig 1887) as a string heart body inside the dorsal blood vessel in the thoracic region situated above a large nephridium (Meyer 1887, 1888, Rouse and Fauchald 1997, Rouse 2001). Neosabellaria cementarium (Moore, 1906) has, like most polychaetes, two well-developed fluid transport systems, blood vascular system and segmented coelomic cavities. Sabellariids have only a simple peritoneal layer of highly interdigitating cells, which separates the blood and coelomic fluid (Smith 1986, as Sabellaria cementarum). The blood in N. cementarium arises as a fluid during the larval stage, and the hemoglobins are produced later (Smith 1986) and are dissolved in the blood without distinct blood corpuscles. Although the branchiae of sabellariids presumably function as sites for gas exchange, this actually needs to be confirmed (Hutchings 2000). Larvae of Neosabellaria cementarum are provided with protonephidia with podocytes (Smith 1986, Smith and Ruppert 1988, as Sabellaria cementarum). The excretory system of adults consists of a single pair of metanephridia and terminal monociliated cells provided with a long duct that extends caudally for a few segments, U-turns frontally, and leads to the exterior of the animal on the dorsal side of the first segment (Meyer 1887, Dehorne 1952, Smith 1986, Smith and Ruppert 1988, Bartolomaeus and Quast 2005). Posterior segmental organs act as gonoducts (Meyer 1887). The ovaries are distinct, retroperitoneal, paired structures located on the genital blood vessels that extend from the caudal face of the intersegmental septa of abdominal segments (Eckelbarger 1979). The brain is surrounded by ganglion cells except on the ventral side and has four commissures, as most annelids (Orrhage 1978), situated in the same plane (Orrhage and Müller 2005). The first two communicate with the ventral roots of the circum esophageal connective and the other two merge laterally into the dorsal roots of this connective (Orrhage and Müller 2005). A detailed description of the cephalic nervous system, placement of ganglia and innervation of some anterior structures on some Sabellaria and Idanthyrsus species can be found in Orrhage (1978). He concludes that the paired anterior structures, referred herein as palps, are homologous to the palps of polychaete families (also corroborated later by Orrhage and Eibye-Jacobsen 1998 and Orrhage and Müller 2005), that the oral filaments are extended lateral parts of the upper lip of the mouth (suggested previously by Johansson 1927), and that the opercular lobes with their paleae and dorsal hooks or chaetae (if present) represent the notopodia of the first two segments (as indicated also by Dales 1952). Helm et  al. (2018b) described the ventral nerve cord in Sabellaria alveolata



as subepithelial and comprising two main cords interconnected by numerous intersegmantal commissures. In each cord a giant fiber is present. Studies on the neurogenesis show that sabellariid larvae express both larval and adult features. For instance, late larval stages of S. alveolata start forming the cerebral ganglion and the two circumesophageal connectives, considered as adult features, before metamorphosis. Moreover, and contrary to previous studies (Lacalli 1984), it seems like sabellariids larvae are not provided with two separate nervous systems but only have one (Voronezhskaya et  al. 2003, McDougall et  al. 2006, Brinkmann and Wanninger 2008). Another distinct attribute with respect to generation of the neural system in other annelids is that, at least in S. alveolata, three pairs of segmental neurons are formed synchronously and simultaneously to the formation of the first three larval segments whereas all commissures of the ventral central nervous system develop sequentially in a strict anterior-to-posterior progression even though the two thoracic segments form anterior to the first three larval segments in Sabellariidae (Wilson 1929, Cazaux 1964, Eckelbarger 1975, Brinkmann and Wanninger 2008). Several sensory organs have been reported in a number of sabellariids. In the median line of the fused part of the opercular lobes, cup-shaped spots of brown pigments are present, containing light-sensitive cells (Eckelbarger 1975, 1977, Orrhage 1978, Kirtley 1994, Capa et  al. 2015, Faroni-Perez et  al. 2016). In Idanthyrsus australiensis (Haswell, 1883), these eyepots were investigated, showing an unusual type of photoreceptors with a corrugated sensory membrane (Helm et al. 2018a). Two pairs of similar eyespots found in S. alveolata have been considered as homologous to the cerebral eyes found in other polychaetes and associated to the brain in this species (Meyer et  al. 2018). The sensory function of the median organ (Fig. 7.4.5.1 A) has been confirmed by two recent studies in S. alveolata and I. australiensis (Helm et  al. 2018a, Meyer et  al. 2018). These studies find evidence for a chemosensory function and their homology with nuchal organs. Both eyespots and median organ are considered as prostomial structures (Dales 1952, Lechapt and Kirtley 1996). It is hypothesized that the median organ is involved in shadow reflex (Meyer et al. 2018). The specialized epithelium at the base of each palp, innervated from the dorsal and ventral commissure of the dorsal root of the circumesophageal connective was considered as evidence of being the nuchal organs (Orrhage 1978, Kirtley 1994, Purschke 1997). However, a recent study found several innervated ciliated pits located along the median organ, sharing ultrastutural similarities to those found in some Spionidae’s nuchal organs (Helm  et  al.

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2018a). Lateral organs are absent. The ciliated tentacles present in larval stages have also been suggested as potential sensory organs in several species (Amieva and Read 1987).

Reproduction and development The reproductive strategies and development in Sabellariidae have been studied in several species, mainly gregarious and with intertidal distribution, including Sabellaria alveolata (see Cazaux 1964, Wilson 1929, 1970a, Brinkmann and Wanninger 2008), Sabellaria spinulosa (Leuckart, 1849) (Wilson 1929, 1970b), Sabellaria vulgaris Verrill, 1873 (Eckelbarger 1975, Curtis 1975), Sabellaria floridensis Hartman, 1944 (Eckelbarger 1977), Sabellaria wilsoni Lana and Gruet, 1989 (Fewkes 1889, Aviz  et  al. 2018) Lygdamis muratus (Allen, 1904) (Bhaud 1975, Wilson 1977), Phragmatopoma caudata Krøyer in Mörch, 1863 (as P. lapidosa, see Eckelbarger 1976, Mauro 1975, Eckelbarger and Chia 1976), Phragmatopoma californica (Fewkes, 1889) (see Eckelbarger 1977, Pernet and Strathmann 2011), Idanthyrsus sp. (see Bhaud and FernándezÁlamo 2001), and Neosabellaria cementarium (see Pernet and Strathmann 2011). Larvae of these species share the external morphology until the late planktonic stage when they develop some of the characteristic generic features such as the number of parathoracic segments, the absence or presence of opercular spines or hooks with or without limbation (Bhaud and Fernández-Álamo 2001), or some of the opercular paleae (Mauro 1975). Larvae of Neosabellaria and Phragmatopoma species are provided with a prototroch and also a recently identified metatroch and food groove ciliary bands, required for opposedband feeding (Pernet and Strathmann 2011) (Fig. 7.4.5.3). Larvae of P. californica possess simple rhabdomeric ocelli as light-sensitive organs on either side of the dorsal hump. The most likely function of the sensory tufts is either mechanoreception or chemoreception (Amieva et al. 1987). Late larval stages are equipped with tentacles with specific motile and immotile cells for perception of settlement cues and discrimination of appropriate adult environments (Amieva and Reed 1987, Amieva et al. 1987). These tentacles are also involved in feeding, construction of the mucous tube in the juvenile, locomotion, attachment, and become the palps of the adults (Amieva and Reed 1987). Because they arise from behind the prototroch (Dales 1962), on the anterior margin of the upper transverse lip, in front of, and dorsal to the mouth (Johansson 1927, Orrhage 1978), they are considered as peristomial palps (for other points of view, see Amieva et  al. 1987). In late larval development, the cauda arises posteriorly

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Fig. 7.4.5.3: Scanning electron micrographs of trochophore larvae showing the ciliary bands and provisional chaetae. A, 9-day-old larva of Neosabellaria cementarium, lateral view; B, 5-day-old larva of Phragmotopoma californica, lateral view. Abbreviations: fg, food groove; mo, mouth; mt, metatroch; pt, prototroch. Originals from Pernet and Strathmann (2011).

(Eckelbarger 1975) but further abdominal segments are added ahead of it with growth after its appearance, indicating that the pygidium is not terminal. In Phragmatopoma, metamorphosis involves an elongation of the body and dramatic changes in the head region. The tentacles rotate anteriorly until they project forward, the chaetae are replaced by 6 to 10 pairs of primary paleae, the entire head shrinks in relative size, the building organ appears ventral to the mouth, and various appendages develop on a number of segments (Eckelbarger 1976). After settlement, development continues rapidly; within one month, juveniles closely resemble the adult worm (Eckelbarger 1976).

Biology and ecology Most species of Sabellariidae live in the surf zone or shallow depths (less than 10 m deep) but members of Bathysabellaria, Gesaia, and Phalacrostemma, and other sabellariid species are restricted to particular oceanic provinces such as the continental shelf or the deep sea. Although most genera of this family occur in several oceans, only Gesaia is regarded as being cosmopolitan (Kirtley 1994). Sabellariid species seem to be geographically restricted even though they have planktotrophic larvae of long duration with the potential to be dispersed (Scheltema 1986, Pawlik and Mense 1994, Giangrande 1997). This suggests that other factors are responsible for their limited distributions, such as habitat, depth, and ecological requirements, which are required for settlement and construction of their tubes (Kirtley 1994, Bastida-Zavala and

Becerril-Tinoco 2009). Larval behavior in the water column (i.e., vertical migration) is not well understood. Considering the statistical modeling of larvae dispersion/retention (Ayata et  al. 2009), it is possible that in stable environmental conditions, sabellariids reproduce by recruitment from nearby populations, which maintains the wellknown reefs or aggregates over time, but the connections between long distances are mainly due to extreme events, evidenced by the release of gametes during storms (Barry 1989, Faroni-Perez pers. com.). At depths below the wave action (2 m deep), there is not enough current for the animals to feed and capture sand grains for tube building (Kirtley 1966) and the colonies reported at less than 100 m are probably located where strong submarine currents occur (Kirtley and Tanner 1968), although there is no actual experimental data to support this concept. Shallow-water sabellariids show some zonation pattern in the intertidal and subtidal (Achari 1974, Pohler 2004, Bailey-Brock et al. 2007), and intertidal species can withstand several hours of exposure to air during low tide (Pohler 2004). Sabellariids are generally found in or near soft bottoms because they rely on the availability of sand grains to build their tubes. However, they do need to firmly cement their tube onto a stable substrate. P. lapidosa has shown some tolerance to burial experiments for short periods and low depth burial, but colonies mostly died after more than 1 week of burial below 10 cm of sand (Sloan and Irlandi 2008). A study dedicated to determining the species delimitation between morphologically similar species of Phragmatopoma in the Atlantic and Pacific coasts of America



(P. californica, P. caudata and P. virgini Kinberg, 1867, two of which have been shown to be able to interbreed in the laboratory), found molecular evidence to support the validity of each of these species (Pawlik 1988b, Drake et al. 2007, Nunes et al. 2016). Sabellariidae has been regarded as a homogenous group of polychaetes in regards to their reproductive strategies based mainly on shallow water species and, at least those that have been studied, seem to be gonochoric, broadcast spawners, and with external fertilization (Wilson 1991, Giangrande 1997). Populations are composed of equal proportions of males and females (Dales 1952, Eckelbarger 1976) with no sexual dimorphism except for the color of the gamete-containing abdominal segments in mature individuals, with creamy-white sperm and steel-blue eggs (Kirtley 1966, 1968, de Jorge et al. 1969, Eckelbarger 1976). In Phragmotopoma caudata (as P. lapidosa) gametes first develop in both sexes approximately 6 to 8 weeks after larval settlement, and the worms are fully mature after 4 months (Eckelbarger 1976). Females have discrete ovaries in abdominal segments where oogenesis takes place until near the end of vitellogenesis (Eckelbarger 2005). Detailed studies on the early stages of oogenesis of Phragmatopoma showed that both Golgi and rough endoplasmic reticulum are involved in yolk synthesis and that distinctive yolk bodies are found but disappear in the mature eggs (Eckelbarger 1979, 1988). The developing oocytes have egg membranes in Sabellaria Lamarck, 1812 (Pasteels 1965a, b, Franklin 1966) and Phragmatopoma (see Eckelbarger 1979, 2005), which have well-developed microvilli and they are assumed to be involved in nutrient absorption during oogenesis and are also involved in fertilization (Franzén and Rice 1988). In P. caudata (as P. lapidosa) oogenesis takes 48 h and the oocytes have extensive contact with the lumen of the genital blood vessels and show high endocytotic activity (Eckelbarger 1979, 1988, 2005). Mature sperm of Sabellaria alveolata and Idanthyrsus australiensis (as I. pennatus) have distinctive long, tapering, and striated acrosomes, and laterally displaced flagella (Pasteels 1965a, Eckelbarger 1984, Jamieson and Rouse 1989). Within the acrosome, three regions may be distinguished: a long tapering anterior region with evenly spaced transverse striations, a central region made up of an electron-dense collar with concentric rings, and a posterior region separated from the nucleus, which is bulbous and surrounds a central subacrosomal space that contains loosely packed filaments (Franzén and Rice 1988). Males and females release the gametes into their tubes through a series of gonoducts in the abdominal segments that are later expelled into the water column in

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short bursts by the rapid withdrawal of the head region into the tube (Eckelbarger 1984). The presence of sperm in the water generally stimulates the spawning of other adjacent males and also induces the eggs to be released by females (Eckelbarger 1984). Phragmatopoma californica is sexually mature all year long (Barry 1989). Spawning has been reported as continuous, semicontinuous, or seasonal depending on the species studied (Eckelbarger 1976, Smith and Chia 1985). The eggs of P. caudata (as P. lapidosa) are sticky, and adhere to sand grains upon expulsion, which could be an adaptation to restrict dispersal in the turbulent surf zone (Eckelbarger 1984). Phragmatopoma californica exhibits a spawning response to damage from intense storms allowing it to maximize reproductive effort when the likelihood of recruitment success and the probability of adult mortality are high (Barry 1989). Experimental studies on the changes occurring inside the fertilized egg and meiotic- and meiosis-related events are critical in polarizing the egg cell (Dorresteijn and Fischer 1988) and setting up the animal and vegetal poles. Parallel to this ooplasmic segregation (Costello 1948), localization of developmental potential is occurring, providing cells the capacity to form the mesoderm and the apical tuft in future larvae as shown for S. vulgaris and N. cementarium (see Hatt 1932, Render 1983). Subsequent cleavages produce blastomeres with quantitative differences of the egg plasm (Speksnijder and Dohmen 1983). For more details of the early cleavages and the development of the early embryo including species of Sabellaria (see Dorresteijn and Fischer 1988 and references therein). In Phragmatopoma, metamorphosis and settlement occur after 14 to 30 days in laboratory conditions (Mauro 1975, Eckelbarger 1975, 1976, 1977, Amieva and Reed 1987). Field study estimated longer planktonic lifetime being between 2 and 5 months for P. californica (Fewkes, 1889) (Barry 1989) and between 4 and 10 weeks for S. alveolata (see Dubois et  al. 2007), although this species has also been reported as remaining competent in the plankton for up to 11 months (Wilson 1971). Upon settling, the larva actively moves over the substrate, presumably evaluating possible attachment sites, and when this is selected, the metamorphosing larva secretes and attaches a cylindrical, mucoproteinaceous tube upon which it begins cementing small fragments that generally increase in size with growth (Kirtley 1966, Multer and Milliman 1967). Sabellariids may live between 3 and 10 years (Wilson 1971, Gruet 1986). They actively build tubes made of sand, shell fragments, or other suitable particles attached by glue to the dark layer of mucoprotein secretions (Vovelle 1965, Gaill and Hunt 1986, Wang et  al. 2010). The tubes are attached to a variety of substrata, including rocks,

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seaweeds, or invertebrates or other sabellariid tubes (Uebelacker 1984, Hutchings 2000, Morgado and Tanaka 2001, Pérez et al. 2005). In sabellariid reefs, the tubes are arranged in parallel as a honeycomb, with the tube opening facing major currents, growing as a three-dimensional structure. Sabellariids are suspension feeders that collect particles from the water column using their extended oral filaments, which can reach approximately 1.5 cm above the aperture of its tube (Dubois et al. 2005, 2009). The body and tentacle movements are able to create a current in the opposite direction to the surrounding water circulation near the animals, which allows them to collect and sort particles efficiently before their collection in food grooves (Dubois et al. 2005). Oral filaments, palps, mouth, and lips are ciliated structures also accompanied by mucocytes that secrete mucopolysaccharides helping in the transport of the particles into the mouth and which prevents particles being removed by local currents (Dales 1952, Dubois et al. 2005). There are several mechanisms preceding the particle ingestion including the above-mentioned bidirectional particle transport on the oral tentacles, acting as a preliminary sorting mechanism, pseudofeces production allowing individuals to reject excess particles before ingestion, and the contribution of the palps to cleaning the oral tentacles when overloaded (Dubois et  al. 2005, 2009). Several species, mainly of Phragmatopoma, Sabellaria, Gunnarea, and Idanthyrsus, build small aggregates to large reefs in the intertidal and shallow waters on temperate and tropical coasts in many parts of the world (Achari 1974, Kirtley 1974, Caline et al. 1988, 1992, McCarthy et al. 2008, Barrios et al. 2009). Sabellaria and Idanthyrsus are present in Australia but massive reefs have not been observed (Hutchings et al. 2012). Larvae in swarms have been observed to settle almost synchronously with densities of up to 4 million per square meter (Kirtley 1994, although Dubois et al. 2007 provide other figures). However, aggregations of adult colonies are seldom more densely spaced than 15,000 to 60,000 individuals per square meter in temperate areas (Caline et al. 1988, Kirtley 1994) and higher in tropical latitudes (Faroni-Perez, pers. com), indicating massive larval death after settlement. Reefs off the coast of Florida can cover areas of nearly 1 km wide and 9.8 km long. These reefs can occupy wide areas along the coast, and dominate the marine habitat and are considered important in the sorting, deposition, and stabilization of beaches and protecting the shore from heavy surf (Kirtley 1967, Multer and Milliman 1967, Gram 1968, Kirtley and Tanner 1968, Achari 1974, Caline et al. 1988, Pawlik 1988a,b). In some places, enhancing its distribution has been considered as a protective measure

to reduce beach erosion (Pohler 2004). Sabellariid reefs are protected under the international network of protected sites Natura 2000 network (www.natura.org). Reef-building sabellariids have been the focus of several taxonomic, biological, and ecological studies because they have been considered as one of the most important building organisms after corals in coastal environments (Fournier et  al. 2010). In such colonies, the number of crevices that could provide shelter for other organisms is reduced but as the reef breaks up with time, it provides habitats for various organisms (Gruet 1982). Large and old reefs are considered hotspots of diversity, providing refuge and food for many invertebrate species (e.g., Wilson 1971, Caline et  al. 1988, Pawlik 1988a,b, Dubois et al. 2002, Sepúlveda et al. 2003, McCarthy et al. 2008, Fournier et  al. 2010, Desroy et  al. 2011), and fish (Gilmore 1977, Lindeman and Snyder 1999). Larvae of gregarious sabellariids are induced to settle by the presence of conspecific cemented sand tubes or mucous tubes of juveniles (Eckelbarger 1978a, b, Pawlik 1986, 1988a,b, 1992) and few species (i.e., P. californica) have been shown to be able to delay metamorphosis while searching for conspecific aggregations (Pawlik 1988b). Chemical signals that control the settlement are species-specific. Specific free fatty acids used in the mucoproteins “cement” secreted by the worms to stick the sand particles in tube formation were isolated as the inducers for metamorphosis in two species of Phragmatopoma (Pawlik 1986, 1988a, b). However, these compounds did not trigger settlement in some gregarious Sabellaria species, suggesting that they are species-specific (Pawlik 1988a,b, 1992). Larvae can also colonize a new substratum if unsuccessful in locating conspecifics (Toonen and Pawlik 1994), if the food supply is low, and also in cases of currents transporting larvae that find suitable and available substrate (Bremec et al. 2013). Solitary species do not show this preference for conspecifics already in the settlement area. In laboratory experiments, N. cementarium (as Sabellaria cementarium) show no settlement preferences for conspecific tube sand (Pawlik and Chia 1991), but a large reef has been reported (Posey et  al. 1984). Similarly, Sabellaria nanella Chamberlin, 1919, reported as solitary (Lana and Bremec 1994), was recently observed in dense aggregates (Bremec et al. 2013). These formations by species previously reported as solitary are likely the result of larval entrainment and concentration at the time of settlement (Pawlik and Mense 1984). Sabellariid reefs are entirely dependent on the recruitment of planktonic larvae for reef maintenance and growth (Pawlik and Faulkner 1988). The main biological factors that affect the structural development



of reefs seem to be the reproduction and recruitment mechanism of the pelagic larvae, which are modeled by physical factors associated with the local hydrodynamics (Gruet 1986, La Porta and Nicoletti 2009, Culloty et al. 2010, Bremec et al. 2013). The proteinaceous adhesive produced to glue tube particles by sandcastle worms is secreted from the building organ onto suitable particles as they are pressed onto the end of the tube. The major protein components of the adhesive are a group of polyacidic and polybasic heterogeneous proteins, referred to as Pc3x (Zhao et al. 2005, Wang et al. 2010). The glue is secreted as a fluid that penetrates into the holes between the particles but seconds after becomes a foam with porous granules, completely solidified after some hours (Vovelle 1965, Wang et  al. 2010). The physicochemical properties of this adhesive make it an ideal water-borne underwater bioadhesive (Shao et al. 2009, Wang et al. 2010). This cement has also been shown to have practical applications in medicine, and is used as a degradable adhesive for broken bone reconstruction (Shao et al. 2009, Shao and Stewart 2010, Winslow et al. 2010).

Phylogeny and taxonomy Similar to many other annelid families, the taxonomic history of the Sabellariidae has been convoluted. The first species of Sabellariidae to be mentioned in the scientific literature was by Réaumur in 1711, which was described 50 years later as Tubularia arenosa anglica (see Ellis 1755). Linnaeus (1758) used these illustrations in Systema Naturae 10th edition and published it as Tubipora arenosa. In the 12th edition, it was synonymized with Sabella alveolata (Linnaeus 1758) and later to Sabellaria alveolata (see Lamarck 1818). Johnston (1865) erected the family Sabellariidae, although many subsequent workers used the younger name Hermellidae, which was erected by Malmgren (1867) based on the name Hermella, a synonym of Sabellaria (see Kirtley 1994). Subsequent studies by Kinberg (1867), Marenzeller (1895), Ehlers (1901), Moore (1906), Caullery (1913), Fauvel (1914) Annenkova (1925), Treadwell (1926) Johansson (1927) Hartman (1944), and Kirtley (1994) described additional species and their morphology. Even before the recent assessment of the monophyly of the family (Capa et al. 2012), the cohesion of the group relied on morphological features such as the presence of the operculum bearing rows of paleae derived from the first two segments, the presence of the oral filaments on the operculum, the division of the body into four regions, and the arrangement of chaetae. One of the main taxonomic

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contributions to this group is the worldwide taxonomic revision of the family undertaken by Kirtley in 1994. He rearranged species within genera and erected new ones, increasing the number of genera to 12. Kirtley (1994) also classified genera into two subfamilies, Sabellariinae and Lygdamiinae, based merely on the number of parathoracic segments, a condition that is established very early in the course of development (Bhaud and FernándezÁlamo 2001). However, his revision and classification was not performed in a phylogenetic framework and recent phylogenetic analyses of the family found no support for these two subfamilies (Capa et  al. 2012, Hutchings et  al. 2012) (Fig. 7.4.5.4). Subsequent studies have dealt mainly with new species descriptions or partial taxonomic revisions of certain genera (e.g., Lechapt and Kirtley 1998, Nishi and Kirtley 1999, Nishi and Núñez 1999, Nishi et al. 2004, 2010, 2015, Bailey-Brock et  al. 2007, Hutchings et  al. 2012), increasing the total number of nominal species in the family to 132. The phylogenetic affinities of the Sabellariidae are still not well understood (e.g., Capa et al. 2012) and close relationships with members of Sabellida (Levinsen 1883, Meyer 1888, Hatschek 1893, Benham 1896, Knight-Jones 1981, Fitzhugh 1989, Rouse and Fauchald 1997), Spionida (Meyer 1888, Caullery 1914, Dales 1962), or Terebellida (Savigny 1822, Fauchald 1977) have been suggested based on morphological features. More recent phylogenetic hypotheses combining morphological and molecular data have indicated that Sabellariidae is closely related to spionids, although with little support (Rousset et  al. 2004, Capa et al. 2011, 2012), and other studies including behavioral and ecophysical information (Amieva and Reed 1987, Dubois et al. 2005) backing up earlier larval development and palp innervation studies (Dales 1962). The two phylogenetic studies of the family to date (Capa et  al. 2012, Hutchings et  al. 2012), based on morphological features, were unable to resolve the relationships between members of Sabellariidae unless implied weighting was applied (see Capa et al. 2012, for details on methodology) due to the high amount of homoplasy accumulated in the group. The subfamilies erected by Kirtley (1994) were, in both cases, recovered as paraphyletic (Fig. 7.4.5.4). Key characters with phylogenetic signals are those from the operculum and anterior end (Capa et  al. 2012). They show a broader morphological variation between members of Sabellariidae and a combination of short opercula, and geniculate outer paleae and inner concave paleae arranged in semicircles were considered the synapomorphies for a well-supported clade including Phalacrostemma, Bathysabellaria, Gunnarea, Paraidanthyrsus, Sabellaria, Phragmatopoma, and Neosabellaria

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 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.5.4: Proposed phylogenetic hypothesis of members of Sabellariidae, based on morphological data (modified from Hutchings et al. 2012).

(Capa et al. 2012). This clade was also recovered monophyletic later on but excluding Neosabellaria and Gunnarea, with an uncertain position in the tree (Hutchings et  al. 2012). In contrast, the number of parathoracic segments was shown to be homoplastic, with four segments being the plesiomorphic condition and reducing to three twice during the radiation of the sabellariids (Capa et al. 2012, Hutchings et  al. 2012). Gregarious and reef-building sabellariids were found scattered on the tree indicating that this behavior, together with the physiological and ecological adaptations found in members of the colonial species, did not seem to have any phylogenetic constraint (Capa et al. 2012). The monophyly of Bathysabellaria, Idanthyrsus, Mariansabellaria, Phalacrostemma, Phragmatopoma, and

Tetreres has been assessed but Gesaia, Lygdamis, Sabellaria, and Neosabellaria could be paraphyletic (Capa et al. 2012, Hutchings et al. 2012). Genera diagnoses Family Sabellariidae Johnston, 1865 Diagnosis: Tubiculous annelid with compact body divided into four regions: operculum (head and thorax), parathorax, abdomen, and cauda. Operculum formed by prostomium, peristomium, and first two segments. It bears two peristomial palps, a median organ, a building organ adjacent to the mouth, tentacular filaments originating from segment 1 and characteristic chaetae called paleae. Nuchal organs present as ciliary pits in medial organ. Parathorax with unique parapodial rami and lanceolate



chaetae in noto- and neuropodia. Abdomen with unequal parapodial rami and with uncini in notopodia, with two longitudinal rows of six to nine teeth each, a subrostrum and subrostral process present, without a handle or manubrium; and simple capillaries or lanceolate chaetae in neuropodia. Cauda is a smooth cylindrical tube, apparently unsegmented, which is curved along the ventral surface of the abdomen. Parapodial branchiae present on most segments along the body. Tube made out of mucus and sediment particles. Bathysabellaria Lechapt and Gruet, 1993 Type species: Bathysabellaria neocaledoniensis Lechapt and Gruet, 1993 Two gregarious species found in deep water (450–700 m) off New Caledonia (Lechapt and Kirtley 1998). Diagnosis: Opercular lobes completely fused along its length. Opercular disc perpendicular to longitudinal axis. Numerous opercular papillae varying in size depending on the species. Outer paleae numerous, arranged in semicircles; shaft and blade slightly geniculate (forming an angle), blades faintly excavated, with smooth margins, except when distal tips frayed or broken. Inner opercular paleae arranged in semicircles, giving the appearance of one row, straight, slightly excavated, with smooth margins. One pair of nuchal spines, only slightly curved distally. Three or four simple (unbranched) tentacular filaments present; buccal flaps absent. Palps similar in length to operculum. Conspicuous median organ present (Kirtley 1994, corrigenda). Neuropodia of segment 1 with one cirrus on each side of building organ and capillary chaetae. Segment 2 with one pair of triangular-shaped lateral lobes. Thoracic branchiae absent. Four parathoracic segments. Parathoracic notochaetae lanceolate and capillaries alternating; neurochaetae only capillaries. Abdominal branchiae present, reduced, or absent in posterior segments. Gesaia Kirtley, 1994 Type species: Phalacrostemma elegans (Fauvel, 1911) Eight species reported from deep waters of all major oceans, between 770 and 5790 m (Kirtley 1994). Diagnosis: Operculum longer than wide, completely divided into two free lobes and distal disc perpendicular to operculum; few (four to eight pairs) long and conical opercular papillae. Three to five simple (unbranched) tentacular filaments along margins of buccal cavity. Buccal flaps absent. Palps shorter or similar in length to operculum with obvious groove. Conspicuous median organ (cirrus) at dorsal junction of lobes present. Outer paleae arranged in semicircles with straight, cylindrical,

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smooth blades (with frayed thecae but no proper denticles). Inner opercular paleae arranged in a single row, like a short line, on the dorsal half of the inner margin of lobes, with straight cylindrical and smooth blades. One pair of nuchal hooks, without limbation. Neuropodia of segment 1 with two or three pairs of cirri on both sides of building organ and without neurochaetae. Two lateral lobes in segment 2 (only described in type species). Thoracic branchiae present (according to Kirtley 1994). Four pairs of parathoracic segments. Parathoracic neurochaetae only capillaries. Gunnarea Johansson, 1927 Type species: Hermella gaimardi (Quatrefages, 1848) One species from Cape Town, South Africa (Quatrefages 1848), forming reefs from intertidal to 47 m (Kirtley 1994). Diagnosis: Operculum length similar to maximum width, with lobes partially fused (with deep indentation on ventral margin) and distal disc perpendicular to longitudinal axis. Numerous small and rounded opercular papillae on its perimeter. Outer paleae arranged in semicircles; geniculate, with flat blades, smooth lateral margins, and distal margin with asymmetrical teeth. Inner paleae arranged in semicircles as a single row, strongly geniculate with flattened but excavated blades. Nuchal spines absent. Palps shorter than half of the operculum. Tentacular filaments compound. Buccal flaps absent. Conspicuous median organ absent. Neuropodia of segment 1 with one cirrus on each side of building organ and capillary neurochaetae. Two triangular lobes between noto- and neuropodia of segment 2, ventral one, broad and subdivided or with crenulated margins. Thoracic branchiae present. Three parathoracic segments. Parathoracic notochaetae lanceolate and capillaries alternating; neurochaetae similar but smaller. Abdominal branchiae present on most abdominal segments. Idanthyrsus Kinberg, 1867 Type species: Idanthyrsus macropaleus Schmarda, 1861 Twenty species, generally found in shallow water in the tropics or temperate waters as isolated individuals but some species also inhabit boreal and deep water domains and aggregations of individuals have also been found (Hutchings et al. 2012). Diagnosis: Operculum longer than wide, with lobes completely divided and distal end sloping posteriorly (oblique to longitudinal axis). Operculum papillae varying in number and size depending on species. Outer paleae arranged in semicircles with straight and flat blades and lateral and distal margins appearing sharply denticulated. Inner opercular chaetae arranged in one row along the inner margin

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 7.4 Sedentaria: Sabellida/Spionida

of opercular lobes, with straight and cylindrical blades. One or two pairs of nuchal spines with bent tips (hooks) with or without limbations on the concave margin. Palps similar in length to the operculum. Conspicuous median organ with eyespots on its sides (on specimens examined). Tentacular filaments compound (branching); buccal flaps absent. Neuropodia of segment 1 with capillary chaetae, with conical cirri (only one pair of cirri in all species examined). Segment 2 with one to four triangular lateral lobes. Three parathoracic segments with notochaetae consisting of lanceolate and capillary chaetae and only thin lanceolate neurochaetae (on species examined). Branchiae from segment 2 diminishing in size on posterior abdominal segments. Lygdamis Kinberg, 1867 Type species: Lygdamis indicus Kinberg, 1867 Twenty-one species (Hutchings et  al. 2012, Capa et  al. 2015). Species are known from the shallow subtidal areas, shallow shelf areas, and on continental slopes to depths of 515 m, most records are from tropical and subtropical latitudes with a few from boreal waters. Diagnosis: Operculum longer than wide with lobes completely separated and distal end sloped posteriorly (oblique to longitudinal axis). Numerous opercular papillae varying in size depending on the species. Outer paleae arranged in semicircles, straight, with flat blades, lateral and distal margins smooth. Inner opercular chaetae arranged in one row along the inner margin of opercular lobes with straight and cylindrical or slightly flattened blades. One pair of nuchal spines with bent tips (hooks) and without limbations. Palps similar in size to the operculum. Median organ elongate at the dorsal junction of the opercular lobes. Tentacular filaments compound (branching); buccal flaps absent. Neuropodia of segment 1 with a conical cirrus, with or without capillary chaetae. Segment 2 with three triangular-shaped lobes between noto- and neuropodia, in some species, rounded and small. Four parathoracic segments with notochaetae consisting of lanceolate and capillary chaetae and neurochaetae similar in shape but smaller. Branchiae from segment 2 to mid-abdominal segments. Mariansabellaria Kirtley, 1994 Type species: Phalacrostemma norvegicum Strømgren, 1971 Two species reported from 180 to 2000 m off the west coast of North and South America and Norway (Kirtley 1994). Diagnosis: Operculum longer than wide with lobes completely divided into two symmetrical halves and distal disc perpendicular to longitudinal axis; long conical papillae around its perimeter. Outer paleae, arranged in semicircles, straight and cylindrical or slightly flattened with

smooth margins. Inner paleae, few in number, arranged in a short single row near the dorsal junction of margin of lobes, straight and cylindrical. One or more pairs of straight nuchal spines without limbation. Palps grooved and (considerably) longer than operculum. Tentacular filaments arranged in single rows. Buccal flaps absent. Conspicuous median organ absent. Neuropodia of segment 1 with one cirrus on each side of building organ; capillary neurochaetae absent. One or two triangular lateral lobes on segment 2. Thoracic branchiae absent. Four parathoracic segments. Parathoracic notochaetae lanceolate and capillaries alternating; neurochaetae only capillaries. Members of the genus have a conspicuous ventral glandular area on the parathoracic segments (Kirtley 1994), a potential autapomorphy for the group. Branchiae present on anterior abdominal segments but not on posterior ones. Neosabellaria Kirtley, 1994 Type species: Sabellaria cementarium Moore, 1906 Seven species, restricted to the Indo-Pacific (Bailey-Brock et al. 2007). Diagnosis: Operculum length similar to maximum width, with lobes completely fused, although shallow midventral indentation sometimes present at the proximal end; distal end flat and perpendicular to the longitudinal axis. Conical and small opercular papillae. Outer paleae numerous, arranged in semicircles, geniculate, with excavated blades, smooth lateral margins and denticulated distal margin with a midline plume. Inner opercular paleae giving the appearance of two rows. Middle paleae geniculate with excavated, smooth blades and pointed tips directed outward, some species with rounded-tipped blades also present. Innermost paleae strongly geniculated, with short and concave ones directed inward. Nuchal spines absent. Compound tentacular filaments arranged in series of rows; buccal flaps absent. Palps shorter than half length of operculum (often half of the operculum length). Median organ at dorsal junction of lobes of opercular stalk present in some specimens, but small. Neuropodia of segment 1 with one pair of cirri and capillary chaetae. Segment 2 with two pairs of triangular-shaped lobes between notoand neuropodia. Thoracic branchiae present. Three parathoracic segments. Parathoracic notochaetae lanceolate and capillaries alternating; neurochaetae similar in shape but smaller. Abdominal branchiae absent in posterior segments. Paraidanthyrsus Kirtley, 1994 Type species: Hermella quadricornis Schmarda, 1861 Monotypic, species known from only from New Zealand nearshore shallow water.



Diagnosis: Operculum with length similar to width, lobes completely divided into two free lobes and distal disc perpendicular to longitudinal axis; numerous short papillae around its perimeter. Outer paleae arranged in semicircles, geniculate, with flat blades, lateral margins with long and pointed denticles, distal margin without a distal plume. Inner paleae in a single row, arranged in semicircles, strongly geniculate, with flat blades and tips directed inward. Two or three pairs of nuchal hooks with bent tips (hooks) and limbation of the convex side. Tentacular filaments compound (branching) arranged in more than eight rows; buccal flaps absent. Palps similar in length to operculum. Conspicuous median organ absent. Segment 1 with a small and rounded cirrus on both sides of building organ and with capillary chaetae on the neuropodia. Segment 2 with two triangular-shaped lateral lobes. Thoracic branchiae present. Three parathoracic segments. Parathoracic notochaetae lanceolate and capillaries, similar in shape but smaller in neuropodia. Abdominal branchiae absent in posterior abdominal segments. Phalacrostemma Marenzeller, 1895 Type species: Phalacrostemma cidariophilum Marenzeller, 1895 Twelve species that live solitary or in aggregations; reported from deep water in different localities of the Atlantic and Indo-Pacific (Lechapt and Kirtley 1998, Hutchings et al. 2012). Diagnosis: Opercular width similar to length, operculum completely divided into two free lobes and distal disc perpendicular to operculum; 8 to 10 pairs of long and conical opercular papillae around lobes. Few simple (unbranched) tentacular filaments along margins of the buccal cavity, absent in some species. Buccal flaps present (or secondarily absent). Palps similar in length to operculum. Small median organ at dorsal junction of lobes. Outer paleae arranged in a spiral with straight, cylindrical, smooth blades (with ornamented thecae but no denticles). Few (two to eight) pairs of inner opercular paleae present, arranged in a short line on the dorsal half of the inner margin of lobes, straight, cylindrical, or slightly flattened blades and smooth margins. Two to five pairs of nuchal spines with bent tips (hooks) present and limbation on the concave margin. Neuropodia of segment 1 with one to three cirri on both sides of the building organ and capillary neurochaetae. Segment 2 with two digitiform lateral lobes between noto- and neuropodia. Thoracic branchiae present. Four pairs of parathoracic segments. Parathoracic notopodia with lanceolate and capillaries alternating, neuropodia with capillaries and fine lanceolate chaetae. Abdominal dorsal branchiae absent in posterior segments.

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Phragmatopoma Mörch, 1863 Type species: Phragmatopoma caudata Krøyer in Mörch, 1863 Five species, all forming large reefs in intertidal and shallow-water areas (with the exception of P. californica found to depths of 200 m), with an amphi-American distribution (Kirtley 1994, Drake et al. 2007), and Indian Ocean (Mohan et al. 2017). Diagnosis: Operculum longer than wide, with lobes completely fused to each other, although shallow midventral indentation sometimes present in proximal end. Distal disc flat and perpendicular to longitudinal axis. Numerous digitiform and short opercular papillae around perimeter of distal disc. Outer paleae numerous, arranged in semicircles; geniculate, with flat blades, smooth lateral margins, distal denticles, and a midline plume. Inner opercular paleae giving the appearance of two concentric rows, with paleae strongly geniculate with convex blades and pointed tips directed inward, middle paleae almost covering innermost paleae. Nuchal spines absent. Compound (branching) tentacular filaments arranged in series of rows; buccal flaps absent. Palps similar in length to operculum. Conspicuous median organ absent. Neuropodia of segment 1 with one pair of conical cirri on both sides of building organ and capillary chaetae. Segment 2 with two pairs of triangular-shaped lateral lobes. Thoracic branchiae present. Three parathoracic segments. Parathoracic notochaetae lanceolate and capillaries alternating; neurochaetae similar in shape but smaller. Abdominal branchiae continue to posterior segments. Sabellaria Lamarck, 1818 Type species: Sabella alveolata Linnaeus, 1767 Forty-one species (Hutchings et  al. 2012, Read and Fauchald 2019); solitary and/or gregarious, found mainly in the Atlantic and Indo-Pacific Oceans. Diagnosis: Operculum length similar to maximum width, completely divided into two symmetrical lobes; distal disc flat and perpendicular to longitudinal axis. Numerous short and conical opercular papillae around operculum. Outer paleae numerous, arranged in semicircles; geniculate, with flat blades, smooth lateral edges, and smooth or denticulated distal margin and, sometimes, a midline plume. Inner opercular paleae of various shapes, giving the appearance of two rows arranged in two concentric rows. Middle paleae strongly geniculate with excavated blades and smooth margins, pointing outward; innermost paleae strongly geniculate, with short concave blades and smooth margins, directed inward. Nuchal spines, when present, as three to six pairs of straight spines. Compound (branching) tentacular filaments

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arranged in series of rows; buccal flaps absent. Palps similar or shorter than operculum. Conspicuous median organ at the dorsal junction of the opercular lobes in some species and small or absent in others, with eyespots on its lateral margins (in the species examined). Neuropodia of segment 1 with one pair of conical cirri and capillary chaetae. One triangular-shaped lobe ventrally on both sides of the building organ. Thoracic branchiae present. Three parathoracic segments. Parathoracic notochaetae lanceolate and capillaries alternating; neurochaetae similar in shape but smaller. Abdominal branchiae present on most abdominal segments, missing from posteriormost in some species. Tetreres Caullery, 1913 Type species: Hermella varians Treadwell, 1901 Twelve species from the Atlantic, Pacific, and Southern oceans (Kirtley 1994, Hutchings et al. 2012). Some species inhabit a broad bathymetric range (Kirkegaard 1996) but also found at 9 to 45 m in the Java Sea. Diagnosis: Operculum longer than wide with lobes partially fused to each other (with deep indentation on ventral margin) and distal disc perpendicular to longitudinal axis, with large conical papillae around its perimeter. Outer paleae arranged in semicircles, straight, with flat blades and smooth lateral and distal margins. Inner paleae few in number, arranged in a single short row on ventral side of operculum, with straight, flattened blades. One pair of large nuchal hooks with broadened shafts; without limbations or enlarged shaft. Palps deeply grooved, longer than operculum. Tentacular filaments arranged in single rows. Buccal flaps absent. Small median organ at the dorsal junction of the lobes present. Neuropodia of segment 1 with one cirrus on each side of building organ; capillary neurochaetae present. Four long, tapering lateral lobes on segment 2. Thoracic branchiae absent. Four parathoracic segments. Parathoracic notochaetae lanceolate and capillaries alternating, similar in shape but smaller in neuropodia. Abdominal branchiae present, diminishing in size posteriorly.

Acknowledgments We thank H. Paxton for her inestimable help with German translations and interpretations of the potential “heart body” in sabellariids. Also thanks to B. Pernet, and R.R. Strathmann in addition to the Biological Bulletin for allowing the reproduction of larvae micrographs. We are grateful to L. Faroni-Perez who thoughtfully reviewed the manuscript and provided very useful and precise comments and suggestions for its improvement.

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Mörch, O.A.L. (1863): Revisio critica Serpulidarum. Et Bidrag til Rørormenes Naturhistorie. Naturhistorisk Tidsskrift, København, Series 3, 1: 347–470. Morgado, E. & Tanaka, M. (2001): The macrofauna associated with the bryozoan (Walters) in southern Brazil. Scientia Marina 65: 173–181. Multer, H.G. & Milliman, J.D. (1967): Geologic aspects of sabellarian reefs, southeastern Florida. Bulletin of Marine Science 17: 257–267. Nishi, E. & Kirtley, D.W. (1999): Three new species of Sabellariidae (Polychaeta) from Japan. Natural History Research 5: 93–105. Nishi, E. & Núñez, J. (1999): A new species of shallow water Sabellariidae (Annelida: Polychaeta) from Madeira Island, Portugal, and Canary Islands, Spain. Arquipelago Boletim da Universidade dos Acores Ciencias Biologicas e Marinhas 17a: 37–42. Nishi, E., Kato, T. & Hayashi, I. (2004): Sabellaria tottoriensis n. sp. (Annelida: Polychaeta: Sabellariidae) from shallow water off Tottori, the Sea of Japan. Zoological Science (Tokyo) 21: 211–217. Nishi, E., Bailey-Brock, J.H., Souza dos Santos, A., Tachikawa, H. & Kupriyanova, E. (2010): Sabellaria isumiensis n. sp. (Annelida: Polychaeta: Sabellariidae) from shallow waters off Onjuku, Boso Peninsula, Japan, and re-descriptions of three Indo-West Pacific sabellariid species. Zootaxa 2680: 1–25. Nishi, E., Matsuo, K., Capa, M., Tomioka, S., Kajihara, H., Kupriyanova, E.K., & Polgar, G. (2015): Sabellaria jeramae, a new species (Annelida: Polychaeta: Sabellariidae) from the shallow waters of Malaysia, with a note on the ecological traits of reefs. Zootaxa 4052(5): 555–568. Nunes, F., Van Wormhoudt, A., Perez-Faroni, L., Fournier, J. (2016): Phy­logeography of the reef-building polychaetes of the genus Phrag­matopoma in the Western Atlantic region. Journal of Biogeography 44: 1612–1625. https://doi.org/10.1111/ jbi.12938. Orrhage, L. (1978): On the structure and evolution of the anterior end of the Sabellariidae (Polychaeta Sedentaria). With some remarks on the general organisation of the polychaete brain. Zoologische Jahrbücher, Anatomie und Ontogenie der Tiere 100: 343–374. Orrhage, L. & Eibye-Jacobsen, D. (1998): On the anatomy of the central nervous system of Phyllodocidae (Polychaeta) and the phylogeny of phyllodocid genera: a new alternative. Acta Zoologica (Stockholm, Sweden) 79: 215–234. Orrhage, L. & Müller, M.C.M. (2005): Morphology of the nervous system of Polychaeta (Annelida). In: Bartolomaeus, T. & Purschke, G., (eds.). Morphology, Molecules, Evolution and Phylogeny in Polychaeta and Related Taxa. Hydrobiologia, 535–536: 79–111. Pasteels, J.J. (1965a): Étude au microscope électronique de la reaction corticale. II. La réaction corticale de l’oeuf vierge de Sabellaria alveolata. Journal of Embryological Experimental Morphology 13: 327–339. Pasteels, J.J. (1965b): Aspects structuraux de la fécondation vus au microscope électronique. Archives of Biology 76: 463–509. Pawlik, J.R. (1986): Chemical induction of larval settlement and metamorphosis in the reef-building tube worm Phragmatopoma californica (Polychaeta: Sabellariidae). Marine Biology 91: 59–68.

Pawlik, J.R. (1988a): Larval settlement and metamorphosis of two gregarious sabellariid polychaetes Sabellaria alveolata compared with Phragmatopoma californica. Journal of the Marine Biological Association of the United Kingdom 68: 101–124. Pawlik, J.R. (1988b): Larval settlement and metamorphosis of Sabellariid Polychaetes, with special reference to Phragmatopoma lapidosa, a reef-building species, and Sabellaria floridensis, a non-gregarious species. Bulletin of Marine Science 43: 41–60. Pawlik, J.R. (1992): Chemical ecology of the settlement of benthic marine invertebrates. Oceanography and Marine Biology—An Annual Review 30: 273–335. Pawlik, J.R. & Chia, F.S. (1991): Larval settlement of Sabellaria cementarium Moore, and comparisons with other species of sabellariid polychaetes. Canadian Journal of Zoology 69: 765–770. Pawlik, J.R. & Faulkner, D.J. (1988): The gregarious settlement of Sabellariid polychaetes: new perspectives on chemical cues. In: Thompson, M.F., Rachakonda, S. & Rachakonda, N, (eds.). Marine biodeterioration: advanced techniques applicable to the Indian Ocean: New Dehli, Bombay & Calcutta. IBH Publishing Co., Oxford: 475–487. Pawlik, J.R. & Mense, D.J. (1994): Larval transport, food limitation, ontogenetic plasticity, and the recruitment of sabellariid polychaetes. In: Wilson, Jr., W.H., Stricker, S.A. & Shinn, G.L. (eds.). Reproduction and Development of Marine Invertebrates. Johns Hopkins University Press, Baltimore: 275–286. Pérez, C.D., Vila-Nova, D. & Santos, A.M. (2005): Associated community with the zoanthid Palythoa caribaeorum (Duchassaing and Michelotti, 1860) (Cnidaria, Anthozoa) from littoral of Pernambuco, Brazil. Hydrobiologia 548: 207–215. Pernet, B. & Strathmann, R.R. (2011): Opposed ciliary bands in the feeding larvae of sabellariid annelids. Biological Bulletin 220: 186–198. Philippi R.A. (1887): Die Tertiären und Quartären Versteinerungen Chiles. FA Broekhaus, Leipzig. Pohler, S.M.L. (2004): The sabellariid worm colonies of Suva Lagoon, Fiji. South Pacific, Journal Natural History 22: 36–42. Purschke, G. (1997): Ultrastructure of nuchal organs in polychaetes (Annelida)—new results and review. Acta Zoologica (Stockholm) 78: 123–143. Purschke, G. & Tzetlin, A.B. (1996): Dorsolateral ciliary folds in the polychaete foregut: structure, prevalence and phylogenetic significance. Acta Zoologica (Stockholm) 77: 33–49. Quatrefages, A. (1848): Études sur les types inferieurs de l’embranchements des Annéles. Mémoire sur la famille des Hermelliens (Hermellea nob.). Annales des Sciences Naturelles Paris, Series 3, 10: 5–58. Read, G.; Fauchald, K. (Ed.) (2019): World Polychaeta database. Sabellariidae Johnston, 1865. Accessed through: World Register of Marine Species at: http://www.marinespecies.org/ aphia.php?p=taxdetails&id=979 on 2019-08-30. Réaumur, R. (1711): Des différentes manières dont plusieurs espèces d’animaux de mer s’attachent au sable, aux pierres, et les uns aux autres. Mémoires de l’Academie des Sciences, Paris 1711, 1–130. Render, J.A. (1983): The second polar lobe of the Sabellaria cementarium embryo plays an inhibitory role in apical tuft formation. Wilhelm Roux’s Archives of Developmental Biology, 192: 120–129.



Riisgård, H.U. & Nielsen, C. (2006): Feeding mechanism of the polychaete Sabellaria alveolata: comment on Dubois et al. (2005). Marine Ecology Progress Series 328: 295–305. Rouse, G.W. (2001): Sabellariidae Johnston, 1865. In: Rouse, G.W. & Pleijel, F. Polychaetes. Oxford University Press, Oxford: 189–192. Rouse, G.W. & Fauchald, K. (1997): Cladistics and polychaetes. Zoologica Scripta 26: 139–204. Rousset, V., Rouse, G.W., Siddall, M.E., Tillier, A. & Pleijel, F. (2004): The phylogenetic position of Siboglinidae (Annelida) inferred from 18S rRNA, 28S rRNA and morphological data. Cladistics, 20: 518–533. Santos A.S., Riul P., Brasil A. & Christoffersen M. (2010): Encrusting Sabellariidae (Annelida: Polychaeta) in rhodolith beds, with description of a new species of Sabellaria from Brazilian coast. Journal of the Marine Biological Association of the United Kingdom 91: 425–438. Savigny, J.C. (1822): Système des annélides, principalement de celles des côtes de l’Égypte et de la Syrie, offrant les caractères tant distinctifs que naturels des Ordres, Familles et Genres, avec la Description des Espèces. Description.de l’Egypte. Histoire Naturelle, Paris 1: 1–128. Schmarda, L.K. (1861): Neue Turbellarien, Rotatorien und Anneliden beobachtet und gesammelt auf einer Reise um die Erde 1853 bis 1857. Erster Band (zweite halfte). Wilhelm Engelmann: Leipzig 164 pp. Sepúlveda, R.D., Moreno, R.A. & Carrasco, F.D. (2003): Macroinvertebrate diversity associated to reefs of Phragmatopoma moerchi Kinberg, 1867 (Polychaeta: Sabellariidae) in the intertidal rocky shore at Cocholgue, Chile. Gayana 67: 45–54. Shao, H., Bachus, K.N. & Stewart, R.J.(2009): A water-borne adhesive modeled after the sandcastle glue of P. californica. Macromolecular Bioscience 9: 464–471. Shao, H. & Stewart, R.J. (2010): Biomimetic underwater adhesives with environmentally triggered setting mechanisms. Advanced Materials 22: 729–733. Sloan, N.J.B. & Irlandi, E.A. (2008): Burial tolerances of reef-building Sabellariid worms from the east coast of Florida. Estuarine, Coastal and Shelf Science 77: 337–344. Smith, P.R. (1986): Development of the blood vascular system in Sabellaria cementarium (Annelida, Polychaeta). An ultrastructural investigation. Zoomorphology 106:67–74. Smith, P.R. & Chia, F.S. (1985): Larval development and metamorphosis of Sabellaria cementarium Moore, 1906 (Polychaeta: Sabellariidae). Canadian Journal of Zoology 63: 1037–1049. Smith, P.R., Ruppert, E.E. (1988): Nephridia. In: Westheide, W. & Hermans, C.O. (eds.). The ultrastructure of Polychaeta. Microfauna Marina 4: 231–262. Speksnijder, J.E. & Dohmen, M.R. (1983): Local surface modulation correlated with ooplasmic segregation in eggs of Sabellaria alveolata (Annelida, Polychaeta). Roux’s Archives Developmental of Biology 192: 248–255. Scheltema, R.S. (1986): On dispersal and planktonic larvae of benthic invertebrates: an eclectic overview and summary of problems. Bulletin of Marine Science 39: 290–322. Storch, V. (1988): Integument. In: Westheide, W. & Hermans, C.O. (eds.). The Ultrastructure of Polychaeta. Microfauna Marina 4: 13–36.

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Strømgren, T. (1971): A new species of Phalacrostemma (Annelida Polychaeta: Sabellariidae) from the Norwegian west coast. Kongelige Norske Videnskabers Selskabs Skrifter 14: 1–4. Treadwell, A.L. (1901): The Polychaetous annelids of Puerto Rico. Bulletin of the United States Fish Commission 20: 181–210. Treadwell, A.L. (1926): Contributions to the biology of the Philippine Archipelago and adjacent regions. Additions to the polychaetous annelids collected by the United States Fisheries steamer ‘Albatross’, 1907–1910, including one new genus and three new species. Bulletin of the United States National Museum 100: 183–193. Uebelacker, J.M. (1984): Family Sabellariidae. In: Uebelacker, J.M. & Johnson, P.G. (eds.). Taxonomic Guide to the Polychaetes of the Northern Gulf of Mexico. Barry A. Vittor & Associates, Inc., Volume 7, Chapter 49: 1–49. Verrill, A.E. (1873): Report upon the invertebrate animals of Vineyard Sound and the adjacent waters, with an account of the physical characters of the region. Report of the United States Commission for Fisheries 1871–72: 295–778. Vovelle, J. (1965): Le tube de Sabellaria alveolata (L.) annélide polychète Hermellidae et son ciment étude ecologique, experimentale, histologique et histochimique. Archives de Zoologie Expérimentale et Générale 106: 1–187. Voronezhskaya, E.E., Tsitrin, E.B. & Nezlin, L.P. (2003): Neuronal development in larval polychaete Phyllodoce maculata (Phyllodocidae). Journal of Comparative Neurology 455: 299–309. Wang, C.S., Svendsen, K.K. & Stewart, R.J. (2010): Morphology of the adhesive system in the sandcastle worm, Phragmatopoma californica. In: Byern J. & Grunwald I., (eds.). Biological Adhesive Systems: From Nature to Technical and Medical Application. Springer, Vienna: 169–179. Wilson, D.P. (1929): The larvae of the British sabellarians. Journal of the Marine Biological Association of the United Kingdom 16: 221–268. Wilson, D.P. (1970a): Additional observations on larval growth and settlement of Sabellaria alveolata. Journal of the Marine Biological Association of the United Kingdom 50: 1–31. Wilson, D.P. (1970b): The larvae of Sabellaria spinulosa and their settlement behaviour. Journal of the Marine Biological Association of the United Kingdom 50: 33–52. Wilson, D.P. (1971): Sabellaria colonies at Duckpool, North Cornwall, 1961–1970. Journal of the Marine Biological Association of the United Kingdom 51: 509–580. Wilson, D.P. (1977): The distribution, development and settlement of the sabellarian polychaete Lygdamis muratus (Allen) near Plymouth. Journal of the Marine Biological Association of the United Kingdom 57: 761–792. Wilson, W.H. (1991): Sexual reproductive modes in polychaetes: classification and diversity. Bulletin of Marine Science 48: 500–516. Winslow, B.D., Shao, H., Stewart, R.J. & Tresco, P.A. (2010): Biocompatibility of adhesive complex coacervates modeled after the sandcastle glue of Phragmatopoma californica for craniofacial reconstruction. Biomaterials 31: 9373–9381. Zhao H, Sun C, Stewart RJ, and Waite JH (2005): Cement proteins of the tube-building polychaete Phragmatopoma californica. Journal of Biological Chemistry 280: 42938–42944.

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María Capa, Adriana Giangrande, João M. de M. Nogueira and María Ana Tovar-Hernández

7.4.6 Sabellidae Latreille, 1825 Introduction Sabellidae is one of the most diverse and ubiquitous polychaete families with more than 400 nominal species described to date, classified in 40 genera. They are found from fresh waters to full marine conditions, and from intertidal to abyssal depths all over the world. Sabellids inhabit the tubes they build with secreted mucus and attached mud or sand particles. Glomer­ ula piloseta (Perkins, 1991) represents an exception as it builds a calcareous tube. They are able to move inside this tube, extending their radiolar crown out of it for fulfilling their feeding needs, or withdraw into it for protection. The radiolar crown is a residue of the prostomium after its reduction during metamorphosis (Wilson 1936, Schroeder and Hermans 1975, Fitzhugh 1989). It is formed by numerous feathery-like appendages, responsible for these animals being commonly known as feather duster worms. The radiolar crown is vascularized, allowing gas exchange with the environment, and is also provided with cilia to capture particles from the water column for feeding and tube building. Sabellids have biramous parapodia where each ramus bears either capillary chaetae or uncini. The body is divided into two regions: the thorax and the abdomen. Thoracic chaetigers bear capillary chaetae on notopodia and uncini on neuropodia, whereas abdominal chaetigers show the opposite arrangement, with uncini present on the notopodia and capillary chaetae on the neuropodia. Sabellids generally withdraw in their tubes when disturbed, but in some small species inhabiting unstable environments (intertidal habitats, fluctuating estuarine conditions, or under strong currents where tubes are detached from the substrate), the worms are able to leave the tubes and build a new one fairly quickly (e.g., Bonar 1972). Some larger species, with slower tube-building processes, can live permanently in the same tube (Fitzsimons 1965) but still have the capability of rebuilding a new tube if excessively agitated or removed from the old one (Nicol

1931, Fitzsimons 1965, Licciano et  al. 2012, Murray et  al. 2013, personal observation). Some species are capable of boring into the calcium carbonate of shells and are considered as parasites of marine and freshwater mollusks or active bioeroders of coral reefs (e.g., Jones 1974, Chughtai and Knight-Jones 1988, Culver et al. 1997, Fitzhugh and Rouse 1999, Goldberg 2013). Several species have been unintentionally translocated on ships hulls, in ballast water, or associated with mariculture species cultivated outside the natural distribution range, generating in some cases ecological and economic negative impacts in the arrival localities (e.g., Clapin and Evans 1995, Patti and Gambi 2001, Tovar-Hernández et al. 2009a,b, Read et al. 2011, Capa et al. 2013a). There have been several attempts of generating phylogenetic hypothesis about their relationships with other polychaetes and it is currently accepted that annelids with a radiolar crown and chaetal inversion are closely related (Kupriyanova and Rouse 2008, Capa et al. 2011a). It is mostly accepted that Sabellidae does not include the previously considered subfamily Fabriciinae (Kupriyanova and Rouse 2008, Capa et al. 2011a), and some groups of genera form well-­established clades (e.g., Fitzhugh 1989, 2003, Rouse and Fitzhugh 1994, Fitzhugh and Rouse 1999, Capa 2007, 2008, Capa et al. 2011a). However, further effort is still required to resolve the sabellid phylogeny. Because of the lack of hard body parts or solid tubes, sabellids have not left fossil records besides a few exceptions. Only members attributed to the genus ­Glomerula Nielsen, 1931, with calcium carbonate tubes, have been found from the Hettangian (approximately 200 million years ago) to the recent, most common, and geographically widespread from the Upper Toarcian until the Eocene (Kočí 2012). In fact, calcification in Sabellidae had apparently originated in the early Mesozoic, and tube ultrastructure has remained unchanged since then (Vinn et al. 2008).

Morphology External morphology Sabellids are tube-dwelling annelids that project an often colorful radiolar crown (= branchial crown) (Fig. 7.4.6.1 A–D)

▸ Fig. 7.4.6.1: General morphology of members of Sabellidae. A, Acromegalomma sp. from Australia, within its tube, embedded with sand

grains, showing two distal compound radiolar eyes sticking out of the radiolar crown (arrow). B, Parasabella sp. from Australia, dorsal view with opened radiolar crown showing the radioles (arrow) and pinnules (asterisk). C, Bispira porifera from Australia, dorsal view, showing the characteristic spongy cushion outgrowth in anterior thoracic chaetigers. D, Notaulax sp. from Australia, lateral view, with groups of orange radiolar eyespots (arrow). E, Amphiglena nishi from Japan, ventral view (arrow points to faecal groove), showing different body regions. F, Desdemona ornata from Australia, dorsal view. G, Desdemona aniara from Australia, lateral and ventral views, respectively. H, Caobangia sp. from Vietnam. em, embryos; rc, radiolar crown; th, thorax; ab, abdomen. A–D, live specimens; E, F, SEM G, H, light microscopy, preserved material. Images: A, B, D, by A. Semevov; C, E, and H, by M. Capa; F, G, by E. Wong.



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out of their tubes (Fig. 7.4.6.1 A). Sabella ­spallanzanii (Gmelin, 1791) can reach up to 40 cm in length (KnightJones and Perkins 1998), but species of Amphicorina Claparède, 1864, Amphiglena Claparède, 1864 (Fig. 7.4.6.1 E), or Desdemona Banse, 1957 (Fig. 7.4.6.1 F, G), do not grow more than 4 mm (Hutchings and Murray 1984, Giangrande et al. 1999, Capa and Rouse 2007). The length of the tubes often reaches twice the length of the worms. In members of Sabellidae, the prostomium and the peristomium are fused and highly modified because of the presence of the characteristic radiolar crown, which is homologous to the palps of other polychaetes (Orrhage 1980). The radiolar crown is provided with a base formed by two generally semicircular radiolar lobes (surrounding the mouth and fused dorsally) and distal anterior projections known as the radioles (Figs. 7.4.6.1 A–H and 7.4.6.2 A–D). The radioles bear two longitudinal rows of small ciliated pinnules on their inner edges (Figs. 7.4.6.1 A, B and 7.4.6.2 A–D). Moreover, in members of Branchiomma Kölliker, 1858, radioles also bear paired appendages along the outer edge, known as stylodes (Fig. 7.4.6.3 D), an autapomorphy for the genus. The r­ adiolar crown, similarly present in Fabriciidae Rioja, 1923, and Serpulidae Rafinesque, 1818, shows some differences on its internal morphology among members of these three families (Fitzhugh 1989, 1991, Rouse and Fitzhugh 1994, Fitzhugh and Rouse 1999, Cochrane 2003, Capa et al. 2011b). The

ventral edge of the radiolar lobes can grow, resulting in spiral crowns as in some members of Bispira Krøyer, 1856; Sabella Linnaeus, 1767; and Sabellastarte Krøyer, 1856 (Knight-Jones and Perkins 1998, Knight-Jones and Mackie 2003, Capa 2008, Capa et al. 2010; Fig. 7.4.6.3 A). Some sabellids have a membrane joining the radioles at their bases, named as the basal membrane (= radiolar membrane or palmate membrane) (Figs. 7.4.6.3 B and 7.4.6.4 A). The condition of its maximum development is shown in Myxicola Renier in Meneghini, 1847. The basal membrane can continue as a narrow sheath of tissue on both lateral sides of the radioles, the radiolar flanges (Figs. 7.4.6.3 C and 7.4.6.4 E, F), or as dorsal and/ or ventral extensions at the base of crown, in between radiolar lobes, the dorsal and ventral radiolar basal flanges (Fig. 7.4.6.4 B) (Perkins 1984, Capa 2008, Capa et al. 2011b). External margins of radioles can be quadrangular (Fig. 7.4.6.4 C) or rounded (Fig. 7.4.6.4 D) (e.g., Fitzhugh 1989; Capa 2007). Radiolar rachis is generally smooth, but in some species of Branchiomma, such as Branchiomma nigromaculatum (Baird 1865) and, at least, Brazilian specimens of Branchiomma ­luctuosum, it has a segmented appearance because of regular obtuse indentations (Nogueira et  al. 2006, Tovar-Hernández and Knight-Jones 2006). Several other structures associated with the radiolar crown are the dorsal and ventral lips (Fig. 7.4.6.2 B–D),

Fig. 7.4.6.2: Opened radiolar crowns showing associated structures. A, Branchiomma sp. from Australia with naturally opened radiolar crown; B, details of the radiolar crown’s internal structures, including radiolar lobes, dorsal lips, and dorsal radiolar appendages (same specimen); C, Bispira porifera from Australia, base of radioles, each with a double longitudinal row of pinnules, dorsal lips, and radiolar appendages; D, opened radiolar crown and internal structures, Notaulax sp. from Australia. Abbreviations: dl, dorsal lip; dra, dorsal radiolar appendages; mo, mouth; rl, radiolar lobe. A–D, live specimens. Images: A, B, A. Semenov; C, D, M. Capa.



the parallel lamellae and ventral sacs (Fig. 7.4.6.3 E–G), the dorsal and ventral radiolar appendages, and the pinnular appendages of the dorsal lips. The dorsal lips are ciliated lappets on the dorsal edge of the mouth, in some cases fused to a modified radiole, called dorsal ­radiolar appendage. Dorsal lips are considered as extensions of the dorsal margins of the radiolar lobes (Banse 1956, 1957, Fitzhugh 1989; Figs. 7.4.6.2 B–D and 7.4.6.3 H). The ventral lips are also lappets that extend from the ventral margin of the radiolar lobes toward the dorsal lips (Nicol 1931, Perkins 1984, Fitzhugh 1989) except Myxicola, in which dorsal lips are surrounded by the ventral lips (Fitzhugh 2003). Many sabellids present ventral extensions of the ventral lips, the parallel lamellae, continuing toward the collar ventral incision and terminating by a pair of ventral sacs, where sediment for tube building is stored (Nicol 1931, Perkins 1984, Fitzhugh 1989). Ventral radiolar appendages are present in several genera, such as Amphicorina, Chone Krøyer, 1856; Euchone Malmgren, 1866; and Jasmineira Langerhans, 1880; these structures are considered as reduced radioles (Fitzhugh 1989, Tovar-Hernández 2008, Capa et al. 2011a, b). A remarkable organ found in some Acromegalomma Gil and Nishi, 2017 species is the caruncle, a prostomial projection placed dorsally above the mouth, between the dorsal lips, supported with vacuolated skeletal cells and innervated directly from the brain (Tovar-Hernández and Salazar-Vallejo 2008, Tovar-Hernández and Carrera-Parra 2011 Capa and Murray 2015; Fig. 7.4.6.4 G, H). Sabellids have a two-ring peristomium. The anterior ring and its associated ventral lobe can be reduced in some taxa (Fitzhugh 1989). The posterior ring is often provided with a membranous collar with a variable degree of development (Figs. 7.4.6.3 G and 7.4.6.4 B, G), but the collar is absent in some taxa (Fig. 7.4.6.3 I). The dorsal margins of this collar can be widely separated (Fig. 7.4.6.3 H), fused to the faecal groove (Fig. 7.4.6.4 B), or form a continuous structure dorsally (Fig. 7.4.6.4 A, B). Collar dorsal margins can be as long as the rest of the collar (Fig. 7.4.6.4 B) or be developed as dorsal lappets (Fig. 7.4.6.4 C), and they can form pockets at either side of the faecal groove (Fig. 7.4.6.4 C, G). Midventral and laterodorsal incisions of the posterior peristomial ring collar may be present in some species; the presence of the former one creates more or less developed ventral lappets (e.g., Fig. 7.4.6.3 E, F). The body is divided into two regions. The thorax, consisting typically of eight, number of chaetigers, and the abdomen, with a variable number of segments. There are, however, some species showing a different pattern, being the most remarkable exception Anamobaea Krøyer, 1856, with remarkably long thorax consisting of 32 to 74

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segments. In turn, shorter thoracic regions can be found in species with asexual reproduction, as explained below. The number of abdominal chaetigers generally varies between and within species except for some species of Amphicorina, Desdemona, and Terebrasabella Fitzhugh and Rouse, 1999, with fixed number of segments. The boundary between thorax and abdomen is clearly distinct by the chaetal inversion and the shift of the position of the faecal groove. The chaetal inversion refers to the condition where thoracic notopodia have capillary chaetae (long slender bristles gradually tapering to a fine tip) and neuropodia bear uncini (stout-handled simple chaetae generally curved and distally toothed), but the opposite condition is found in abdominal segments, which bear notopodial uncini and neuropodial capillary chaetae (Fig. 7.4.6.5 A). The inversion of the faecal groove is the deviation of this ciliated path from the ventral midline in the abdomen, running along the side between the first abdominal neuropodia and the last thoracic notopodia and continuing along the dorsal midline along the thorax (Figs. 7.4.6.1 E and 7.4.6.5 A). Both chaetal and faecal groove inversions are features shared by all members of Sabellidae, Fabriciidae, and Serpulidae and unique among annelids (Kieselbach and Hausen 2008, Capa et al. 2011a). Ventral shields are cushions composed of a glandular columnar epithelium present midventrally (Fig. 7.4.6.5 A, C, E) (Evenkamp 1931, Tovar-Hernández and Sosa-Rodríguez 2006). In each thoracic chaetiger, shields are entire, whereas in abdominal segments, shields are longitudinal divided in two by the faecal groove. As mentioned previously, sabellids have biramous parapodia, except the first chaetiger that only bears notopodial chaetae known as the collar chaetae. Rami-bearing capillary chaetae show a variety of shapes, such as well-developed conical lobes, transverse ridges, or inconspicuous rami, where chaetae seem to protrude directly from body wall (Figs. 7.4.6.5 B, D and 6 A, C–F). Rami-bearing uncini are more or less conspicuous transverse ridges, often referred to as tori, and show more uniformity between taxa and body regions. Thoracic and abdominal capillary chaetal fascicles generally present two groups of chaetae, originated from independent formation sites (Kryvi 1989, Kieselbach and Hausen 2008; Fig. 7.4.6.6 A, C–F). In some cases, one of the groups may be absent. Both groups may show similar or different chaetal morphologies (Fitzhugh 1989, Capa et al. 2011a). In the abdominal region, the chaetae are generally arranged in transverse rows (anterior and posterior) protruding from conical tori or ridges (Fig. 7.4.6.6 F). Exceptions are the Branchiomma–Sabellastarte clade (Capa 2008), with well-developed conical neuropodia with chaetae of the anterior group in a C-shape to spiral arrangement and

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Fig. 7.4.6.3: Radiolar crown and associated structures. A, Radiolar crown with right radiolar lobe spiraled, dorsal view, Sabella spallanzanii from Australia; B, basal membrane joining radioles (arrow), same species; C, radioles with radiolar flanges (white arrow) and paired compound eyes (black arrow), Bispira serrata from Australia; D, radioles with stylodes (white arrow) and paired compound eyes (black arrow), Branchiomma bairdi from Australia; E, base of radiolar crown with incipient growing radioles (white arrow), ventral sacs, and collar ventral lappets, B. serrata from Australia; F, detail of base of radiolar crown, ventral view, showing ventral sacs, parallel lamellae, and folded collar ventral lappets, S. spallanzanii from Australia; G, base of radiolar crown and anterior thoracic segments, ventral view, showing persitomial collar, ventral sacs, and parallel lamellae, B. bairdi from Australia; H, same, dorsal view, with dorsal lips and dorsal radiolar appendages (white arrow); I, base of radiolar crown and anterior thoracic segments, ventral view, Myxicola infundibulum from Australia. Abbreviations: co, collar; pl, parallel lamellae; vs, ventral sacs; vl, ventral lappets. A–I, light microscopy. Images: A–I, by E. Wong.



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Fig. 7.4.6.4: Radiolar crown and caruncle. A, Radiolar crown with radioles joined by a well-developed basal membrane (arrow) and anterior chaetigers, dorsal view, Notaulax sp. from Australia; B, detail of base of radiolar crown showing dorsal radiolar flanges (arrow) and collar chaetae with oblique arrangement (black arrow), same specimen; C, junction of thorax and radiolar crown, showing well-developed dorsal margins of collar (arrow) and collar “pockets” (black arrow), Acromegalomma cf. acrophthalmos from Australia; D, radioles with rounded and smooth edges, Parasabella sp. from Australia; E, radiole with serrated radiolar flanges and compound eyes (arrow), Bispira serrata from Australia; F, radiole with serrated radiolar flanges, without eyes, Stylomma juani from Australia; G, anterior thoracic segments with detached radiolar crown, showing a caruncle (arrow), Acromegalomma sp. from Australia; H, details of caruncle with four transverse ciliated rows, same specimen. A–H, SEM. Images: A–H by M. Capa.

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Fig. 7.4.6.5: Thoracic and abdominal segments and pygidia. A, Posterior thoracic and anterior abdominal chaetigers, lateral view, showing the faecal groove running between body regions (arrow) and interramal eyespots (arrowhead), Branchiomma bairdi from Australia; B, abdominal parapodia, ventral view, Bispira porifera from Australia (arrowhead, interramal eyes); C, abdominal chaetigers with conspicuous ventral shields divided by the longitudinal faecal groove, Sabella spallanzanii from Australia; D, thoracic parapodia, Myxicola infundibulum from Australia, lateral view; E, posterior abdominal segments and pygidium, ventral view, Bispira serrata from Australia; F, posterior abdominal segments showing prepygidial depression and pygidium, dorsal view, Euchone limnicola from Australia; G, posterior abdominal segments showing with prepygidial depression and lateral wings, dorsal view, Euchone variabilis from Australia; H, posterior abdominal segments and pygidium provided with pygidial cirrus, ventral view, Jasmineira sp. from Australia. A–G, light microscopy (or stereomicroscopy); H, SEM. Images: A–G, E. Wong; H, M. Capa.

chaetae of posterior group enclosed in this arc (Fig. 7.4.6.5 A–C), and Myxicola with chaetae protruding directly from the body wall in irregular bundles (Fig. 7.4.6.5 D). Sabellid capillary chaetae, like those present in some other polychaetes, are not simple cylindrical or tapering

bristles. Instead, they show a midlength enlargement that narrows progressively toward the distal tip, sometimes resembling a thin arrow tip. They have commonly been referred to as winged or limbated capillary chaetae, although detailed studies showed that there is no such



limbation (Perkins 1984, Kryvi and Sørvig 1990, Hausen 2005). The emergent part of the chaetae is composed of a core with tightly packed, narrow rods or canals, continuation of the shaft from the proximal part of the chaetae, surrounded distally by a hood composed of a thin layer of loosely packed small tubules and a series of irregular lacunar spaces in between the shaft and the hood (Perkins 1984, Kryvi and Sørvig 1990, e.g., Fig. 7.4.6.7 B, C). Chaetal terminology, according to their shape and ultrastructure, has been reviewed (for details, see Perkins 1984, Fitzhugh 1989, Capa et al. 2011a). Chaetae with a hood visible on both sides of the shaft are termed broadly hooded (Perkins 1984, Fitzhugh 1989, KnightJones and Perkins 1998, Capa et  al. 2011a; Figs. 7.4.6.6 A, C–E and 7.4.6.7 C). Paleate chaetae resemble externally the broadly hooded chaetae, but they lack a shaft running inside the distal hood, generally observed under the compound microscope (Perkins 1984, Fitzhugh 1989, Knight-Jones and Perkins 1998, Capa et al. 2011a; Figs. 7.4.6.6 F and 7.4.6.7 A, B). Chaetae with a narrow hood only on one side of the shaft, perceptible under the compound microscope, have been defined as narrowly hooded (Figs. 7.4.6.6 A, C–F and 7.4.6.7 D, E). When the hood is observed on one side of the shaft but

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it is wide, such as those present the collar chaetae or Notaulax and Anamobaea or the inferior row in the Branchiomma–Sabellastarte clade, chaetae have been referred to as spinelike chaetae (Perkins 1984, KnightJones and Perkins 1998, Capa et  al. 2011a; Figs. 7.4.6.6 B and 7.4.6.7 D). Other subtypes of narrowly hooded chaetae, as defined by Perkins (1984) and Fitzhugh (1989), are referred to as elongate or modified, elongate narrowly hooded chaetae depending on their proportions, terms that not often have been followed in subsequent studies. Members of some genera, such as Amphicorina, Jasmineira, Chone, and Euchone, possess a tier of small chaetae parallel to the inferior thoracic chaetae, with a thin hood and termed bayonet chaetae (Fitzhugh 1989, Capa et al. 2011a; Fig. 7.4.6.6 C). Sabellids uncini (= hooks) are arranged side by side forming a transverse line embedded in the tori, with the dentate distal end directed anteriorly (Fig. 7.4.6.6 E). These uncini have a well-developed main fang (= rostrum) on their distal end, usually surmounted by a series of smaller teeth (= capitium) generally arranged in an imbricated pattern (Figs. 7.4.6.7 F–I and 7.4.6.8 A–C). The proximal end, known as handle (= shaft), varies greatly in length among taxa. It is secondarily reduced in Laonome

Fig. 7.4.6.6: Thoracic capillary chaetae. A, Superior thoracic chaetae elongate narrowly hooded, inferior broadly hooded, Parasabella sp. from Australia; B, inferior thoracic chaetae, spinelike (narrowly hooded), Bispira sp. from Australia; C, superior thoracic chaetae, elongate narrowly hooded, inferior broadly hooded, bayonet chaetae, Jasmineira sp. from Australia; D, superior thoracic chaetae elongate narrowly hooded, inferior broadly hooded, Parasabella sp. from Australia; E, broadly hooded chaetae, Amphiglena bondi from Australia; F, superior thoracic chaetae elongate narrowly hooded, inferior paleate, Notaulax sp. from Australia. Abbreviations: bc, bayonet chaetae; bhc, broadly hooded chaetae; enhc, elongate, narrowly hooded chaetae; nhc, narrowly hooded chaetae; pc, paleate chaetae. A–F, SEM. Images: M. Capa.

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Malmgren, 1866 (Fig. 7.4.6.7 H), and also in the abdominal uncini of Chone, Dialychone Claparède, 1870; Paradi­ alychone Tovar-Hernández, 2008; Euchone; and Myxicola (Fitzhugh 1989, Capa et  al. 2011a; Fig. 7.4.6.7 I). Handles can be straight or gently curved (acicular; Fig. 7.4.6.7 F) or bent in a Z shape (avicular; Fig. 7.4.6.7 G–I). They show a high variability in length among taxa, a feature that has frequently been used in genus and species diagnoses. The avicular uncini have an inflated area below the main fang referred to as a breast (e.g., Fitzhugh 1989). Breasts are well developed in most genera, usually swollen, distally rounded (Fig. 7.4.6.7 G, H), but they are reduced to a narrow swelling in species of Fabrisabella, Potamethus, and Jasmineira (Fitzhugh 1989; Fig. 7.4.6.7 F). Abdominal uncini of members of Amphicorina, Chone, Dialychone, Euchone, and Paradialychone have a square or rectangular breast (Fig. 7.4.6.7 I). Most genera have uncini with teeth above the main fang of nearly uniform size. In

Paradialychone, however, abdominal uncini have a large tooth above the main fang at midline, followed by a series of smaller teeth. The extension of dentition above the main fangs varies among and within genera (Figs. 7.4.6.7 F–I and 7.4.6.8 A–D, F, G) being the extreme condition found uncini on the posterior abdomen of Amph­ icorina, Dialychone, Euchone, and Paradialychone, in which teeth cover the entire length of main fang, giving it a rasp-shaped appearance (Tovar-Hernández 2008). In the region behind the teeth and directly opposite the main fang, thoracic uncini of some Chone, Dialychone, Paradialychone, Euchone, and Jasmineira species have a hyaline structure, which was referred to as a hood (Uebelacker 1984, Tovar-Hernández et  al. 2007, Tovar-Hernández 2008), probably composed of loosely packed tubules. A special type of uncini is present on the anterior chaetigers of members of Caobangia Giard, 1893 and Terebras­ abella, in which uncini are distally palmate (Jones 1974,

Fig. 7.4.6.7: Capillary chaetae and uncini. A, Paleate chaetae, first chaetiger, Laonome triangularis from Australia; B, paleate, midthoracic chaetae, Euchone limnicola from Australia (core absent in tip of the hood); C, broadly hooded, anterior abdominal chaetae, L. triangularis (core present in tip of hood, arrow); D, spinelike (narrowly hooded), inferior thoracic chaetae, Sabellastarte australiensis from Australia; E, elongated narrowly hooded, superior thoracic chaetae, same species; F, acicular uncini from thoracic segment with well-developed handles and narrow breasts, E. limnicola; G, avicular uncini from abdominal segment, with well-developed handles and breasts, S. australiensis; H, avicular uncini from thoracic segment lacking handles, L. triangularis; I, uncini with squared breasts and reduced handle, abdominal segment, Euchone variabilis from Australia. Abbreviations: br, breast; co, core; ha, handle; ho, hood; mf, main fang; te, distal teeth. A–I, Compound microscopy. Images: E. Wong.



Fitzhugh 1989, Fitzhugh and Rouse 1999, Murray and Rouse 2007; Fig. 7.4.6.8 E). Some genera bear another kind of thoracic uncinial chaetae, referred to as companion chaetae. Companion chaetae have a long shaft embedded in the tissue and a head with a distal hyaline structure (= hood) as in members of Amphiglena, Bispira, Eudistylia (Bush 1905), Notaulax (Tauber 1879), Perkinsiana (Knight-Jones 1983), Potaspina Hartman, 1969, Pseudobranchiomma Jones 1962, and Sabella (Fig. 7.4.6.8 F, G), or a mucro, as in Paras­ abella Bush, 1905; Fig. 7.4.6.8 H]. Usually, companion chaetae form a row parallel to that of the thoracic uncini. The pygidium can be rounded, conical, bilobed, or resembling a rim around the anus (Figs. 7.4.6.1 F, G and 7.4.6.5 E–G), and in some Dialychone, Jasmineira, and

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Paradialychone species, it is provided with a pygidial cirrus (Tovar-­Hernández 2008; Fig. 7.4.6.5 H). Pygidial eyespots are frequently present (see below), especially in juveniles but also in adults of the species. The segments preceding the pygidium in some species of Euchone, Euchoneira Licciano, Giangrande and Gambi, 2009, Dialychone, Para­ dialychone, and Chone are flattened, ventrally forming a prepygidial depression (= anal depression) (Tovar-Hernández 2007, 2008; Fig. 7.4.6.5 F, G). Ventral patches of cilia on the peristomium is typical of Amphiglena (Fig. 7.4.6.1 E). Similar patches, but on the collar (= posterior peristomial ring), have been recorded in Laonome, Amphicorina, Paradialychone ecaudata (Moore, 1903), Dialychone trilineata (Tovar-Hernández, 2007), and Pseudobranchiomma schizogenica (Tovar-Hernández and

Fig. 7.4.6.8: Uncini and companion chaetae. A, Thoracic uncini with teeth different in size over main fang, Jasmineira sp. from Australia; B, thoracic uncini with similar sized teeth over main fang, Sabellastarte sp. from Australia; C, abdominal uncini with high number of small teeth covering most of length of main fang, Notaulax sp. from Australia; D, thoracic uncini, with teeth over main fang arranged in a single line, Laonome triangularis from Australia; E, thoracic uncini, distally palmate, Caobangia sp. from Vietnam; F, thoracic uncini and companion chaetae with roughly symmetrical, Notaulax sp. from Australia; G, thoracic uncini and companion chaetae with asymmetrical hoods, Acromegalomma sp. from Australia; H, companion chaetae with enlarged mucro and distal tip, Parasabella sp. from Australia. A–H, SEM. Images: M. Capa.

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Dean, 2014). Besides, in P. schizogenica, the thoracic and abdominal segments also have patches of typical cilia (kinocilia-type), distributed in pairs. Cilia may be of different kinds, and not all are necessarily sensory because some seem to have different functions such as to generate water currents inside tubes (Tovar-Hernández 2008, Tovar-Hernández and Dean 2014). Sabellidae holds the largest variation of type and arrangement of eyes of the Annelida. A great diversity is found among species, and several types of eyes can be found in a single individual because they can have radiolar, peristomial, segmental, and pygidial eyes. Radiolar eyes can be arranged in different positions along the radioles and appear as single ocelli (e.g., Parasabella), compound eyes consisting of numerous repetitive units or ocelli (e.g., Bispira, Branchiomma, Acromegalomma, and Pseudopotamilla; Krasne and Lawrence 1966, Verger-Bocquet 1992, Nilsson 1994, Bok and Nilsson 2016, Bok et al. 2016; Figs. 7.4.6.3 C–E and 7.4.6.9 B–F), or as an intermediate state between compound eyes and groups of individual ocelli, like in the case of Notaulax (Nilsson 1994, Bok et al. 2016; Fig. 7.4.6.9 A). Peristomial eyespots are present in small- or medium-sized sabellids and are considered to be cerebral eyes because of proximity to the brain (Purschke 2005, Purschke et  al. 2006). Members of Branchiomma, Pseudobranchiomma, Bispira, Sabella, Sabellastarte, Sabellomma (Nogueira, Fitzhugh and Rossi, 2010) and Stylomma Knight-Jones, 1997, bear simple, pigmented eyes between the notoand the neuropodia, called interramal eyes (Fitzhugh 1989, Capa 2008, Nogueira et al. 2010; Fig. 7.4.6.5 A, B). Some authors have also described interramal eyespots in Acromegalomma, Parasabella, and Perkinsiana species (Tovar-Hernández and Salazar-Vallejo 2006, Capa et  al. 2011a, Tovar-Hernández et  al. 2012), although further studies have to be undertaken to determine their ultrastructure and similarity with previous taxa. Pygidial eyes are present in some species, generally those sabellids with the ability of leaving the tube and building new ones ­(Purschke 2005). Out of the tube, they crawl with the pygidium in front and the radiolar crown folded up. Tube morphology. The structure of tubes can be very different and often is a useful feature in taxonomic identification, at least at genus level (Tovar-Hernández and Carrera-Parra 2011). Some species, such as S. ­spallanzanii and Sabellastarte spectabilis (Grube, 1878), combine mucus with feces to build a flexible and pergamentaceous tube (Giangrande et  al. 2014; Fig. 7.4.6.10 B). In Branchiomma and Bispira, a thin-walled tube is formed of mucus combined with sand sediment, giving a parchmentlike appearance (Fig. 7.4.6.10 C). In this case, the

opening of the tube can be closed when the worm withdraws. Species of Anamobaea, Notaulax, Perkinsiana, and Pseudopotamilla Bush, 1905, construct thick and horny mucous tubes, leathery in appearance, inside dead coral blocks or limestone (Chughtai and Knight-Jones 1988). Acromegalomma species build tubes by attaching gravel of different sizes, echinoderm spines, and shell fragments to a very thin layer of mucus, and sometimes the tube is completely buried in the soft substrate (Giangrande et  al. 2014; Fig. 7.4.6.10 E, F). Bispira serrata Capa, 2007, constructs tubes with an additional outer lining covering the muddy sediment (Fig. 7.4.6.10 D). Panousea sp. has translucent tubes, covered with scattered sand grains and shell fragments (Fig. 7.4.6.10 G). Soft-bottom species, such as Chone, Euchone, and Jasmineira, produce very flexible tubes formed by fine sand. In some cases, the worms can incorporate algae, shell fragments, detritus, ascidians, sponges, and hydrozoans within the tube (Fig. 7.4.6.10 A, F). The calcareous tubes of G. piloseta are circular in cross-section, coiled, plain, or with anterior end erect (Perkins 1991). Its wall is composed of subparallel lamellae of aragonitic, irregular spherulitic prisms in the inner layer, and spherulites in the outer layer, and calcified lamellae are separated by organic films of different thickness (Vinn et al. 2008). Tube microstructure is known in species of Anamobaea and Notaulax. The shape varies between an irregular or chaotic organic structure, to a regular structure with oriented fibers in a homogeneous matrix (Vinn et al. 2018). Anatomy Radiolar crown. The radiolar crown of the sabellids is supported by hyaline cartilage (Person and Mathews 1967, Tovar-Hernández and Sosa-Rodríguez 2006, Capa et  al. 2011a; Fig. 7.4.6.11 A), where chondrocytes and chondroblasts secrete a homogeneous matrix made of granules and fibers (Kryvi 1977). Some chondrocytes have a large vacuole and run along the radiolar lobes, radioles, pinnules, and in some cases the radiolar appendages in packed rows, which have been often referred to as the “skeleton” (Nicol 1931, Fitzharris 1976, Kryvi 1977, KnightJones 1983, Perkins 1984, Fitzhugh 1989, Capa et al. 2011a; Fig. 7.4.6.11 A, B). The presence of vacuolated cells suporting the radiolar crown is an autapomorphy of Sabellidae, being absent from fabriciids and serpulids (Hanson 1949, Orrhage 1980, Cole and Hall 2004, Capa et al. 2011b). Epidermis. Epidermal glandular regions in sabellids are extensive and may be diffuse or clearly limited as ventral glandular shields (Chughtai and Knight-Jones 1988, Fitzhugh 1989, Cochrane 2003, Tovar-Hernández 2007, 2008;



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Fig. 7.4.6.9: Radiolar eyes. A, Eyespots (arrow) on lateral edges of radioles, Notaulax sp. from Australia; B, paired compound eyes, Branchiomma sp. from Australia (arrow); C, paired compound eyes in another Branchiomma species from Australia; D. unpaired compound eyes (arrow), Pseudopotamilla sp. from Australia; E, distal compound eye, Acromegalomma phyllisae from Australia; F, same in Megalomma sp. from Australia. A–F, light microscopy. Images: A, B, D–F, M. Capa; C, R. Springthorpe.

Fig. 7.4.6.11 C, G). Staining worms with methyl green solution is useful to reveal epidermal glandular patterns (Fig. 7.4.6.12 A–C). In addition, Amphicorina, Chone, Des­ demona, Euchone, Euchoneira, Jasmineira, Myxicola, and Potamethus Chamberlin, 1919, have a pale transverse ridge located on the second chaetiger (glandular ridge on chaetiger 2) (Tovar-Hernández and Sosa-Rodríguez 2006, Tovar-­Hernández 2007; Fig. 7.4.6.12 B). Members of some

of these groups also present glandular ridges on posterior thoracic chaetigers (Tovar-Hernández 2007, 2008), as well as some species of Acromegalomma Johansson, 1925 (Tovar-Hernández and Carrera-Parra 2011). Musculature. Longitudinal muscles run along the length and usually form four discrete bands, two running ventrally and two larger ones running dorsally (Evenkamp 1931, Kryvi

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Fig. 7.4.6.10: Sabellid tubes. A, Tube covered with botryllid ascidians, Branchiomma bairdi from Mexico; B, Sabellastarte sp. from Australia, with a muddy tube; C, tube of Bispira manicata covered with fine sand; D, unusual tube of Bispira serrata, with a ringed and shiny outer lining; E, Acromegalomma sp. from Australia, with the remnants of shells attached to the sandy tube; F, tube of Acromegalomma pacifici from Panama; G, Panousea sp. from Panama, tube with leathery appearance. A–C, E, Live specimens light microscopy. Images: A, H. Bahena-Basave; B, M. Capa; C, E, C. Granich; D, E. Wong; F, G, M.A. Tovar-Hernández.

1971, Tzetlin and Filippova 2005, Tovar-Hernández 2007; Figs. 7.4.6.3 C and 7.4.6.12 D, E). The fibers making up these bands are arranged as two reverse helices with each coil tightly adjoining the previous one (Johansson 1925, Tzetlin and Filippova 2005; Fig. 7.4.6.3 C, F). Circular and other transverse fibers are poorly developed compared with the longitudinal muscles. Digestive System. The alimentary canal in Sabellidae is a straight, ciliated tube (Fig. 7.4.6.11 C, D). The foregut is simple and lacks a buccal organ (Tzetlin and Purschke 2005), the midgut consists of a stomach and an intestine (Dales 1962), and the posterior part is the rectum (Nicol 1931). The anterior portion of the gut is greatly constricted by the mesenteries and swells out between them into a series of almost spherical chambers, while the intestine is often distended with feces and bent from one side to another on each segment (Nicol 1931). The walls of the gut consist typically of four layers: an outer peritoneal layer, the lining of the body cavity, a muscular coat of circular and longitudinal fibers, a vascular sinus surrounding completely the gut from segment two to the posterior end of the body, and a ciliated and glandular epithelium resting on a well-­developed basal membrane (Nicol 1931).

Blood vascular system. The circulatory system is closed and lacks a heart (Hanson 1951). A ventral blood vessel runs from the second segment to the pygidium and connects to segmental ring vessels and the sinus around the gut. In the anterior end, this ventral vessel continues forward as two laterodorsal vessels and a periesophageal plexus. In the peristomium, the laterodorsal vessels join to form a median dorsal vessel, which opens into a transverse vessel just behind the cerebral ganglia. The latter also irrigates the radiolar crown and other prostomial structures (Ewer 1941, Hanson 1950, 1951). A pair of lateral vessels run along each side of the body in most sabellids examined from pygidium back to the second thoracic segment. The blood supply of the body wall and parapodia shows variation among taxa. In some species, it is derived from these lateral vessels in addition to the segmental ring vessels and in other just from the ring vessels. Branching patterns and distribution of these vessels also show variation within the family (Hanson 1950). The blood lacks blood cells, and it is green in most studied sabellids because of the presence of chlorocruorin (Hanson 1951, Imai and Yoshikawa 1985, de Hass et al. 1996). Other characteristic peristomial structures are the vascular loops (= vascular coil), which are circular cavities situated dorsolaterally on the peristomium and



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Fig. 7.4.6.11: Internal anatomy and histology. A, Cross-section at base of radioles, Laonome triangularis from Australia; B, cross-section at the base of radioles, Acromegalomma carunculatum from Mexico; C, abdomen in crosssection, Dialychone quebecensis from Canada (dorsal in upper side of picture); D, gut, D. quebecensis; E, detail of C showing ventral nerve chord (arrows), D. quebecensis; F, muscular package, D. quebecensis; G, glandular epithelium, Chone infundibuliformis from Greenland. Abbreviations: bv, blood vessel; dra, dorsal radiolar appendage; g, gut; pi, pinnules; vc, vacuolated cells (chondrocytes) supporting radioles in upright position; vl, collar ventral lappets, tissue dyed in blue is hyaline cartilage. A–G, Compound microscopy. Images: A, from Capa et al. (2011b); B, photo by TovarHernández; C–F, from Tovar-Hernández (2007); G, from Tovar-Hernández and SosaRodríguez (2006).

containing an S- or C-shaped vessel. In Sabellidae, they can be observed in Euchone analis (Krøyer 1856), some species of Jasmineira, and Fabrisabella Hartman, 1969 (Hartman 1969, Fitzhugh 2002, Tovar-Hernández 2008). Excretory system. A single pair of nephridia opens into the first segment (Goodrich 1945, Orrhage 1980, Schulze 2001, Bartolomaeus and Quast 2005). These are classified as metanephridia with podocytes (Goodrich 1945, Koechlin 1966, 1981, Orrhage 1980, Smith and Ruppert 1988, Bartolomaeus 1993). In Sabella pavonina Savigny, 1822, the nephridia are giant and fill almost all the coelomic space between the digestive tract and the body walls in the 8 to 11 anterior segments (Koechlin 1981). Nervous system. The brain is located in the peristomium because of the reduction of prostomium after metamorphosis (Schroeder and Hermans 1975). Like in most polychaetes, the brain of Sabellidae contains four transverse commissures. A pair of dorsal and ventral commissures ­ nterior circumesophageal root, while contact with an a another pair of commissures is connected to a posterior root of the ­connectives (Orrhage and Müller 2005). The

innervation of the radiolar crown is equivalent to that of the palps of other groups of polychaetes and is consequently considered to be homologous (Orrhage 1980, Orrhage and Müller 2005). The ventral nerve cord is double in the first four thoracic segments and single posteriorly (Nicol 1948a; Fig. 7.4.6.11 E). A single giant axon, up to 1 mm in diameter, is found in Myxicola infundibu­ lum Montagu, 1808 (Nicol and Young 1946, Nicol 1948b), whereas other sabellids possess two giant axons (Nicol 1948a, Hagiwara et al. 1964, Mellon et al. 1980). Sensory organs. The nuchal organs, paired ciliated sensory structures generally appearing as ciliated patches or bands, pits, or grooves on the head, have an anomalous position in sabellids, serpulids, and fabriciids. They have become internalized, probably because of the development of the radiolar crown and form a pair of pouches arising from the dorsal epithelium of the mouth cavity (Orrhage 1980, Purschke 1997, 2005). The diversity of eyes in members of this family can be found not only in their arrangement and external morphology but also at the cellular level. Radiolar eyes are fomed by unites or ocelli. These can bear one to four

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Fig. 7.4.6.12: Glandular patterns revealed using methyl green and internal anatomy. A, Glandular epithelium along the entire body of Paradialychone ecaudata from USA; B, glandular epithelium in collar and thoracic segments, Paradialychone paramollis from USA, glandular ridge as indicated by arrow; C, internal view of thorax, longitudinal section, Chone mollis from USA. D, Longitudinal muscles as indicated by arrows and septa, Chone aurantiaca from USA; E, details of longitudinal muscular fibers, C. aurantiaca. A–C, stained with methyl green; D, E, coated with gold A–E, light microscopy. Images: A–E, by M.A. Tovar-Hernández.

cells and the pattern is conserved among members of the same or related genera. Members of Pseudopotamilla, Eudistylia, and Schizobranchia have single-cell ocelli with a sensory membrane, and extracellular invagination forming a lens, and a pigment cup. Members of Acromeg­ alomma have two-cell ocelli with a lense cell on top of the sensory cell containing a pigment cup. The three-cell ocelli present in Branchiomma and Bispira have a pigment cup formed by two pigment cells surrounding an extracellular lens and a sensory cell. Members of Notaulax and Anamobaea present four-cell ocelli with three pigment cells and a single sensory cell (Nilsson 1994, Bok et al. 2016). Peristomial, segmental, and pygidial ocelli are composed of several pigment and a few sensory cells (rhabdomeric photoreceptor cells) forming a follicle-like epidermal invagination filled with a cuticular lens except for the cerebral (peristomial) eyes which are internalized. (Ermak and Eakin 1976, Dragesco-Kernéis 1980, Purschke 2005, Purschke et al.  2006). Statocysts, structures that act as gravity detectors, have been found in the peristomium of Amphicorina

(Rouse 1990, 1992, Yoshihara et al. 2012) and other small Sabellidae (Rouse 2001), but no ultrastructural studies have been conducted to date (Purschke 2005). There is no evidence of lateral organs, densely ciliated areas, pits, or small papillae present segmentally between the neuro- and the notopodia with sensory function in Sabellidae (Purschke and Hausen 2007). Other characteristic peristomial structures are the vascular loops (= vascular coil), which are circular cavities situated ­dorsolaterally on the peristomium and containing an S- or C-shaped vessel. In Sabellidae, they can be observed in Euchone analis (Krøyer 1856), some species of Jasmineira, and Fabrisabella Hartman, 1969 (Hartman 1969, Fitzhugh 2002, Tovar-Hernández 2008).

Reproduction and development Sabellidae is among the best-understood polychaete families in terms of reproduction (Rouse and Fitzhugh 1994, Giangrande 1997, Rouse et al. 2006). Sexual reproduction

7.4.6 Sabellidae Latreille, 1825 



 179

Tab. 7.4.6.1: Studies about reproductive issues in Sabellidae after Giangrande (1997). Species

Reference

Aracia heterobranchiata Nogueira, López, and Rossi, 2010 Aracia riwo (Rouse, 1996) Aracia sinaloae Tovar-Hernández, 2014 Amphiglena lindae Rouse and Gambi, 1997 Amphiglena mediterranea Leydig, 1851 Amphiglena nathae Rouse, 1994 Amphiglena pacifica Annenkova, 1934 Bispira brunnea Treadwell, 1917 Bispira volutacornis Montagu, 1804 Branchiomma bairdi McIntosh, 1885 Branchiomma luctuosum Grube, 1870 Euchone pallida Ehlers, 1912 Myxicola cf. sulcata Ehlers, 1912 Parasabella polarsterni Gambi, Patti, Micaletto and Giangrande, 2001 Perkinsiana antarctica Kinberg, 1866 Perkinsiana littoralis Hartman, 1967 Perkinsiana borsibrunoi Giangrande & Gambi, 1997 Perkinsiana milae Giangrande & Gambi, 1997 Pseudopotamilla reniformis Bruguière, 1789 Pseudobranchiomma schizogenica Tovar-Hernández & Dean, 2014 Sabella pavonina Savigny, 1822 Sabella spallanzanii Gmelin, 1791 Sabellastarte spectabilis Grube, 1878 Sabellastarte sp. Terebrasabella heterouncinata Fitzhugh and Rouse, 1999

Nogueira et al. 2004 Rouse 1996a Tovar-Hernández 2014 Rouse and Gambi (1998b) Rouse and Gambi (1998a,b) Rouse and Gambi (1998a,b) Rouse and Gambi (1998b) Tovar-Hernández and Pineda-Vera (2008), Dávila-Jiménez et al. (2017) Nash and Keegan (2003) Tovar-Hernández et al. (2011), Arias et al. (2013) Licciano et al. (2002), Mastrototaro et al. (2015) Gambi et al. (2001) Gambi et al. (2001) Gambi et al. (2001) Gambi and Patti (1999), Gambi et al. (2000) Gambi et al. (2000) Gambi et al. (2000) Gambi et al. (2000) Kolbasova et al. (2013) Tovar-Hernández and Dean (2014) Murray et al. (2011, 2013) Giangrande et al. (2000), Lee et al. (2018) Bybee et al. (2006a,b, 2007) Murray et al. (2013) Fitzhugh and Rouse (1999), Gray and Kaiser (2007a,b)

was reviewed by Rouse and Fitzhugh (1994), and compilations of reproductive features for several sabellid species were provided by McEuen et  al. (1983) and Giangrande (1997). Subsequently, many studies have been published about reproduction issues of 25 species (Tab.  7.4.6.1). Sabellids display a range of sexual reproductive modes, from broadcast spawning to ovoviviparity. They are mainly gonochoric, but some taxa show simultaneous or protandric hermaphroditism. Sabellids lack permanent gonads, but there are ­dispersed ovaries in which packets of germ cells, previtellogenic oocytes, and mature oocytes float in the coelom of mainly the abdominal region (Rouse and Fitzhugh 1994, Currie et  al. 2000, Bybee et  al. 2007), although Amphi­corina, Branchiomma, Chone, Dialy­ chone, Euchone, Jasmineira, and Paradialychone also contain gametes in the thorax (e.g., Rouse and Fitzhugh 1994, Nogueira  and Amaral 2000, Tovar-Hernández et  al. 2011). Primary gametes of both sexes seem to be derived from peritoneal cells. The maturation of gametes happens along the entire length of the coelom, and mature eggs and sperm are expelled through paired lateral gonoducts that extend from the coelom of each chaetiger and open at the neuropodia of the next posterior segment (e.g., Currie et al. 2000, Giangrande et al.

2000; Fig. 7.4.6.13 A, B). Simultaneous hermaphrodites can have eggs and sperm in the same segments, as in Caobangia, Sabellastarte magnifica, Branchiomma luc­ tuosum, Parasabella (Rouse and Fitzhugh 1994, Licciano et  al. 2002), and Branchiomma bairdi (Tovar-Hernández et  al. 2009a), or in different segments, as in some members of Amphiglena, Laonome, and Perkinsiana (Rouse and Fitzhugh 1994). Protandric hermaphroditism has been described only in Sabellastarte spectabilis (Bybee et al. 2006a) and is supposed to occur in Sabella spallanzanii (Giangrande and Petraroli 1994), which was found to be gonochoric in further investigations (Giangrande et al. 2000). Lastly, Laonome albicingillum Hsieh, 1995, is also simultaneous hermaphrodite (Hsieh 1995), but the distribution of its gametes is unknown. Oogenesis has been studied in Sabella spallanzanii (Giangrande et  al. 2000), Sabella pavonina (Murray et  al. 2011), Branchiomma luctuosum (Licciano et al. 2002), Bispira volutacornis (Nash and Keegan 2003), Terebrasabella heter­ ouncinata (Simon 2004), Sabellastarte spectabilis (Bybee et  al. 2007), and Branchiomma bairdi (Tovar-Hernández et al. 2011, Arias et al. 2013). Spermatogenesis happens in tetrads in most of Sabellinae, but clusters of spermatids attached to a cytophore can be found in several genera. The clusters can be composed of more than 100 spermatids, as

180 

 7.4 Sedentaria: Sabellida/Spionida

in Caobangia and Potamilla, or of less than 100 spermatids, as in Amphiglena and Laonome (Rouse and Fitzhugh 1994, Fitzhugh and Rouse 1999, Rouse et al. 2006). Mature sperm have spherical heads and mitochondria and a free flagellum (e.g., Bispira, Sabella, ­Branchiomma, Parasabella, Perkinsiana, Eudistylia, and Pseudopotamilla; Fig. 7.4.6.13 D, E), cylindrical head and spherical mitochondria and free flagellum (e.g., ­Myxicola, Chone, Euchone, and Potamethus; Fig.  7.4.6.13 C), or elongate heads with elongate mitochondria forming a long midpiece and free flagellum (e.g., Caobangia, Amphicorina, and Amphiglena) (Giangrande and Petraroli 1994, Rouse and Fitzhugh 1994, Giangrande et al. 2000).

Spermathecae have been described only in Amphic­ orina, Amphiglena, and Terebrasabella. Terebrasabella is unusual in having a single spermatheca, with blind ending and extending along the ventral epidermis from the basal part of the crown to at least the first chaetiger (Simon and Rouse 2005), whereas in Amphicorina and Amphiglena spermathecae are always paired (Rouse 1992, Rouse and Gambi 1998b). Based on the classification system of sperm defined by Jamieson and Rouse (1989), ect-aquasperm type is found in broadcasting species with external fertilization, in which sperm are released into the water and fertilize similarly released eggs, as in B. luctuosum (Sordino and Gambi 1994,

Fig. 7.4.6.13: Oocytes, spermatozoa and brooding. A, Acromegalomma carunculatum from Mexico, a gravid female releasing oocytes after body wall rupture; B, sperm of Branchiomma bairdi from Mexico. C–E, Acrosome development and internal structure in broadcasting sabellids; C, Myxicola infundibulum from Italy (×12,000); D, Branchiomma luctuosum from Italy (×28,000); E, Eudistylia vancouveri (×20,000). F, Embryos of Aracia sinaloae from Mexico attached to the dorsalmost pair of radioles. A, F, light microscopy B, SEM C–E, TEM Images: A, B, F, by M.A. Tovar-Hernández; C–E, by A. Giangrande.



Licciano et  al. 2002; Fig. 7.4.6.13 D) and Sabellastarte spectabilis (Bybee et al. 2006a). In turn, ent-aquasperm type is found in species with in situ fertilization, in which sperm are also released freely into the water but are gathered by or in some other way reach the female before fertilization that never happens in the water column. Ent-aquasperm have been reported in Amphicorina spp. (Rouse 1992), Amphi­ glena spp. (Rouse 1993, Rouse and Gambi 1998a,b), Perkin­ siana antarctica (Kinberg, 1866) (Gambi and Patti 1999), Aracia riwo (Rouse, 1996) (Rouse 1996a), and T. heterounci­ nata (Fitzhugh and Rouse 1999, Simon and Rouse 2005). The egg size varies from very small, as 82 µm diameter in Amphicorina brevicollaris (Rouse, 1990) and Jas­ mineira regularis Hartman, 1978 (Giangrande 1997), or 110 µm in B. bairdi (Tovar-Hernández et  al. 2009a), to large, as 250 µm diameter in Parasabella microphthalma (Verril, 1883) and Sabella spallanzanii (Giangrande 1997), with the largest eggs being 500 µm in diameter in Potamilla torelli (Malmgren, 1866) (Rouse and Fitzhugh 1994) and 600 µm in Amphiglena marita (Chlebovitsch 1959). However, most of the species have eggs measuring from 120 to 150 µm (Giangrande 1997). Estimates of egg numbers range from a minimum of one per body in Caobangia (Rouse and Fitzhugh 1994) to nearly 660,000 in Eudistylia vancouveri (Kinberg, 1866) Rouse and Fitzhugh 1994), with intermediate ranchiomma such as 2500 in Chone duneri Malmgren, 1867 (Yun and Kikuchi 1991a) or 1300 in Branchiomma bairdi (Tovar-Hernández et al. 2011). There is no information about male fecundity in sabellids. Natural spawning has been detailed for Acromeg­ alomma vesiculosum by Hornell (1893). In laboratory, spawning and fertilization is not easy to observe. It was obtained for some broadcasting species such as Myxi­ cola  infundibulum (Dean et  al. 1987), Bispira volutacor­ nis (Yun and Kikuchi 1991a), Sabellastarte spallanzanii (Giangrande et  al. 2000), Branchiomma luctuosum (Licciano et  al. 2002), and Sabellastarte spectabilis (Bybee et  al. 2007). In the last species, fertilization probably does not happen in the water column but takes place in the tube just after the eggs are released from the coelomic cavity, and the produced mucus acts as a medium in which eggs are released and fertilized (Stabili et  al. 2011). B. volutacornis releases all its gametes in a single large batch, surviving to breed again. Gravid specimens have a bloated appearance before spawning, with the coelom filled to its maximum capacity with gametes. Gametes are released through gonoducts located segmentally and midlaterally to the parapodia. The deeply segmented ventral shields aid in the organized passage of the gametes. The gametes travel along the transverse

7.4.6 Sabellidae Latreille, 1825 

 181

furrows, in a streamlike fashion, reach the midline of faecal groove, and follow this groove anteriorly. The flow of gametes is assisted by rapid muscular contractions of the abdomen, which continue for the duration of spawning. In the crown, the gametes enter upward flowing rejection current (Nash and Keegan 2003). Also under laboratory conditions, many adults of C. duneri were seen to emerge from the anterior half of the body from their tubes during spawning (Yun and Kikuchi 1991a). Most large sabellids are iteroparous (able to reproduce more than once, often annually or semiannually), devoting considerable amounts of energy and body space to the reproduction of copious numbers of gametes seasonally (Giangrande 1997, Patti et  al. 2003). Chone duneri is semelparous; it spawns only once and dies soon after discharging the gametes (Yun and Kikuchi 1991a). Sabellastarte spectabilis has a broad maturation period with clear evidence of one peak in October (annual producers) in which wild-caught worms were induced to spawn (Bybee et al. 2007). Small worms generally have semicontinuous reproduction (reproduce continuously over an extended season) because of limitations in body volume as seen in Amphiglena mediterranea Leydig, 1851 (Rouse and Fitzhugh 1994). In Sabellastarte spallanzanii, males were recorded to account for more than 80% of the reproductive population in the Mediterranean Sea (Giangrande and Petraroli 1994); however, further investigations revealed an actual sex ratio of 1:1 (Giangrande et al. 2000). A sex ratio of 1:1 was also described for Chone duneri (Yun and Kikuchi 1991a), Branchiomma luctuosum (AG, unpublished data), and Sabellastarte spectabilis (Bybee et al. 2006a). Protection of larvae (brooding) is present in some sabellids, be it intratubular or extratubular, although the first pattern is more common in the group (e.g., Amphi­ corina, Amphiglena, Caobangia, and Potamilla; Rouse and Fitzhugh 1994). Three types of extratubular brooding have been documented. One consists in keeping the larvae in a jelly ring located around the mouth of the tube (McEuen et al. 1983) and was observed in Parasabella media Bush, 1905, and Branchiomma lucullanum (Delle Chiaje, 1828). In another type, larvae form a mass attached to a single radiole, as seen in Perkinsiana antarctica (Knight-Jones and Bowden 1984, Gambi and Patti 1999, Gambi et  al. 2000); on ventralmost radiolar pair, as in A. riwo (Rouse 1996a); or on the modified dorsalmost pair of radioles, as in Aracia heterobranchiata (Nogueira et al. 2004) and Aracia sinaloae (Tovar-Hernández 2014; Fig. 7.4.6.13 F). A third type consists in brooding the larvae embedded in a jelly mass attached to the mouth of the tube and is only known for Chone infundibuliformis (Okuda, 1946).

182 

 7.4 Sedentaria: Sabellida/Spionida

Fig. 7.4.6.14: Larvae of Sabellastarte spectabilis from Hawaii. A, 24 h after hatching; B, 5 days after hatching; C, settled larva, 7 days old A–C, SEM. Images by D. Bybee.

All sabellids present lecithotrophic larvae (Rouse  and Fitzhugh 1994) with a short planktonic phase (Fig. 7.4.6.14 A–C), lasting only 1 to 2 days in Laonome albicingillum (Hsieh 1995, 1997), 3 days in Branchiomma luctuosum (Licciano et al. 2002), 6 days in Branchiomma nigromaculatum (Berrill 1978), 7 days in Myxicola infundibulum (Dean et  al. 1987), and 9 days in Acromegalomma vesiculosum (Wilson 1936) and Parasabella media (McEuen et  al. 1983). The longest period, 2 weeks, was recorded for Sabellastarte spallan­ zanii (Giangrande et al. 2000, Pernet et al. 2002). Detailed accounts of the complete sequences of larval development through metamorphosis are known for Chone infundibul­ iformis, Chone duneri (Yun and Kikuchi 1991b), Terebrasa­ bella heterouncinata (Gray and Kaiser 2007a,b), and Sabel­ lastarte spectabilis (Bybee et al. 2006b). Larvae of P. media settle 9  days after spawning, and metamorphosis begins with the ­emergence of branchial buds and loss of prototroch and neurotroch; however, metamorphosis is only completed at day 15 (McEuen et al. 1983). In S. spectabilis, settlement occurs 6 to 7 days after spawning, when prototroch is lost and larvae drop out of the water column, no longer able to swim, and settles on the bottom (Bybee et al. 2006b). Very little is known about sabellid longevity. The largest species, Sabellastarte spallanzanii, can live for more than 5 years and attain a very large size (50 cm) (Giangrande and Petraroli 1994), but Branchiomma luctuosum can reach a large size (40 cm) in only 2 years. The former species reproduces at the second year of its life, whereas the latter reproduces during the first year of its life, and oogenesis starts at just the third month (Mastrototaro et al. 2014). Small-sized species live for only 1 year, e.g., such as Chone duneri (Yun and Kikuchi 1991a), or even less than 1 year, such as Amphi­ glena mediterranea (AG, unpublished data). Sabella pavonina (as Sabella penicillus), Myxicola infundi­bulum, and Chone infundibuliformis have a diploid count of 28 chromosomes (Christensen 1980). Asexual reproduction in sabellids takes the form of architomy (spontaneous fission or autotomy followed

by subsequent regeneration). Thus, natural fission or ­autotomy has been recorded in 14 species (Tab. 7.4.6.2). Among these species, Sabella discifera, Branchiomma bairdi, Bispira brunnea, Pseudopotamilla reniformis, and Pseudobranchiomma spp. form dense aggregations, and natural fission seems a process that leads to the formation of colonial forms as in some serpulids (Nishi and Nishihara 1994; Pernet 2001). Acromegalomma cinctum, P. reniformis, Bispira ­manicata, B. brunnea, and B. bairdi also reproduce sexually (all are gonochoric, except for hermaphrodite B. bairdi). In A. cinctum, a small portion of the population (4%–13% of individuals) exhibited scissiparity (Yuan 1992), and in B. brunnea, 92% of the population reproduce asexually (Dávila-Jiménez et al. 2017). In the Gulf of California, 82% of the population of Pseudobranchiomma schizogen­ ica was found to be undergoing architomy during summer (Tovar-Hernández and Dean 2014). In the White Sea, 95% of the entire population of P. reniformis reproduce asexually during winter (Kolbasova et  al. 2013), and asexual reproduction happens throughout the year in B. bairdi, with an annual mean approximately 11% (Tovar-Hernández et  al. 2011). In Sabella discifera, worms regenerating posterior ends may be accompanied by one or two shorter individuals of similar width, regarded as offspring budded off by fission from the parent portion. The tubes are separate and unbranched, except for occasional short branches near the proximal end. Presumably, the clonal offspring leave the parental tube at one end or the other before they secrete their own tubes (Rioja 1929, Knight-Jones and Bowden 1984). Abdominal constrictions resulted in two to four abdominal fragments positioned in the parental tube of Pseudopotamilla reniformis in a chainlike fashion. These fragments are different, and some clonal offspring regenerate the crown and the thorax, whereas other restore both the crown and the thorax anteriorly and pygidium posteriorly. The clonal offspring make cracks in the posterior part of the parental tube, curve their bodies sidewise, and pull

7.4.6 Sabellidae Latreille, 1825 



 183

Tab. 7.4.6.2: Sabellids where asexual reproduction has been reported. Note that species marked with an asterisk also reproduce sexually, see text for details. Species

References

*Bispira brunnea (Treadwell, 1917) *Bispira manicata Capa, 2008 *Branchiomma bairdi (McIntosh, 1885) Branchiomma curtum (Ehlers, 1901) *Acromegalomma cinctum (as Megalomma sp. in Yuan 1992) Myxicola aesthetica (Claparéde, 1870) Perkinsiana milae Giangrande & Gambi, 1997 Perkinsiana rubra (Langerhans, 1880) Pseudobranchiomma minima Nogueira & Knight-Jones, 2002 Pseudobranchiomma perkinsi Knight-Jones & Giangrande, 2003 Pseudobranchiomma punctata (Treadwell, 1906) Pseudobranchiomma schizogenica Tovar-Hernández & Dean, 2014 *Pseudopotamilla reniformis Bruguière, 1789 Sabella discifera Grube, 1874

Tovar-Hernández and Pineda-Vera (2008), Dávila-Jiménez et al. (2017). Capa (2008) Tovar-Hernández et al. (2009b), Arias et al. (2013) Tovar-Hernández and Knight-Jones (2006) Fitzhugh (2003) Knight-Jones and Bowden (1984) Gambi et al. (2000) Knight-Jones and Bowden (1984) Nogueira and Knight-Jones (2002) Knight-Jones and Giangrande (2003) Nogueira and Knight-Jones (2002) Tovar-Hernández (2014) Kolbasova et al. (2013) Rioja (1929), Knight-Jones and Bowden (1984)

their head and posterior abdomen first and then the rest of the body through the opening. The emerging clone builds a transparent tube attached to a neighboring tube in the basal layer of the aggregation (Kolbasova et al. 2013). The same developmental pattern was also documented in Pseudobranchiomma schizogenica, where clonal offspring regenerate the crown and the collar, whereas others were found restoring both the crown and the collar anteriorly and the pygidium posteriorly (Tovar-Hernández and Dean 2014). Tubes of Branchiomma curtum contained many developing ­scissiparous offspring posterior to the parents. The posteriormost parts of the abdomen separate into a few multisegment fragments, and anteriorly each segment chaetae of thoracic type are gradually formed. Such regeneration is usually imperfect, producing individuals with fewer thoracic segments than the usual eight thoracic segments (Tovar-Hernández and Knight-Jones 2006), as also seen in Branchiomma nigromaculatum (Berrill 1978), Branchiomma bairdi (Tovar-Hernández et al. 2009b, 2011), and some species of Sabellastarte (Murray et al. 2013). By contrast, in Bispira manicata, a higher number of thoracic segments is produced after regeneration (Capa 2008; Fig. 7.4.6.15 D). Within Sabellidae, the replacement of a body part lost  through traumatic injury (either natural fission or autotomy and amputation) is variable (Bely 2006, Licciano et  al. 2012; Fig. 7.4.6.15 A–H). Species may be capable or incapable of regenerating anterior segments (Fig. 7.4.6.15 A, D–F), posterior segments, and/or terminal asegmental structures (Fig. 7.4.6.15 B, C, G, H). Specimens of Branchiomma bairdi have been found with two pygidia and bifurcated posterior end (Tovar-Hernández et al. 2009b; Fig. 7.4.6.15 B). Regeneration takes place via

epimorphosis (replacement of missing parts by cell proliferation and the growth of new tissue), morphallaxis (the remodeling of preexisting structures without cell proliferation), or a combination of both mechanisms. However, Agata et  al. (2007) proposed the “intercalary model” whereby organisms initially form the most distal part and then reconstitute the intermediate regions by appropriate intercalation of newly generated tissues between the newly formed distal part and the remaining body. Epimorphosis was described for Amphiglena mediter­ ranea (Giangrande et al. unpubl. obs.), Sabellastarte spp. (Murray 2010), and Branchiomma luctuosum (Licciano et  al. 2012). Combining epimorphosis and morphallaxis is a process described by Berrill (1931, 1977, 1978), Berrill and Mees (1936a,b), Murray (2010), Licciano et al. (2012), Murray et al. (2013), and Kolbasova et al. 2013 for Branchi­ omma bombyx (Dalyell 1853), B. nigromaculatum, Bispira melanostigma (Schmarda 1861), B. volutacornis, Mega­ lomma vesiculosum, Potamilla  torelli (Malmgren 1866), P. reniformis, Sabella pavonina, and S. spallanzanii. According to Kolbasova et  al. (2013), morphallaxis is likely to be less energy consuming than epimorphosis because it involves remodeling of some preexisting structures, whereas epimorphosis requires ex novo ­formation of missing segments from blastema. Moreover, morphallaxis provides rapid restoration of a large amount of thoracic segments simultaneously and supports rapid regeneration and high survival rate. Thus, Branchiomma luctuosum survives after induced fragmentation but shows high mortality of fragments and slow regeneration rate, whereas Branchiomma  nigromaculatum, Sabella spallanzanii, Sabellastarte spp., and Pseudopotamilla reniformis regenerate easily and have a high ­survival rate (Berrill 1977,

184 

 7.4 Sedentaria: Sabellida/Spionida

1978, Licciano et  al. 2012, K ­ olbasova et  al. 2013, Murray et al. 2013). The regeneration capabilities can vary greatly even between phylogenetically close species. For instance, Myx­ icola  infundibulum cannot regenerate anterior segments, even if just a single anterior segment is removed (Nicol in Wells 1952). It just can regenerate the crown, and only if a stump of this structure is present. By contrast, its congener Myxicola aesthetica (Claparéde, 1870) can regenerate several anterior segments lost (Berrill 1931, Okada 1934). In Fabrisabella, Jasmineira, and some species of Sabella (as S. penicillus), an abscission zone at the base of crown has been documented (Kennedy and Kryvi 1980, Tovar-Hernández 2008). It is a preestablished zone of rupture where, under various circumstances, the radiolar crown becomes detached from the body. In Fabrisabella and Jasmineira, the abscission zone or

breaking plane is a discrete area located immediately above the radiolar bases (Cochrane 2003, Tovar-Hernández 2008; Fig. 7.4.6.15 A, E, F), and it is a typical feature of members of these genera. In Sabella pavonina and Myxicola aesthetica, the abscission zone is located in the cartilaginous matrix, and this allows for a fast regeneration of the missing structure (Berrill 1931, Okada 1934). Abscission involves a rupture of the paramyosin muscle cells, which form bridges connecting extensions from the epimysium of the body wall musculature and form the cartilage matrix of the crown (Kennedy and Kryvi 1980). S. pavonina is able to control the loss of its radiolar crown, so this abscission is a kind of autotomy. The high regenerative ability found in several sabellids is not necessarily linked to the presence of asexual reproduction, as in Sabella spallanzanii and Amphiglena med­ iterranea (Giangrande et al. unpubl. obs.).

Fig. 7.4.6.15: Breakage and regeneration. A, Radiolar crown broken at abscission zone, Fabrisabella sp. from USA; B, Branchiomma bairdi from Mexico, with two pygidia after imperfect regeneration; C, Bispira manicata from Australia, regenerating posterior abdominal segments and pygidium; D, thorax of B. manicata showing a high number of thoracic segments (to the arrow) after imperfect regeneration; E, radiolar crown broken at abscission zone, ventral view, Jasmineira sp. from Australia; F, same, anterior view; G, Pseudobranchiomma schizogenica from Mexico, offspring after scissiparity; H, Parasabella sp. from Australia regenerating posterior abdominal segments and pygidium. A–D, light microscopy; E–H, SEM. Images: A, C, E, F, H, by M. Capa; B, by H. Bahena-Basave; D, by E. Wong; G, by M.A. Tovar-Hernández.



Biology and ecology Symbiotic associations Sabellids can act both as host and symbiont. In their large revision of symbiotic polychaetes, Martin and Britayev (1998, 2018) mentioned Sabellidae as boring parasites. Some interactions between these boring worms and their hosts seem to be negative, making the species to be labeled as “parasitic” borers. Among them, Caobangia (Fig. 7.4.6.1 H) exclusively inhabits shells of several freshwater genera of snails (Jones 1974), and Terebrasabella heterouncinata Fitzhugh and Rouse, 1999 (Ruck and Cook 1998, Fitzhugh and Rouse 1999), burrows into the shells of various marine gastropods. Infestation by T. heterouncinata has been shown to cause deformation and weakening of the shell, a reduction in the growth rate, or the death of the abalone and marketability of cultured abalone in South Africa and California, where it was introduced three decades ago (Fitzhugh 1996, Oakes and Fields 1996, Culver et al. 1997). Members of Acromeg­ alomma, Notaulax, Perkinsiana, and Pseudopotamilla can bore into dead coral and limestone (Chugthai and KnightJones 1988, Nishi and Nishimira 1999, Fonseca et al. 2006). Mesoparasitic copepods belonging to Gastrodelphyidae List, 1889, Sabelliphilidae Gurney, 1927, Jasmineiricolidae Boxshall et al. 2015, and Euchonicolinae Boxshall et al. 2019, are typically external symbionts of Sabellidae (Boxshall and Halsey 2004; Fig. 7.4.6.16 A–C), and only one species of Rhynchomolgidae Humes and Stock, 1972, was recorded as parasite of sabellids, associated with Myxicola infundibulum (Bocquet and Stock 1958). Euchonicolinae is a subfamily of mesoparasitic copepods which members lives associated to species of Euchone, Chone and Jasmineira (Boxshall et al. 2019). Some copepods, such as Gastrodelphys dalesi (Green 1961), can use different sabellid species as hosts (Dudley

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1964, Boxshall and Halsey 2004, Gómez and Tovar-­ Hernández 2008). By contrast, Gastrodelphys clausii Graeffe, 1883, is only known from Bispira volutacornis (Nash and Keegan 2006). Species of Sabellacheres Sars, 1862, are known to establish species-specific relationships with sabellid hosts: Sabellacheres gracilis Sars, 1862, with Myxicola infundibulum; Sabellacheres aen­ igmatopygus Carlton, 1971, with Pseudopotamilla reni­ formis; Sabellacheres drachi Laubier, 1968, with Potamilla torelli (Malmgren 1866); and Sabellacheres antarcticus Suárez-Morales and Boxshall, 2012, with Perkinsiana brigittae Tovar-Hernández et  al., 2012 (Dudley 1964, Laubier 1968, Carton 1971, Boxshall and Halsey 2004, Suárez-Morales and Boxshall 2012). Moreover, Sabel­ liphilus elongatus Sars, 1862, has only been found on the ­radioles of Sabella pavonina, and Sabelliphilus sarsi Claparède, 1870, on Sabella spallanzanii (Gotto 1960, Carton 1966). It has been reported that S. elongatus extracts oil or fat by slight erosion of the pigmented epithelium and may also utilize its mucus. Nevertheless, although these copepods are reported to be ectoparasites, there are no specific studies concerning the infestation, and much of the nature of the association between copepods and their sabellid hosts remains largely unknown (Nash and Keegan 2006). The life cycle of Ceratomyxa auerbachi Kabata, 1962, a myxosporean parasite of the Atlantic herring Clupea harengus Linnaeus, 1761, requires Chone infundibuliformis Krøyer, 1856, as an alternate invertebrate host. During the life cycle of this parasite, the actinospore is released from the coelom of the sabellid host, infests the fish, and develops in the kidney to form a parvicapsula myxospore, which is the stage infective to the polychaete worm (Køie et al. 2008). Recently, an unidentified parasite gregarine, apicomplexan, has been found within the coelomic cavity of Branchiomma bairdi (Arias et al. 2013).

Fig. 7.4.6.16: Symbiont copepods. A, Copepod Gastrodelphys dalesi attached to the dorsal pockets of collar on Acromegalomma circumspectum from Mexico; B, details of G. dalesi; C, Sabellacheres antarcticus attached to radioles of Perkinsiana antarctica. A–C, light microscopy. Images: A, B M.A. TovarHernández; C B. Yáñez-Rivera.

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 7.4 Sedentaria: Sabellida/Spionida

Behavior Sabellids are epibenthic suspension feeders exposing their radiolar crown out of their tube for collecting particles from the water column (Figs. 7.4.6.1 A and 7.4.6.116 A–E). The radiolar crown can be protected from hostile environment or predation by quickly and completely retracting inside the tube (Higuchi et  al. 1986, Giangrande 1991, Licciano et  al. 2012). Some Sabellidae are also characterized by unpalatable crown protected from predation either chemically or structurally, and these features of the branchial crown are often inversely correlated to the presence of soft tubes that offer weak resistance to tearing and weak protection to worms (Kicklighter and Hay 2007; Giangrande et  al. 2014). Interestingly the different chemical compounds accumulated in the branchial crown for defense seem to have phylogenetic signal (Giangrande et al. 2016). Moreover, the autotomy of the radiolar crown can occur in some taxa as an escape mechanism (to distract predators while the worm retracts inside tube), as a selective mechanism (rejecting a crown that has been mutilated or suffers malformation), or, for example, as a response to stress (Kennedy and Kryvi 1980) similar to Sabella spallanzanii (Giangrande et al. 2014). Radiolar crown plays also a role in gas exchange. It accounts for 80% of the total respiration in species having a strongly attached crown (Giangrande 1991), but worms loosing the crown (explained below) can compensate their gas exchange needs with body wall respiration. This is made possible by rhythmic movements of the body that generate currents of the water contained in the tube in both directions (i.e., irrigation) (Giangrande 1991, Nash and Keegan 2003). The involved respiratory surfaces seem to be the ventral shields and the parapodial areas, both greatly vascularized (Giangrande 1991). Some species open apart the two halves of the crown almost forming one plane (Figs. 7.4.6.1 B, C and 7.4.6.2 A–D), whereas others keep them close forming a shallow funnel around their mouth (Figs. 7.4.6.1 D and 7.4.6.4 A). The expanded radioles and the arrangement of each of the two rows of pinnules (forming an angle of more than 90°) generate an intricate grid for capturing particles from the water column (Nicol 1931). Water currents are created by the cilia on the pinnules and the ventral radiolar appendages if present (Bonar 1972). When particles are collected by the cilia, they are directed into the ciliated grove located at the inner side of the radioles, where they are taken down to the mouth area with the help of mucus secreted by ­epithelial cells (Nicol 1931, Bonar 1972). In most sabellids, a sorting of particles according to their size takes place, a process in which radiolar structures such as the dorsal lips and radiolar appendages play a main role (Bonar 1972, Perkins 1984). The

small-sized particles are swept into the mouth as food, the medium-sized ones enter the ventral sacs to be used for tube building (when present; Fig. 7.4.6.3 E–G), and the large-sized ones are rejected off the dorsal lips and radiolar appendages. Medium-sized particles are cemented together with mucus, molded into strings at the edges of the anterior end of the tube. Small species with no such radiolar appendages use the dorsal lips for rough material sorting in two categories (Bonar 1972). Most of the species feed on phytoplankton, but they can also utilize both particulate and dissolved organic matter, as well as bacterioplankton (Licciano et al. 2005, 2007). Gut content of Bispira volutacornis (Montagu 1804) included rests of benthic diatoms, peridinians, silicoflagellates, foraminiferans, tintinnids, annelid/crustaceans bristles, and detritus (Nash and Keegan 2003). The ventral shields present in most sabellids secrete a semitransparent material consisting of a mucopolysaccharide–protein complex secreted by the ventral shield glands or other epithelial glands. This mucus is used to cement different particles in tube building, which is a constant process accompanying animal growth. The ventral sacs and some of the anterior appendages, when present, are involved in the growth and reconstruction of the anterior end of the tube, whereas the pygidial structures and epithelium that secretes mucus are responsible for the tube building at the posterior end (Nicol 1931). The ventral sacs and the collar folds, when present, are the two most essential parts of the sediment–tube-building apparatus. Myxicola lacks both of these structures, the reason why its tube is entirely built with the mucus secreted by the glands occurring dorsally as well as ventrally, and no sediment is attached (Nicol 1931). In Chone, and probably other small sabellids, the sorting mechanism is only rudimentary and nothing is collected for tube building. Worms out of a tube immediately start boring into the sediment with their pygidia, initially laying on their ventral surface but soon rolling from side to side gaining traction on the substratum with their parapodial chaetae and pushing deeper into the sediment. Glands in the epidermis secrete mucus around their surface sticking sand, shell fragments, faecal material, and assorted debris forming a thin sand-covered tube (Bonar 1972). The mucus outer layer hardens but its production is continuous, lubricating the inner side of the tube and also making it thicker (Bonar 1972). The resulting tube is oriented vertically in the sediment, which is two or three times the length of the animal. However, Chone is not as sedentary as most tube worms and can leave and build several tubes within a week (Bonar 1972). Tube building in Glomerula pilosetosa has not being studied, but it is possible that members of this



species have secretory glands in the collar similar to those present in serpulids. The role of mucous secretions has been investigated not only in tube-building process but also in absorbing metabolites (Bonar 1972). Sabellids, as other invertebrates, can release defensive molecules against ­microorganisms and/or epibionts mixed with their mucus (Bonar 1972, Stabili et  al. 2009). A defensive hemolytic activity of the mucus in Sabella spallanzanii (Canicattì et  al. 1992) may be related with their association to eutrophic environments that require efficient mucosal defense mechanisms because they are under constant threat from a rich mixture of microorganisms in the surrounding water (Stabili et al. 2006, 2009, 2011). Unlike serpulids that left a significant fossil record, sabellid fossils are uncommon. A reported case is that of Glomerula lombricus (Defrance 1827) as encrusters on scleractinian corals from the Agrio Formation (Early Cretaceous; 132–126 million years ago) in Neuquén Basin, Argentina (Garberoglio and Lazo 2011). Subsequently, several fossil species of Glomerula have been recorded for the Netherlands, Campan, Maastricht, Belgium, northern Germany (Jäger 2004, 2012, Kočí 2012). and ­

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Not long ago, Calcisabella piloseta Perkins, 1991, was described as the first sabellid with calcareous tube. This monotypic genus is currently considered synonymous of Glomerula (see Jäger 2004), and the species G. pilosetosa represents the unique known extant species of the genus, endemic from the Great Barrier Reef, Australia. The ultrastructure of the tubes of Glomerula is clearly different from that of serpulids, suggesting that the acquisition of calcareous tubes is an evolutionary convergence with serpulids (Vinn et al. 2008). Distribution Sabellids live typically in marine environments, although some taxa belonging to the genera Desdemona, Laonome, and Euchone are able to live in estuarine conditions, withstanding abrupt changes in salinity and temperature (Hutchings and Murray 1984, Castelli et  al. 1988, Capa et al. 2014, Bick et al. 2018), and members of Caobangia are exclusive of fresh waters (Jones 1974, Glasby et al. 2009). Many species inhabit littoral hard substrates as epibionts on algae, associated with sponges, mollusks, and ascidians (Fig. 7.4.6.17 A, D). Others live in crevices of rocks and corals, and some of them, such as some

Fig. 7.4.6.17: Sabellids in their environment. A, Sabella spallanzanii from Italy; B, Sabellastarte sp. from Indonesia; C, Bispira brunnea from Mexico; D, Bispira viola from Italy; E, Branchiomma luctuosum from Italy. Images: A, R. Pronzato; B, C. Pichon; C, H, Bahena-Basave; D, S. Causio; E, F. Mastrototaro.

188 

 7.4 Sedentaria: Sabellida/Spionida

species of Sabellastarte or Bispira are exploited for ornamental purposes (Capa et  al. 2010, Murray et  al. 2013; Fig. 7.4.6.17 B, C). Several species are foulers, colonizing artificial substrates of marinas, harbors, and other sheltered areas, where they can reach very high densities, as reported for species of Branchi­ omma, Eudistylia, Acromegalomma, Parasabella, and Sabella (Licciano et  al. 2005, 2007, Stabili et  al. 2006, 2009, Tovar-­Hernández et al. 2009b, Capa et al. 2013a; Fig. 7.4.6.17 A, E). Species belonging to Jasmineira, Chone, Euchone, Fab­ risabella, Perkinsiana, and Potaspina have been reported in soft bottoms, from shallow waters down to 1000 m (e.g., Hartman 1969, 1978, Fauchald 1972, Ruff and Brown 1989, Capa 2007, Méndez 2006, 2013, Tovar-Hernández 2008), but some have been collected down to 3000 m in Antarctica (Tovar-Hernández et al. 2012, Capa et al. 2013b). Considering the distribution on the continental shelf, a latitudinal pattern can be recognized at generic level. Thirty genera and most of the species are found in tropical areas, mainly in the Indo-Pacific (Giangrande and Licciano 2004; Fig. 7.4.6.17). Caobangia, Amamobaea Krøyer, 1856, and Stylomma are exclusive to the tropics (Jones 1974, Tovar-Hernández and Salazar-Vallejo 2006, Capa 2007), whereas Acromegalomma, Sabellastarte, Sabellonga Hartman, 1969, Branchiomma, Bispira, and Notaulax seem to have, with few exceptions, a tropical and temperate distribution (Perkins 1984, Knight-Jones and Perkins 1998, Knight-Jones and Mackie 2003, Tovar-Hernández and Knight-Jones 2006, Tovar-Hernández and Carrera-Parra 2011). Most of the genera abundant in the Indo-Pacific region are absent at high latitudes. By contrast, genera well represented in cold areas (such as Chone, Euchone, and Jasmineira) are almost absent in the Indo-Pacific.

The genus Eudistylia is present only in the northern hemisphere, whereas Amphi­corina is mainly distributed in the Southern Hemisphere (Giangrande and Licciano 2004). Lastly, Perkinsiana has 11 species distributed in southern cool areas and is particularly abundant in the Antarctic Ocean (Tovar-Hernández et al. 2012). The Antarctic region seems richer in number of genera than the Arctic (15 present in the Antarctic against 9 in the Arctic) and shows a higher degree of ­endemism (AG, unpublished data). Several recent revisions, in some cases including molecular data, have clarified and restricted the distribution of some species, as has happened with Chone duneri (Tovar-Hernández et  al. 2007), Acromegalomma vesicu­ losum Montagu, 1815 (Giangrande and Licciano 2008), several species of Branchiomma (Capa et al. 2013a), Sabella (Knight-Jones and Perkins 1998), and Sabellastarte (Capa et al. 2011a). In this context, some species such as Myxi­ cola infundibulum, formerly considered cosmopolitan, are currently under investigation, searching for the existence of cryptic forms (Greaves et al. unpubl. obs.). The distribution range of some species was recently expanded after unintentional translocation out of their natural expected distribution range (e.g., Kuris and Culver 1999, Çinar et al. 2006, El Haddad et al. 2008, Çinar 2009, Tovar-Hernández et al. 2009a,b, 2011, Gravili et al. 2010, Zenetos et al., 2010, 2012, Capa et al. 2014). In some cases, none or very little genetic variation between long distance and disjunct populations has been quantified, assessing the status as introduced by these species (Patti and Gambi 2001, Read et al. 2011, Capa et al. 2013a). A well-known case is the Atlantic-Mediterranean species, Sabella spallanza­ nii (Fig. 7.4.6.16 A), which was introduced into ­Australia approximately 20 years ago and subsequently into New  Zealand. In these countries, S. spallanzanii became

Fig. 7.4.6.18: Distribution of sabellids species richness among domains.



a pest, heavily affecting marine ecosystems and causing serious coastal economic consequences (Lemmens et  al. 1996). Other examples of invasive species are Branchiomma luctuosum (Grube 1870) originally described from the Red Sea, introduced in the Mediterranean basin at least 20 years ago and currently reaching densities of up to $$900 ind m2 (Bianchi 1983, Licciano et  al. 2002, Çinar et  al. 2006, El Haddad et al. 2008, Zenetos et al. 2010) and also reported from Brazil (Nogueira et al. 2006), and Branchi­ omma bairdi (­McIntosh 1885) originally described from the ­Caribbean and reported in the Gulf of California, the Mediterranean, the Canary Islands, and Australia (Çinar 2009, Tovar-Hernández et al. 2009a,b, 2011, Zenetos et al. 2010, Giangrande et al. 2012, Arias et al. 2013, Capa et al. 2013a), reaching densities of 16 ind m2 in the Mediterranean (Arias et  al. 2013) and 18,000 ind m2 in the Gulf of ­California (Tovar-Hernández et al. 2014).

Phylogeny and taxonomy Phylogeny. The first sabellid described was Sabella peni­ cillus Linnaeus, 1767, and the family Sabellidae was erected by Latreille in 1825. A close relationship between Sabellidae (including Fabriciinae) and Serpulidae has always been assumed, being the group classified under names such as Serpulacea (Grube 1850), Sabelliformia (Benham 1896), or Serpulimorpha (Uschakov 1955). The current name for the order Sabellida was established by Dales in 1962, but the order has undergone changes in its composition along time (Fauchald 1977, Fitzhugh 1989, Rouse and Pleijel 2001, among others). It is now mostly accepted the restricted use of Sabellida to accommodate three families: Sabellidae, Serpulidae, and Fabriciidae (Kupriyanova and Rouse 2008, Capa et al. 2011a). The change on the concept of Sabellida through time has also affected the diagnosis of Sabellidae. Fitzhugh (1989) performed the first phylogenetic analysis of the group, synonymized with Sabellidae some taxa previously considered as separate families (i.e., ­Sabellongidae Hartman, 1969, and Caobangiidae Jones, 1974), and subdivided the family into two subfamilies, Sabellinae and Fabriciinae, emending both diagnoses. Rather than the presence of avicular or acicular uncini, which were thought by that time to separate Sabellinae from Fabriciinae (Rioja 1923, Fauchald 1977), or the presence or absence of thoracic uncinial companion chaetae (Fauchald 1972), the author showed that what separates these two groups is the presence of at least two rows of vacuolated skeletal cells within the radioles, except Cao­ bangia, and the dorsal fusion of radiolar lobes, both characters occurring in Sabellinae only (Fitzhugh 1989, 1991).

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This view of Sabellidae changed recently, when Serpulidae was found nested within Sabellidae and sister to Fabriciinae (Kupriyanova and Rouse 2008, Capa et al. 2011b, Huang et al. 2011; Fig. 7.4.6.19 A). Kupriyanova and Rouse (2008) raised the fabriciid clade to family level, whereas Capa et al. (2011b) added the presence of dorsal and ventral lips as diagnostic for Sabellidae, together with several synapomorphies for Fabriciidae. As currently conceived, Sabellidae counts on 40 genera. The most comprehensive phylogeny to date, including both morphological and molecular data, included representatives of 20 of these genera, among a broad range of outgroups (Capa et al. 2011a; Fig. 7.4.6.19 A). Sabellidae was found to gather two major clades, none of them with robust support. These clades are somehow consistent with other recent phylogenetic hypothesis based on morphological features, except the position of the Amphicorina-Myxicola-ChoneDialychone-Jasmineira-­Fabrisabella group and related taxa (e.g., Nogueira et  al. 2010; Fig. 7.4.6.19 B), basal in analyses that only consider morphological features but not in combined molecular and morphological analyses. Nevertheless, further studies are needed before formulating conclusions about the evolution of features within the sabellid radiation. Taxonomy The diagnoses for Sabellidae and each of its genera are given below. Numbers of currently accepted nominal species are also given, but some genera still require a deep taxonomic revision. When numbers are tentative, it has been indicated with an asterisk. A relative measure of the size of the specimens is given in the diagnoses: forms less than 1 cm long were considered short bodied, medium-sized taxa are between 1 and 5 cm long, and those longer than 5 cm are considered herein as long bodied. Genera diagnoses Family Sabellidae Latreille, 1825 Type genus: Sabella Linnaeus, 1767 Diagnosis: Tube-dwelling annelids inhabiting mucous tubes, frequently with particles of sediment embedded (Glomerula represents the exception, with calcified tubes). Radiolar crown with two basal lobes fused dorsally, supported by an internal structure of vacuolated cells arranged in at least two rows along radiolar axes (except for Caobangia, which has a single row). Radiolar crown with dorsal and ventral lips, vacuolated cells frequently also supporting dorsal lips. Radiolar flanges, basal membrane, basal flanges, and dorsal and ventral radiolar appendages present or not. Peristomium subdivided into two rings; posterior peristomial ring usually

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Fig. 7.4.6.19: Phylogenetic hypotheses within Sabellidae based on (A) morphological and molecular data (fragments of the nuclear ribosomal RNA genes 18S and 28S, and the mitochondrial gene 16S) and (B) morphological data. A, modified from Capa et al. 2011a; B, modified from Nogueira et al. 2010.

forming a collar around base of radiolar crown. Notopodia from segment 1, neuropodia from segment 2. Thoracic notopodia with chaetae arranged in superior and inferior groups. Thoracic neuropodia with acicular or avicular uncini, sometimes with companion chaetae. Abdominal notopodia with avicular uncini, or as rasp-shaped plates. Abdominal neuropodia with neurochaetae arranged in anterior and posterior groups. Compound eyes or eyespots frequently present on radioles, peristomium, body segments (interramal eyespots), and pygidium. Pygidial cirrus absent or present. Acromegalomma Gil and Nishi, 2017 Type species: Branchiomma köllikeri Claparède, 1870, a junior synonym of Sabella lanigera Grube, 1846 (34 species) Diagnosis: Medium- to large-sized sabellids, with variable number of pairs of radioles in semicircular to circular radiolar lobes, each radiole with numerous rows of vacuolated cells (up to 30 cells). Basal membrane,

radiolar flanges and basal flanges all absent. One to several radioles with a single, sessile, compound radiolar eye, situated subdistally on inner margin of radiole (feature unique among sabellids; Figs. 7.4.6.1 A, 7.4.6.2 E, F, and 7.4.6.12 E, F). Dorsal lips with radiolar appendages, pinnular appendages absent or present; ventral radiolar appendages absent, ventral lips and parallel lamellae both present, ventral sacs usually present, inside radiolar crown; keel and caruncle present in some species (Fig. 7.4.6.4 G, H). Anterior peristomial ring low, of even height. Posterior peristomial ring collar with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with at least eight chaetigers, abdomen with variable number. Glandular ridge on chaetigers 2 to 3 sometimes present. Ventral shields present. Interramal eyespots usually present. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae broadly



hooded, classified into three types: type A (distal end narrowing abruptly), type B (progressively tapering to tip), and type C (emergent shaft thick, short and distally rounded). Thoracic uncini avicular, with several rows of similar sized teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae with asymmetrical hood, teardrop shaped, with elongate tip (Fig. 7.4.6.8 G). Abdominal uncini similar to ­thoracic ones. Abdominal neurochaetae as broadly or narrowly hooded chaetae in both groups. Pygidial eyespots absent. Pygidial cirrus absent. Main references: Fitzhugh (1989, 2003), Tovar-Hernández and Salazar-Vallejo (2008), Capa and Murray (2009), and Tovar-Hernández and Carrera-Parra (2011). Amphicorina Claparède, 1864 Type species: Fabricia (Amphicorina) armandi Claparède, 1864, by subsequent monotypy (Rouse 1994) (40 species) Diagnosis: Short-bodied sabellids, with two to five pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane and radiolar flanges present, basal flanges absent. Radiolar eyes absent. Dorsal radiolar and pinnular appendages both absent; one to two pairs of ventral radiolar appendages. Ventral lips present; parallel lamellae and ventral sacs absent. Anterior peristomial ring with ventral lobe entire or bifurcated. Posterior peristomial ring collar with middorsal gap and straight, crenulated, or with small ventral notch on anterior margin. Peristomial vascular loops absent. Peristomial eyespots present. Thorax with eight chaetigers, abdomen with 4 to 15. Glandular ridge on chaetiger 2 present, not always conspicuous. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior thoracic notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae as bayonet chaetae. Thoracic uncini acicular, with teeth above main fang arranged in transverse rows, progressively shorter, or with at least one distinctly larger tooth in proximal row; neuropodial companion chaetae absent. Abdominal uncini with raspshaped dentition, main fang present, handle absent and poorly developed, squared to rectangular breast. Abdominal neurochaetae as needlelike chaetae, on anterior group, and modified, elongate, narrowly hooded chaetae, on posterior one. Pygidium with eyespots. Pygidial cirrus absent. Main references: Fitzhugh (1989), Rouse (1994) (as Oriopsis Caullery and Mesnil, 1896), Giangrande et al. (1999), and Yoshihara et al. (2012). Amphiglena Claparède, 1864 Type species: Amphicora mediterranea Leydig, 1851, designated by Bush (1905) (14 species)

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Diagnosis: Short-bodied sabellids (Fig. 7.4.6.1 E), with four to eight pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane and radiolar flanges present; dorsal basal flanges absent, ventral basal flanges present. Radiolar eyes absent. Dorsal lips with radiolar appendages, pinnular appendages absent; ventral radiolar appendages absent. Ventral lips, parallel lamellae and ventral sacs absent. Anterior peristomial ring low, of even height. Posterior peristomial collar absent (Fig. 7.4.6.1 E). Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with seven to nine segments; abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, broadly hooded; inferior thoracic notochaetae paleate. Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, developed breast and medium to long-sized handle; neuropodial companion chaetae with distally elongated teardrop-shaped hood. Abdominal uncini avicular, with several rows of progressively shorter teeth, developed breast, and short to medium-sized handle. Abdominal neurochaetae of anterior group as elongate, broadly hooded chaetae, posterior group of abdominal neurochaetae absent. ­ Pygidium with eyespots. Pygidial cirrus absent. Main references: Fitzhugh (1989), Rouse and Gambi (1997), ­ Capa and Rouse (2007) and Tilic et al. (2019). Anamobaea Krøyer, 1856 Type species: Anamobaea orstedi Krøyer, 1856, by monotypy (two species) Diagnosis: Medium-sized sabellids, with numerous pairs of radioles in semicircular radiolar lobes, each radiole with at least four rows of vacuolated cells. Radiolar crown with elongate basal lobes; basal membrane present, radiolar flanges absent, dorsal and ventral basal flanges present. Radiolar eyes as numerous eyespots arranged in longitudinal rows in restricted area of radioles. Dorsal lips with radiolar and pinnular appendages; ventral radiolar appendages absent. Ventral lips and parallel lamellae present; ventral sacs inside the radiolar crown. Anterior peristomial ring low, of even height. Posterior peristomial ring collar present, with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision and short ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax and abdomen with numerous chaetigers, each more than 30 (such long thorax is unique among sabellids). Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae as superior notochaetae of following chaetigers, spinelike; inferior

192 

 7.4 Sedentaria: Sabellida/Spionida

thoracic notochaetae paleate. Thoracic uncini avicular, with similar in size teeth arranged transverse rows above main fang, developed breast, and medium-sized handle; neuropodial companion chaetae with roughly symmetrical hood and gently tapering distal end. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae paleate in anterior group, and modified, elongate, narrowly hooded chaetae in posterior one. Presence of pygidial eyespots unknown. Pygidial cirrus absent. Main references: Fitzhugh (1989) and Tovar-Hernández and Salazar-Vallejo (2006). Aracia Nogueira, Fitzhugh, and Rossi, 2010 Type species: Kirkia heterobranchiata Nogueira, López, and Rossi, 2004, by original designation (three species) Diagnosis: Short-bodied sabellids, with four to six pairs of  radioles in semicircular radiolar lobes, each radiole with  two rows of vacuolated cells. Basal membrane, radiolar flanges, and basal flanges absent. Radiolar eyes absent. Dorsal lips low and rounded, dorsal radiolar and pinnular appendages absent; ventral radiolar appendages present. Ventral lips present; parallel lamellae and ventral sacs absent. Anterior peristomial ring low, of even height. Posterior peristomial ring collar with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots present. Thorax with eight chaetigers, abdomen with variable number. ­Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae paleate. Thoracic uncini avicular, with short handle, developed breast and several rows of progressively shorter teeth above main fang; neuropodial companion chaetae with denticulate head and long, gently tapering roughly symmetrical tip. Abdominal uncini similar to the thoracic ones. Abdominal neurochaetae of anterior group as elongate, broadly hooded chaetae, posterior group with modified, elongate, narrowly hooded chaetae. Pygidial eyespots present in juveniles. Pygidial cirrus absent. Main references: Nogueira et al. (2004) and Tovar-Hernández (2014). Bispira Krøyer, 1856 Type species: Amphitrite volutacornis Montagu, 1804, designated by Bush (1905) (23 species) Diagnosis: Medium- to large-sized sabellids, with numerous pairs of radioles in semicircular (Fig. 7.4.6.16 D) to spiral radiolar lobes; each with at least four rows of vacuolated cells. Basal membrane and radiolar flanges present, basal flanges absent. Paired compound eyes

usually present along radioles (Fig. 7.4.6.3 C). Dorsal lips with radiolar and pinnular appendages (Fig. 7.4.6.2  C); ventral radiolar appendages absent. Ventral lips and parallel lamellae present; ventral sacs outside radiolar crown (Fig. 7.4.6.3 E). Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar present, with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with at least eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots present. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae spinelike (Fig. 7.4.6.6 B). Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, developed breast and medium-sized handle; neuropodial ­companion chaetae with asymmetrical hood and gently tapering tip. Abdominal uncini similar to the thoracic ones. Abdominal neurochaetae of anterior group in C-shaped to spiral arrangement, chaetae of posterior group enclosed in the arc; spinelike chaetae in anterior group and modified, elongate, narrowly hooded chaetae, in posterior one. Pygidium with eyespots. Pygidial cirrus absent. Main references: Fitzhugh (1989), Knight-Jones and Perkins (1998), Capa (2008) and Cepeda and Lattig (2017). Branchiomma Kölliker, 1858 Type species: Amphitrite bombyx Dalyell, 1853, by monotypy (Fitzhugh 1989) (30 species) Diagnosis: Short- to large-sized sabellids (Figs. 7.4.6.12 A and 7.4.6.16 E), with variable number of pairs of radioles in semicircular to one-whorled radiolar lobes, each radiole with at least four rows of vacuolated cells. Basal membrane present, radiolar flanges and basal flanges absent. Paired stylodes present on outer radiolar surface (feature unique among sabellids), variable in shape. Paired compound radiolar eyes present along radioles (Figs. 7.4.6.3 D and 7.4.6.9 B, C). Dorsal lips with radiolar appendages (Figs. 7.4.6.2 B and 7.4.6.3 H), pinnular appendages present or absent; ventral radiolar appendages absent. Ventral lips and parallel lamellae present; ventral sacs outside radiolar crown (Fig. 7.4.6.3 G). Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar with middorsal gap, fused or not to faecal grove laterally, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots may be present in juveniles and smaller species. Thorax usually with eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots present. Collar chaetae similar to superior notochaetae of following chaetigers,



elongate, narrowly hooded; inferior thoracic notochaetae spinelike. Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae absent. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae of anterior group spinelike chaetae in C-shaped arrangement, chaetae of posterior group enclosed in the arc, elongate or modified, elongate, narrowly hooded chaetae, on anterior and posterior abdominal chaetigers, respectively. Pygidium frequently with eyespots. Pygidial cirrus absent. Main references: Fitzhugh (1989), Knight-Jones et  al. (1991), Knight-Jones (1994), Nogueira et al. (2006), and Tovar-Hernández and Knight-Jones (2006). Caobangia Giard, 1893 Type species: Caobangia billeti Giard, 1893, by monotypy (seven species) Diagnosis: Short-sized sabellids (Fig. 7.4.6.1 H), a few millimeters long, with three pairs of radioles in semicircular radiolar lobes, each with single row of vacuolated cells (unique feature among sabellids). Basal membrane, radiolar flanges, and basal flanges all absent. Radiolar eyes absent. Dorsal lips, ventral lips, ventral sacs, and parallel lamellae all absent. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar absent. Peristomial vascular loops absent. Presence of peristomial eyespots unknown. Thorax with seven chaetigers, abdomen with numerous segments. Glandular ridge on chaetiger 2 absent. Ventral shields inconspicuous. Interramal eyespots absent. Collar chaetae unknown, superior thoracic notochaetae of following chaetigers, elongate, narrowly hooded, inferior thoracic notochaetae from chaetiger  3, narrowly hooded. Neuropodial uncini only present on chaetiger 2, as palmate hooks (Fig. 7.4.6.8 E). Abdominal uncini avicular, with rasp-shaped crest, developed tapered breast and short handle; posterior uncini with elongate neck between breast and main fang. Abdominal neurochaetae as elongate, narrowly hooded chaetae to short, broadly hooded, in single group, probably the anterior one. Pygidial eyespots absent. Pygidial cirrus absent. Main references: Jones (1974) and Fitzhugh (1989). Chone Krøyer, 1856 Type species: Chone infundibuliformis Krøyer, 1856, by original designation (12 species) Diagnosis: Large-bodied sabellids, with numerous pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane and radiolar flanges present, basal flanges absent. Radiolar eyes absent. Dorsal lips rounded, radiolar appendages absent, dorsal pinnular appendages present; two to eight pairs of

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ventral radiolar appendages. Ventral lips present, ventral sacs, and parallel lamellae absent. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar present, usually with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with eight chaetigers, abdomen with variable number. Narrow glandular ridge on chaetiger 2. Ventral shields absent. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae as bayonet chaetae and paleate. Thoracic uncini acicular, with teeth above the main fang of different sizes arranged in transverse rows, medial tooth of basal row larger, hood present, handle long; neuropodial companion chaetae absent. Abdominal uncini with squared to rectangular breast, handle absent, few rows of teeth above main fang; uncini progressively larger from dorsal to ventral edges of tori. Abdominal neurochaetae of anterior group as elongate, narrowly hooded chaetae, on anterior abdominal chaetigers, and modified, elongate, narrowly hooded chaetae in posterior group of anterior abdominal chaetigers, and both groups of posterior segments. Pygidium with eyespots. Pygidial cirrus absent. Main references: Tovar-Hernández and SosaRodríguez (2006) and Tovar-Hernández (2008). Claviramus Fitzhugh, 2002 Type species: Sabella candela Grube, 1863, by original designation (three species) Diagnosis: Short-sized sabellids, with variable number of pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane absent, radiolar flanges only present at radiolar tips, expanded and cup shaped (feature unique among sabellids), basal flanges absent; radiolar eyes absent. Dorsal lips with radiolar appendages, pinnular appendages apparently absent; ventral radiolar appendages present, few to several pairs. Ventral lips present, ventral sacs, and parallel lamellae absent. Anterior peristomial ring with broad, triangular, ventral lobe. Posterior peristomial ring collar with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots may be present. Thorax with eight chaetigers, abdomen with 9 to 12. Glandular ridge on chaetiger 2 present or not. Ventral shields present on thorax, absent on abdomen. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae broadly hooded, or narrowly and broadly hooded. Thoracic uncini acicular, with short teeth above main fang arranged in transverse rows, hood present, handle

194 

 7.4 Sedentaria: Sabellida/Spionida

long; neuropodial companion chaetae absent. Abdominal uncini avicular, with distinctly short handle, developed squared to rectangular breast, and several transverse rows of short teeth above main fang. Abdominal neurochaetae in single group of narrowly hooded chaetae. Pygidium with eyespots present in at least some species. Pygidial cirrus absent. Main reference: Fitzhugh (2002). Desdemona Banse, 1957 Type species: Desdemona ornata Banse, 1957, by original designation (three species) Diagnosis: Short-bodied sabellids, with three pairs of radioles (Fig. 7.4.6.1 F, G) in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane present, radiolar flanges and basal flanges both absent. Radiolar eyes absent. Dorsal radiolar and pinnular appendages both absent; one pair of ventral radiolar appendages. Ventral lips present, ventral sacs, and parallel both absent. Anterior peristomial ring with wide ventral lobe. Posterior peristomial ring collar absent. Peristomial vascular loops absent. Peristomial eyespots present. Thorax and abdomen each with eight chaetigers. Glandular ridge on chaetiger 2 present, not always conspicuous. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, narrowly hooded; inferior thoracic notochaetae as bayonet chaetae. Thoracic uncini acicular, with similarly sized teeth above main fang arranged in transverse rows, hood absent, handle long; neuropodial companion chaetae absent. Abdominal uncini raspshaped, main fang present, handle absent, and poorly developed breast. Abdominal neurochaetae as single group of modified, elongate, narrowly hooded chaetae. Pygidium with eyespots. Pygidial cirrus absent (Fig. 7.4.6.1 F, G). Main references: Banse (1957), Hutchings and Murray (1984), and Fitzhugh (1989). Dialychone Claparède, 1870 Type species: Dialychone acustica Claparède, 1870, by original designation (18 species) Diagnosis: Mid- to large-sized sabellids, with variable number of pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane and radiolar both present, basal flanges absent. Radiolar eyes absent. Dorsal lips elongate, ­radiolar and pinnular appendages both absent; ventral radiolar appendages present. Ventral lips present, ventral sacs and parallel both absent. Anterior peristomial ring with triangular or bilobed ventral lobe. Posterior peristomial ring collar present, low, with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops

absent. Peristomial eyespots absent or present. Thorax with eight chaetigers, abdomen with variable number. Glandular ridge present on chaetiger 2, in some species also on other posterior thoracic and anterior abdominal segments. Ventral shields absent. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae as bayonet chaetae and paleate. Thoracic uncini acicular with teeth progressively shorter, arranged in transverse rows above main fang, hood present, handle long; neuropodial companion chaetae absent. Abdominal uncini with breast squared to rectangular, handle absent, main fang with several rows of similarly sized teeth on top; uncini progressively larger from dorsal to ventral edges of tori. Abdominal neurochaetae as elongate, narrowly hooded chaetae. Posterior body with simple prepygidial depression. Pygidium with eyespots. Pygidial cirrus sometimes present. Main reference: Tovar-Hernández (2008). Euchone Malmgren, 1866 Type species: Sabella analis Krøyer, 1856, designated by Bush (1905) (36 species) Diagnosis: Short- to large-bodied sabellids, with several pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane and radiolar both usually present, basal flanges absent. Radiolar eyes absent. Dorsal lips with radiolar appendages, dorsal pinnular appendages absent or present; two to six pairs of ventral radiolar appendages. Ventral lips present, ventral sacs and parallel both absent. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops present in E. analis. Peristomial eyespots absent. Thorax with eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 present. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae as bayonet chaetae and paleate. Thoracic uncini acicular (Fig. 7.4.6.7 F), with similar sized teeth above main fang arranged in transverse rows, hood present, handle long; neuropodial companion chaetae absent. Anterior abdominal uncini with roughly triangular breast, or squared to rectangular (Fig. 7.4.6.7 I), handle absent, main fang with several rows of similarly sized teeth on top; posterior abdominal uncini, especially on prepygidial depression, with rasp-shaped dentition (covering the entire length of main fang) or transitional between few rows of teeth (covering partially main fang) and rasp shaped.



Abdominal neurochaetae of anterior group as elongate, narrowly hooded chaetae on anterior abdominal chaetigers; modified, elongate, narrowly hooded chaetae on posterior group of anterior abdominal chaetigers and both groups of posterior segments. Posterior body with prepygidial depression (Fig. 7.4.6.5 F, G) occupying at least three chaetigers, usually with lateral wings. Pygidial eyespots absent. Pygidial cirrus absent (Fig. 7.4.6.5 F, G). Main references: Banse (1970, 1972), Fitzhugh (1989), Cochrane (2003), Bick and Randel (2005), Giangrande and Licciano (2006), and Capa and Murray (2015a). Euchoneira Licciano, Giangrande, and Gambi, 2009 Type species: Euchoneira knoxi Licciano, Giangrande, and Gambi, 2009, by original designation (monotypic) Diagnosis: Large species, with several pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane, radiolar flanges, and basal flanges all absent. Radiolar eyes absent. Dorsal lips without radiolar and pinnular appendages; ventral radiolar appendages present. Ventral lips present, ventral sacs and parallel both absent. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar with wide middorsal gap, dorsal margins entire (dorsal gap absent), with short midventral incision, ventral lappets absent. Peristomial vascular loops absent. Persitomial eyespots absent. Thorax with eight chaetigers, large number of chaetigers in abdominal region. Glandular ridge on chaetiger 2 present. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, narrowly hooded; inferior thoracic notochaetae as bayonet chaetae and broadly hooded. Thoracic uncini acicular with teeth progressively shorter, arranged on transverse rows above main fang, hood present, handle long; neuropodial companion chaetae absent. Abdominal notopodia with avicular uncini with well-developed handle, squared to rectangular breast, rows of teeth over the main fang similar sized. Abdominal neuropodial fascicles with transverse rows of narrowly hooded chaetae in both groups. Prepygidial depression present, well developed, with lateral wings. Pygidial eyespots absent. Pygidial cirrus absent. Main reference: Licciano et al. (2009). Eudistylia Bush, 1905 Type species: Sabella vancouveri Kinberg, 1866, senior synonym of Eudistylia gigantea Bush, 1905, by original designation (six species*) Diagnosis: Medium- to large-sized sabellids, with numerous pairs of radioles in spiraled radiolar lobes, each radiole with at least four rows of vacuolated cells; larger specimens sometimes with dichotomously

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branching radioles (feature unique among sabellids). Basal membrane, radiolar flanges, and basal flanges absent. Unpaired compound radiolar eyes present on all radioles except for ventralmost pair. Dorsal lips with radiolar and pinnular appendages; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs inside the radiolar crown. ­Anterior peristomial ring low, of even height. Posterior peristomial ring collar present, with wide middorsal ­ gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax usually with eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior ­ horacic uncini avicular, thoracic notochaetae paleate. T with several rows of progressively shorter teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae with roughly symmetrical hood and gently tapering tip. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae of both groups elongate, broadly hooded chaetae. Pygidial eyespots may be present. Pygidial cirrus absent. Main references: Bush (1905) and Fitzhugh (1989). Euratella Chamberlin, 1919 Type species: Laonome salmacidis Claparède, 1870, by monotypy (monotypic*) Diagnosis: Radioles in semicircular radiolar lobes. Basal membrane present. Radiolar eyes present. Other radiolar structures unknown. Posterior peristomial collar reduced or absent. Thorax with eight chaetigers, abdomen with variable number. Superior thoracic notochaetae narrowly hooded, inferior thoracic notochaetae broadly hooded (probably paleate). Thoracic uncini avicular with short handle; neuropodial companion chaetae absent. Abdominal uncini similar to thoracic ones. Other features not mentioned herein unknown. Main references: Claparède 1870, ­Fauchald 1977. Fabrisabella Hartman, 1969 Type species: Fabrisabella vasculosa Hartman, 1969, by monotypy (two species) Diagnosis: Medium-sized sabellids, with variable number of pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane, radiolar flanges and basal flanges all absent. Radiolar eyes absent. Radiolar crown often incomplete, severed at abscission zone above radiolar bases (feature only shared with Jasmineira). Dorsal lips without radiolar or pinnular appendages; ventral radiolar appendages

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 7.4 Sedentaria: Sabellida/Spionida

present. Ventral lips present, parallel lamellae and ventral sacs both absent. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar with narrow middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops present. Thorax with eight chaetigers, abdomen with variable number. ­Glandular ridge on chaetiger 2 present (Fig. 7.4.6.15 A). Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae paleate. Thoracic uncini acicular, with teeth similar in size arranged in transverse rows above main fang, hood present, handle long; neuropodial companion chaetae absent. Abdominal uncini avicular, with long handle, breast reduced to narrow swelling and distinctly elongate neck between breast and main fang. Abdominal neurochaetae of anterior group as elongate, narrowly hooded chaetae, on anterior abdominal chaetigers, and modified, elongate, narrowly hooded chaetae in posterior group of anterior abdominal chaetigers, and both groups of posterior segments. Pygidial eyespots absent. Pygidial cirrus absent. Main references: Hartman (1969), Fauchald (1972), and Fitzhugh (1989, 2002). Glomerula Nielsen, 1931 Type species: Serpulites gordialis von Schlotheim, 1820 (seven species: one extant, originally described as Calcis­ abella pilosetosa Perkins, 1991, and six extinct) Diagnosis: Short-sized sabellids, with five pairs of radioles in semicircular radiolar lobes, each radiole with four rows of vacuolated cells. Basal membrane and radiolar flanges both present, basal flanges most likely absent. Radiolar eyes absent. Dorsal lips without radiolar or pinnular appendages; ventral radiolar appendages present, ventral lips and parallel lamellae both present, ventral sacs unknown. Peristomial collar with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots present. Thorax with 11 to 15 chaetigers, abdomen with 9 to 12. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, narrowly hooded; inferior thoracic notochaetae broadly hooded. Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, developed breast, handle absent; neuropodial companion chaetae distally hooked. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae as elongate and modified, elongate, narrowly hooded chaetae, in both groups. Pygidial eyes unknown. Pygidial cirrus absent. Main reference: Perkins (1991).

Hypsicomus Grube, 1870 Type species: Sabella stichophthalmos Grube, 1863, subsequent designation by Bush (1905) (monotypic) Diagnosis: Medium-sized sabellids, with numerous pairs of radioles in semicircular radiolar lobes, each radiole with at least four rows of vacuolated cells. Radiolar crown with elongate basal lobes, basal membrane and radiolar flanges both present, basal flanges absent. Numerous radiolar eyespots arranged in longitudinal groups on lateral sides of radioles. Dorsal lips with radiolar appendages, pinnular appendages absent; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs inside radiolar crown. Anterior peristomial ring low, of even height. Posterior peristomial ring collar present, with wide middorsal gap, midventral incision, and ventral lappets. Posterior peristomial ring with two pairs of accessory lamellae, inbetween dorsal collar margins (feature unique among sabellids). Peristomial vascular loops absent. Peristomial eyespots absent. Thorax and abdomen with numerous chaetigers. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, spinelike; inferior thoracic notochaetae paleate. Thoracic uncini avicular, with several rows of minute teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae with roughly symmetrical hood and gently tapering tip. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae of anterior group paleate; posterior group with elongate, narrowly hooded and modified, elongate, narrowly hooded chaetae, on anterior and posterior abdominal segments, respectively. Pygidial eyespots may be present. Pygidial cirrus absent. Main references: Perkins (1984) and Fitzhugh (1989). Jasmineira Langerhans, 1880 Type species: Jasmineira caudata Langerhans, 1880, by monotypy (18 species*) Diagnosis: Short- to medium-sized sabellids, with variable number of pairs of radioles in semicircular radiolar lobes, each with two rows of vacuolated cells. Basal membrane, radiolar flanges and basal flanges all absent. Radiolar eyes absent. Radiolar crown often incomplete, severed at abscission zone above radiolar bases (feature only shared with Fabrisabella). Dorsal lips with or without radiolar appendages, pinnular appendages absent; ventral radiolar appendages present; ventral lips present, ventral sacs and parallel lamellae both absent. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets.



Peristomial vascular loops present is some species. Peristomial eyespots absent. Thorax with eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 present. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae as bayonet chaetae and paleate (Fig. 7.4.6.6 C). Thoracic uncini acicular, teeth similar in size arranged in transverse rows above main fang (Fig. 7.4.6.8 A), hood present; neuropodial companion chaetae absent. Abdominal uncini avicular, with long handle, breast reduced to narrow swelling and distinctly elongate neck between breast and main fang. Abdominal neurochaetae of anterior group as elongate, narrowly hooded chaetae on anterior abdominal chaetigers, and modified, elongate, narrowly hooded chaetae in posterior group of anterior abdominal chaetigers, and both groups of posterior segments. Pygidium without eyespots. Pygidial cirrus absent or present (Fig. 7.4.6.5 H). Main references: Knight-Jones (1983), Fitzhugh (1989, 2002) and Capa and Murray (2015). Laonome Malmgren, 1866 Type species: Laonome kroyeri Malmgren, 1866, by monotypy (10 species) Diagnosis: Medium-sized sabellids with numerous pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane reduced or absent, radiolar flanges and basal flanges both absent. Radiolar eyes absent. Dorsal lips with or without radiolar appendages, pinnular appendages absent; ventral radiolar appendages absent. Ventral lips present, parallel lamellae absent or fused to each other, ventral sacs absent. Peristomial collar present, usually with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thin, white transverse ridge at border between posterior peristomial ring and chaetiger 1 (feature unique among sabellids). Thorax usually with eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded, inferior thoracic notochaetae paleate (Fig. 7.4.6.7 A). Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, developed breast, handle absent (Fig.  7.4.6.7 H); neuropodial companion chaetae usually absent. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae broadly hooded in both groups. Pygidial eyespots absent. Pygidial cirrus absent.

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 197

Main references: Fitzhugh (2002), Capa (2007) and Bick et al. (2018). Myxicola Renier in Meneghini, 1847 Type species: Terebella infundibulum Renier, 1804, designated by Bush (1905) (eight species*) Diagnosis: Medium- to large-sized sabellids, with variable number of pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane and radiolar flanges both present, basal flanges absent. Radiolar eyes absent. Dorsal lips with radiolar appendages, pinnular appendages absent; three to six pairs of ventral radiolar appendages, ventral lips developed, extending dorsoventrally along inner surface of base of radiolar lobes; parallel lamellae and ventral sacs both absent. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar absent (Fig. 7.4.6.3 I). Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with up to eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 present. Ventral shields absent. Interramal eyespots sometimes present. Thoracic notochaetae and abdominal neurochaetae in irregular bundles, arranged in low, circular tori, groups within fascicles not differentiated. Thoracic uncini acicular, with similar sized teeth above main fang in transverse rows, hood absent, long handle; neuropodial companion chaetae absent. Abdominal uncini avicular, handle absent, breast developed, and several rows of shorter teeth above main fang. Abdominal notopodial tori forming almost complete cinctures around body (feature unique among sabellids) with elongate, narrowly hooded chaetae. Pygidial eyespots absent. Pygidial cirrus absent. Main references: Fitzhugh (1989, 2003) Capa et al. (2011), and Capa and Murray (2015). Notaulax Tauber, 1879 Type species: Notaulax rectangulata Levinsen, 1883, by monotypy (20 species) Diagnosis: Medium- to large-sized sabellids, with numerous pairs of radioles in semicircular radiolar lobes, each radiole with at least four rows of vacuolated cells. Radiolar crown with elongate basal lobes (Fig. 7.4.6.4 A, B); basal membrane (Fig. 7.4.6.4 A), radiolar flanges, and dorsal and ventral basal flanges all present (Fig. 7.4.6.4 B). Numerous eyespots arranged in longitudinal rows on lateral sides of radioles (Figs 7.4.6.1 D and 7.4.6.9 A). Dorsal lips with radiolar appendages, pinnular appendages absent; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs inside ­radiolar crown. Anterior peristomial ring low, of even height. Posterior peristomial ring collar with narrow

198 

 7.4 Sedentaria: Sabellida/Spionida

middorsal gap, dorsal margins laterally fused to faecal groove, ventrally entire or with midventral incision and short ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with at least eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae spinelike, arranged in distally oblique longitudinal rows (feature unique among sabellids); superior thoracic notochaetae spinelike, inferior thoracic notochaetae paleate (Fig. 7.4.6.6 F). Thoracic uncini avicular, with several rows of minute and similar sized teeth above main fang, developed breast and ­medium-sized handle; neuropodial companion chaetae with strongly asymmetrical hood stouter on one margin (Fig. 7.4.6.8 F) and thin, elongate tip. Abdominal uncini similar to thoracic ones (Fig. 7.4.6.8 C). Abdominal neurochaetae as paleate and needlelike chaetae, in anterior and posterior groups, respectively. Pygidial eyespots sometimes present. Pygidial cirrus absent. Main references: Perkins (1984) and Fitzhugh (1989). Panoumethus Fitzhugh, 2002 Type species: Panoumethus dubius Fitzhugh, 2002, by monotypy (monotypic) Diagnosis: Medium-sized sabellids, with eight pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane, radiolar flanges and basal flanges all absent. Radiolar eyes absent. Dorsal lips with radiolar appendages, pinnular appendages absent; two to three pairs of ventral radiolar appendages. Ventral lips and parallel lamellae both present, ventral sacs absent. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and short ventral lappets. Peristomial vascular loops absent. Presence of peristomial eyespots unknown. Thorax with eight chaetigers, abdomen with numerous segments. Glandular ridge on chaetiger 2 present. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae paleate. Thoracic uncini acicular, with similar sized teeth above main fang in transverse rows, hood absent, long handle; neuropodial companion chaetae with asymmetrical hood and elongate tip. Abdominal uncini avicular, with several rows of short teeth above main fang, developed breast, and handle reduced to short knob. Abdominal neurochaetae of both groups as narrowly hooded chaetae. Pygidial eyespots absent. Pygidial cirrus absent. Main reference: Fitzhugh (2002).

Panousea Rullier and Amoureux, 1969 Type species: Panousea africana Rullier and Amoureux, 1969, by monotypy (monotypic) Diagnosis: Medium-sized sabellids, with numerous pairs of radioles in semicircular radiolar lobes, each radiole with two rows of vacuolated cells. Basal membrane, radiolar flanges and basal flanges all absent. Radiolar eyes absent. Dorsal lips with radiolar and pinnular appendages; several pairs of ventral radiolar appendages. Ventral lips and parallel lamellae both present, ventral sacs inside the crown. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops absent. Presence of peristomial eyespots unknown. Thorax with eight chaetigers, abdomen with numerous segments. Glandular ridge on chaetiger 2 present. Ventral shields present. Interramal eyespots absent. Collar chaetae in longitudinal, distally oblique rows of narrowly hooded chaetae; superior thoracic notochaetae elongate, narrowly hooded; inferior thoracic notochaetae as bayonet and paleate chaetae. Thoracic uncini acicular, with similar sized teeth above main fang arranged in transverse rows, hood present, handle long; neuropodial companion chaetae with roughly symmetrical hood and elongate tip. Abdominal uncini avicular, with several rows of short teeth above main fang, developed breast and handle reduced to short knob. Abdominal neurochaetae as elongate and modified, elongate, narrowly hooded chaetae. Pygidial eyespots absent. Pygidial cirrus absent. Main references: Rullier and Amoureux (1969) and Fitzhugh (1989). Paradialychone Tovar-Hernández, 2008 Type species: Chone americana Day, 1973, by original designation (15 species) Diagnosis: Medium- to large-sized sabellids, with 3 to 13 pairs of radioles in semicircular radiolar lobes, each with two rows of vacuolated cells. Basal membrane and radiolar flanges both present, basal flanges absent. Radiolar eyes absent. Dorsal lips with radiolar and pinnular appendages; one to six pairs of ventral radiolar appendages. Ventral lips present, parallel lamellae and ventral sacs both absent. Anterior peristomial ring with triangular or bilobed ventral lobe. Posterior peristomial ring collar low, with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent or present. Thorax with eight chaetigers, abdomen with variable number. Ventral shields absent. Glandular ridge on chaetiger



2 present, narrow or laterally broader (Fig. 7.4.6.12 B). Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae as bayonet and paleate chaetae. Thoracic uncini acicular, with transverse rows of progressively shorter teeth above main fang, larger tooth offset from midline in basal row, hood present, handle long; neuropodial companion chaetae absent. Anterior abdominal uncini, with roughly rectangular breast, handle absent, and large tooth at midline of main fang on proximal row, followed by series of smaller teeth; uncini progressively larger from dorsal to ventral edges of tori. Posterior abdominal uncini with hooked breast, handle absent. Abdominal neurochaetae as elongate and modified, elongate, narrowly hooded chaetae. Posterior body segments with prepygidial depression. Pygidium with eyespots. Pygidial cirrus sometimes present. Main references: Tovar-Hernández (2008). Parasabella Bush, 1905 Type species: Parasabella media Bush, 1905, by original designation (28 species) Diagnosis: Medium- to large-sized sabellids, with numerous pairs of radioles in semicircular radiolar lobes, each radiole with at least four rows of vacuolated cells. Basal membrane and radiolar flanges both present, basal flanges absent. Radiolar eyes usually absent. Dorsal lips with radiolar and pinnular appendages; ventral radiolar appendages absent. Ventral lips and parallel lamellae present, ventral sacs inside radiolar crown. Peristomial collar present, with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots may be present in juveniles. Thorax with up to nine chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae broadly hooded (Fig. 7.4.6.6 A). Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, developed breast and mediumsized handle; neuropodial companion chaetae with bulbous hood and elongated tip (feature unique among sabellids; Fig. 7.4.6.8 H). Abdominal uncini similar to thoracic ones. Abdominal neurochaetae elongate and modified, elongate, narrowly hooded chaetae, the latter present in posterior group of posterior abdominal segments. Pygidial eyespots may be present in juveniles. Pygidial cirrus absent. Main references: Perkins (1984), Fitzhugh (1989), Capa and Murray (2015b) and Tovar-Hernández et al., (2017).

7.4.6 Sabellidae Latreille, 1825 

 199

Perkinsiana Knight-Jones, 1983 Type species: Sabella rubra Langerhans, 1880, by original designation (19 species) Diagnosis: Short- to medium-sized sabellids, with variable number of pairs of radioles in semicircular radiolar lobes, each with at least two rows of vacuolated cells, frequently four or more rows. Basal membrane and radiolar flanges both present or absent, basal flanges absent. Radiolar eyes absent. Dorsal lips usually with both radiolar and pinnular appendages; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs absent. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots may be present in juveniles. First segment enlarged (about twice length of following ones). Thorax with eight chaetigers, abdomen with variable number. ­Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded, inferior thoracic notochaetae paleate. Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, developed breast and handle variable in length; neuropodial companion chaetae with roughly symmetrical hood and gently tapering tip. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae fascicles with transverse rows of broadly hooded chaetae in anterior group; posterior group either with elongate, broadly hooded chaetae, on anterior abdominal segments, or elongate, narrowly hooded chaetae, on posterior abdominal chaetigers. Pygidial eyespots sometimes present. Pygidial cirrus absent. Main references: Knight-Jones (1983), Fitzhugh (1989), Capa (2007), and Tovar-Hernández et al. (2012). Potamethus Chamberlin, 1919 Type species: Potamis spathiferus Ehlers, 1887, by monotypy (9 species*) Diagnosis: Medium-sized sabellids, with variable number of pairs of radioles in semicircular radiolar lobes, each with at least four rows of vacuolated cells (one species with a single row). Basal membrane present, radiolar flanges and basal flanges both absent. Radiolar eyes absent. Dorsal lips with radiolar appendages, pinnular appendages absent; ventral radiolar appendages absent, ventral lips, parallel lamellae and ventral sacs all present, the latter inside radiolar crown. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar of variable morphology. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with eight chaetigers, abdomen with variable number. Glandular

200 

 7.4 Sedentaria: Sabellida/Spionida

ridge on chaetiger 2 present. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae paleate. Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, breast developed or not, and medium-sized handle; neuropodial companion chaetae present, with long handle and distal asymmetrical tip. Abdominal uncini avicular, with several rows of short teeth above main fang, reduced breast, distinctly elongate neck between breast and main fang, and elongate handle. Abdominal neurochaetae as elongate, narrowly hooded chaetae, in anterior group, and modified, elongate, narrowly hooded chaetae, in posterior group. Pygidial eyespots absent. Pygidial cirrus absent. Main references: Knight-Jones (1983) and Fitzhugh (1989). Potamilla Malmgren, 1866 Type species: Sabella neglecta Sars, 1850, designated by Bush (1905) (18 species*) Diagnosis: Medium-sized sabellids with numerous pairs of radioles in semicircular radiolar lobes, each with at least four rows of vacuolated cells. Basal membrane present, radiolar flanges and basal flanges both absent. Radiolar eyes absent. Dorsal lips without radiolar appendages, pinnular appendages present; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs inside radiolar crown. Anterior peristomial ring low, of even height. Posterior peristomial ring collar with narrow middorsal gap, dorsal margins fused laterally to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax usually with eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae broadly hooded. Thoracic uncini avicular, with several rows of similar sized teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae with roughly symmetrical hood and gently tapering tip. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae as elongate, broadly hooded chaetae, in both groups. Pygidial eyespots probably present in juveniles. Pygidial cirrus absent. Main references: Knight-Jones (1983) and Fitzhugh (1989). Potaspina Hartman, 1969 Type species: Potaspina pacifica Hartman, 1969, by monotypy (two species)

Diagnosis: Short- to medium-sized sabellids, with numerous pairs of radioles in semicircular radiolar lobes, each with at least four rows of vacuolated cells. Basal membrane present or absent, radiolar flanges and dorsal basal flanges both absent, ventral flanges present or absent. Radiolar eyes absent. Dorsal lips with both radiolar and pinnular appendages; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs probably absent. Anterior peristomial ring low, of even height. Posterior peristomial ring collar with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Presence of peristomial eyespots unknown. Thorax with 8 to 9 chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 probably absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae paleate. Anterior thoracic uncini avicular, with several rows of similar sized teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae with denticulate head and elongate, gently tapering symmetrical or ­asymmetrical tip; neurochaetae of last three thoracic chaetigers as subdistally bent, distally tapering spines replacing uncini (feature unique among sabellids), lacking companion chaetae. Abdominal uncini avicular, with short- to medium-sized handle, poorly developed breast and elongate neck between breast and main fang, with transverse rows of similar sized teeth above main fang. Abdominal neurochaetae of both groups elongate, broadly hooded chaetae. Pygidial eyespots unknown. Pygidial cirrus absent. Main references: Fitzhugh (1989) and Capa (2007). Pseudobranchiomma Jones, 1962 Type species: Pseudobranchiomma emersoni Jones, 1962, by monotypy (17 species) Diagnosis: Short- to medium-sized sabellids, with variable number of pairs of radioles in semicircular radiolar lobes, each with at least four rows of vacuolated cells. Basal membrane and radiolar flanges both present, the later usually with lateral serrations along some extension; basal flanges absent. Dorsal lips with radiolar appendages, pinnular appendages absent; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs outside radiolar crown. Peristomial collar with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots may be present in juveniles. Thorax with 4 to 14 chaetigers, usually less than eight, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal



eyespots present. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae spinelike. Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, developed breast and shortsized handle; neuropodial companion chaetae absent. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae of anterior group spinelike chaetae, in arc or spiral arrangement, and modified, elongate, narrowly hooded chaetae, enclosed in the arc, in posterior group. Pygidium with eyespots. Pygidial cirrus absent. Main references: Jones (1962), Fitzhugh (1989), Nogueira and Knight-Jones (2002), Knight-Jones and Giangrande (2003), Nogueira et  al. (2006), Tovar-Hernández and Dean (2014) and Capa and Murray (2015a), and Çinar and Giangrande (2018). Pseudopotamilla Bush, 1905 Type species: Amphitrite reniformis Bruguière, 1789, by original designation (16 species*) Diagnosis: Medium-sized sabellids with numerous pairs of radioles in semicircular radiolar lobes, each with at least four rows of vacuolated cells. Basal membrane, radiolar flanges and basal flanges all absent. One to several unpaired compound radiolar eyes bulging along outer radiolar margins, on at least some dorsal radioles, except for dorsalmost pair (Fig. 7.4.6.9 D). Dorsal lips with both radiolar and pinnular appendages; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs inside radiolar crown. Anterior peristomial ring low, of even height. Posterior peristomial ring collar present, with narrow middorsal gap, dorsal margins laterally fused to faecal groove, with a midventral incision and short ventral lappets, and usually also with dorsolateral incisions. Peristomial vascular loops absent. Peristomial eyespots sometimes present. Thorax and abdomen with variable number of chaetigers. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae paleate. Thoracic uncini avicular, with several rows of similar sized teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae with asymmetrical hood and gently tapering tip. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae of both groups as elongate, broadly hooded chaetae. Pygidial eyespots sometimes present. Pygidial cirrus absent. Main references: Knight-Jones (1983), Fitzhugh (1989), Capa (2007) and Tovar-Hernández et al. (2017).

7.4.6 Sabellidae Latreille, 1825 

 201

Sabella Linnaeus, 1767 Type species: Sabella pavonina Savigny, 1822, designated by Bush, 1905 (three species) Diagnosis: Medium- to large-sized sabellids, with numerous pairs of radioles with radiolar lobes in semicircles to spiraled arrangement (Figs. 7.4.6.3 A and 7.4.6.16 A), each with at least four rows of vacuolated cells. Basal membrane present (Fig. 7.4.6.3 B), radiolar flanges and basal flanges both absent. Radiolar eyes absent. Dorsal radiolar appendages present, pinnular appendages absent; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs outside radiolar crown (Fig. 7.4.6.3 F). Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar present, with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with at least eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots present. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded, inferior thoracic notochaetae spinelike. Thoracic uncini avicular, with several rows of similar sized teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae present, with gently tapering asymmetrical tip. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae of anterior group as spinelike chaetae, in spiraled arrangement, posterior group absent on anterior abdominal segments, as modified, elongate, narrowly hooded chaetae on posterior segments. Pygidial eyespots present. Pygidial cirrus absent. Main references: Fitzhugh (1989) and Knight-Jones and Perkins (1998). Sabellastarte Krøyer, 1856 Type species: Sabellastarte indica Savigny, 1822, designated by Bush (1905) (eight species) Diagnosis: Large-sized sabellids, with numerous pairs of radioles in semicircular to spiraled arrangement (Fig. 7.4.6.16 B), each with at least four rows of vacuolated cells. Basal membrane present, radiolar flanges absent, dorsal basal flanges present, ventral flanges absent. Radiolar eyes absent. Dorsal radiolar ­appendages present, pinnular appendages absent; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs inside radiolar crown. Anterior peristomial ring with narrow ventral lobe. Posterior peristomial ring collar with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with seven to nine

202 

 7.4 Sedentaria: Sabellida/Spionida

chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots present. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded (Fig. 7.4.6.7 E); inferior thoracic notochaetae spinelike (Fig. 7.4.6.7 D). Thoracic uncini avicular, with several rows of similar sized teeth above main fang, developed breast and medium-sized handle (Fig. 7.4.6.8 B); neuropodial companion chaetae absent. Abdominal uncini similar to thoracic ones (Fig. 7.4.6.7 G). Abdominal neurochaetae of anterior group spinelike, in a C-shaped or spiraled arrangement, posterior group with modified, elongate, narrowly hooded, and needlelike chaetae, on anterior and posterior abdominal segments, respectively. Pygidial eyespots present. Pygidial cirrus absent. Main references: Fitzhugh (1989) and Knight-Jones and Mackie (2003). Sabellomma Nogueira, Fitzhugh, and Rossi, 2010 Type species: Parasabella minuta Treadwell, 1941, by original designation (four species) Diagnosis: Short- to medium-sized sabellids with four to nine pairs of radioles in semicircular radiolar lobes, each with four rows of vacuolated cells. Basal membrane present, radiolar flanges and basal flanges both absent. Radiolar eyes irregularly distributed along radioles. Dorsal radiolar appendages present, pinnular appendages absent or present; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs outside radiolar crown. Peristomial collar present, with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax usually with four to five chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots present. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae paleate. ­Thoracic uncini avicular, with several rows of progressively shorter teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae with slightly asymmetrical hood and gently tapering tip. Abdominal uncini similar to thoracic ones; abdominal neurochaetae of both groups as elongate, narrowly hooded chaetae. Pygidium with eyespots. Pygidial cirrus absent. Main reference: Nogueira et al. (2010) Capa and Murray (2015b). Sabellonga Hartman, 1969 Type species: Sabellonga disjuncta Hartman, 1969, by monotypy (monotypic)

Diagnosis: Medium-sized sabellids known from a single complete specimen missing crown (Fitzhugh 1989). Ventral lips, parallel lamellae and ventral sacs all ­apparently present. Anterior peristomial ring not visible. Peristomial collar present, with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Thorax with 13 chaetigers, abdomen with many chaetigers. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae paleate. Thoracic uncini avicular, with several rows of similar sized teeth above main fang, developed breast and medium-sized handle; neuropodial companion chaetae with roughly symmetrical hood and gently tapering tip. Most abdominal uncini similar to thoracic ones, last five notopodia with falcate acicular spines replacing uncini (feature unique among sabellids); abdominal neurochaetae of both groups as elongate, broadly hooded chaetae. Pygidial eyespots probably present. Pygidial cirrus absent. Main reference: Fitzhugh (1989). Schizobranchia Bush, 1905 Type species: Schizobranchia insignis Bush, 1905, by ­original designation (three species) Diagnosis: Medium- to large-sized sabellids, with numerous pairs of radioles in semicircular radiolar lobes, each with at least four rows of vacuolated cells; some radioles branched (feature unique among sabellids). Basal membrane and radiolar flanges both absent, dorsal basal flanges present, ventral flanges absent. Unpaired compound eyes along radioles on all but ventralmost pair. Dorsal lips with both radiolar and pinnular appendages; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs inside radiolar crown. Anterior peristomial ring low, of even height. Posterior peristomial ring collar with narrow m ­ iddorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and short ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax usually with eight chaetigers, abdomen with variable number. Ventral shields present. Glandular ridge on chaetiger 2 absent. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded, inferior thoracic n ­ otochaetae paleate. Thoracic uncini avicular, with several rows of similar sized teeth above main fang, developed breast, and medium-sized handle; neuropodial companion chaetae with roughly symmetrical hood and gently tapering tip. Abdominal uncini similar to thoracic ones. Abdominal neurochaetae

7.4.6 Sabellidae Latreille, 1825 



of both groups as elongate, broadly hooded chaetae. Pygidial eyespots sometimes present. Pygidial cirrus absent. Main references: Bush (1905) and Fitzhugh (1989). Stylomma Knight-Jones, 1997 Type species: Sabella palmata de Quatrefages, 1866, by monotypy (two species) Diagnosis: Medium-sized sabellids, with numerous pairs of radioles in semicircular radiolar lobes, each with more than four rows of vacuolated cells. Basal membrane and radiolar flanges both present, dorsal basal flanges with anterior joint (feature unique among sabellids), ventral flanges absent; large unpaired compound radiolar eyes on inner surface of tip of radioles or close to it (unique among sabellids) or paired eyes along lateral sides of radioles. Dorsal radiolar appendages present, pinnular appendages absent; ventral radiolar appendages absent. Ventral lips and parallel lamellae both present, ventral sacs inside radiolar crown. Anterior peristomial ring low, of even height. Posterior peristomial ring collar with wide middorsal gap, midventral incision, and ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with eight chaetigers, abdomen with variable number. Glandular ridge on chaetiger 2 absent. Ventral shields present. Interramal eyespots present. Collar chaetae like following chaetigers with superior elongate, narrowly hooded chaetae, and inferior spinelike chaetae. Thoracic uncini avicular, with several rows of minute teeth above main fang, developed breast, and medium-sized handle; neuropodial companion chaetae with asymmetrical hood and gently tapering tip. Abdominal uncini similar to thoracic ones. Anterior group of abdominal neurochaetae absent, posterior group with spinelike chaetae, in C-shaped arrangement. Pygidial eyespots sometimes present. Pygidial cirrus absent. Main references: Knight-Jones and Perkins (1998) and Capa (2007). Terebrasabella Fitzhugh and Rouse, 1999 Type species: Terebrasabella heterouncinata Fitzhugh and Rouse, 1999, by monotypy (three species) Diagnosis: Short-sized sabellids, a few millimeters long, with two pairs of radioles, each with two rows of vacuolated cells. Basal membrane and radiolar flanges both absent, dorsal basal flanges absent, ventral flanges present. Radiolar eyes absent. Dorsal radiolar appendages present, pinnular appendages absent; ventral radiolar appendages absent. Ventral lips, parallel lamellae, and ventral sacs all absent. Anterior peristomial ring indistinct. Posterior peristomial ring collar with narrow middorsal gap, dorsal margins laterally fused to faecal groove, midventral incision, and

 203

ventral lappets. Peristomial vascular loops absent. Peristomial eyespots absent. Thorax with eight chaetigers, abdomen with three. Glandular ridge on chaetiger 2 absent. Ventral shields poorly marked. Interramal eyespots absent. Collar chaetae similar to superior notochaetae of following chaetigers, elongate, narrowly hooded; inferior thoracic notochaetae broadly hooded. Thoracic uncini of two to three types, anterior chaetigers with acicular uncini, with several rows of teeth above main fang, or palmate; posterior thoracic uncini ­avicular, with medium-sized handle, developed breast and similar sized teeth above main fang; neuropodial companion chaetae present on chaetigers 2 to 6, with roughly symmetrical teardrop-shaped hood and gently tapering tip, absent on chaetigers 7 and 8. Abdominal uncini ­acicular, breast poorly to well developed, several rows of teeth above main fang, or palmate. Abdominal chaetae of both groups narrowly hooded. Pygidial eyespots absent. Pygidial cirrus absent. Main references: Fitzhugh and Rouse (1999) and Murray and Rouse (2007).

Acknowledgments We thank several colleagues for facilitating original images for this chapter: H. Bahena-Basave, S. Causio, G. Cranitch, F. Mastrototaro, C. Pichon, R. Pronzato, A. Semenov, R. Springthorpe, B. Yáñez-Rivera, and E. Wong. Some of the collected and photographed specimens were part of the Census of Coral Reefs Ecosystems (CReefs) field trips founded by BHP Billition (MC) or Workshop on Polychaetes of The Great Barrier Reef founded by the Lizard Island Foundation (MC). Other sources of funding for the performance of this chapter are the Norwegian University of Science and Technology (NTNU), Trondheim, Norway, and the Australian Museum, Sydney (as post doc contracts to MC). We are grateful to E. López and an anonymous reviewer for their detailed revision and useful suggestions for improving the manuscript and to Günter Purschke for his editorial work. JMMN currently receives a productivity fellowship from CNPq – Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil. References Agata, K., Saito, Y. & Nakajima, E. (2007): Unifying principles of regeneration I: epimorphosis versus morphallaxis. Development Growth and Differentiation 49: 73–78. Annenkova, N.P. (1934): Kurze Übersicht der Polychaeten der Litoralzone der Bering-Insel (Kommador-Inseln) nebst Beschreibung neuer Arten. Zoologischer Anzeiger 106: 322–331.

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Elena K. Kupriyanova, Alexander V. Rzhavsky† and Harry A. ten Hove

7.4.7 Serpulidae Rafinesque, 1815 We dedicate this chapter to our friend and co-author Alexander (Sasha) Rzhavsky (1959–2018) Introduction The family Serpulidae belongs to the order Sabellida (also includes families Sabellidae and Fabriciidae; see Kupriyanova and Rouse 2008), the group of sedentary tubicolous polychaetes that share a presence of radiolar crown used for both collecting food particles suspended in water (suspension feeding) and respiration, as well as separation of the body into an anterior thoracic and posterior abdominal region. They also show chaetal inversion, the arrangement when the ventral rows of toothed gripping chaetae (uncini) and dorsal rows of capillary chaetae invert position in the abdomen so that the uncini occupy the dorsal side of the body and the capillary chaetae become ventral. The family Serpulidae, known as calcareous tubeworms, is distinguished from all other polychaetes by their characteristic calcareous tubes, the opercula, and the thoracic membranes. According to the most recent review of serpulid taxonomy (ten Hove and Kupriyanova 2009), the family comprises 46 genera with approximately 350 extant species. Since then, four monotypic genera [Kimberleya, Pseudoprotula, Turbocavus (Fig. 7.4.7.19 A, B), and Zibrovermilia (Fig. 7.4.7.19 C, D)] have been added. Quite a few species have been newly described, some old species names have been resurrected (e.g., Hydroides inornata, Hydroides basispinosa, and Spirobranchus dendropoma), but other nominal species have been synonymized. All these taxonomic activities resulted in an increase of 37 accepted species. Ten Hove and Kupriyanova (2009), however, did not include the subfamily Spirorbinae Chamberlin, 1919, in their count. Summarized by Ippolitov and Rzhavsky (2014), the latter subfamily adds 133 (137?) species and 24 genera. The total number of accepted serpulid species, including spirorbins, currently is 506, but the diversity of serpulids is significantly underestimated because of poorly known deep-sea fauna and multiple supposedly cosmopolitan species (Hutchings and Kupriyanova 2018). Morphology Tubes Serpulids build tubes using paired calcium glands located laterally on the collar. The tubes consist of calcite,

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aragonite, or a mixture of both modifications of calcium carbonate (Bornhold and Milliman 1973, Vinn et al. 2008) interspersed with an organic mucopolysaccharide matrix. An inner organic membrane lining the lumen is found in all serpulids (Nishi 1993c, Vinn 2011). It should be noted that temperature may influence the robustness and shape of the tube (Li et al. 2016). Serpulid tube morphology is reviewed by Ippolitov et al. (2014). The general tube shape in most serpulins is undetermined, resulting in a variety of straight or ­irregularly twisted tubes. Some tubes have a determined shape, e.g., tusk-shaped Ditrupa, Bathyditrupa, and spirally coiled Spirodiscus (Fig. 7.4.7.1 A, B, J). Normally, tubes are attached to the substrate completely or partially with a free distal part, although the larvae of Bathyditrupa, Ditrupa, Spirodiscus, and Helicosiphon biscoeensis settle on small objects, as adults they are (secondarily) free-living. Spirorbins live in small spiral (hence the name) tubes 1.5 to 4 (up to 8) mm in diameter. Normally, the spirals are flat (Fig. 7.4.7.1 W), but the distal parts may be uncoiled and raised above the substrate (Fig. 7.4.7.1 V, X), with whorls being positioned on top of one another or attached to the substrate, not forming a spiral. Spirorbin tubes may be coiled clockwise (sinistral) (Fig. 7.4.7.1 U, V) or counterclockwise (dextral) (Fig. 7.4.7.1 W, X). Most species show only one coiling direction, but tubes of some Spirorbis coil in either direction. Dextral forms have never been recorded for typically sinistral species. The tube color is commonly white, but may also be completely or partly pink, bluish, orange (e.g., Spirobranchus, Serpula, and one Hydroides), or purple, as well as mustard (Spiraserpula), or even multicolored, i.e., white with dark-brown cross-striation as in Serpula vittata or with purple longitudinal stripes as in Spirobranchus taeniatus. Tubes are either opaque or porcellanous (with internal opaque and external hyaline layer), but Placostegus, Vitreotubus (Fig. 7.4.7.1 M, N), and some spirorbins (e.g., Paradexiospira spp.) have completely transparent tubes. Transparency is determined by tube ultrastructures and orientation of calcium carbonate crystals predominantly in one direction (ten Hove and Zibrowius 1986). In spirorbins with vitreous tubes, the inner tube lining or body of live specimens may be visible through tube walls, thus making the tubes appear colored (e.g., Paradexiospira). In the serpulin genus Placostegus, the hyaline tube permits a view on the girdle of red ocelli around the thorax (Fig. 7.4.7.1 N, near the tube mouth). In many cases, serpulid tubes are simply cylindrical lacking external sculpture (e. g., Apomatus, Hyalopomatus, and Protula) (Fig. 7.4.7.1 C, E). The sculpture consists of longitudinal elements, such as keels or rows of

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denticles, and transverse elements, such as ridges and peristomes of varying complexity (Fig. 7.4.7.1 F, G, J, K, N, O, P, R, S). Transverse peristomes indicate growth stops and can be sparsely and irregularly spaced, or almost regularly spaced (e.g., Pseudochitinopoma beneliahuae, Fig. 7.4.7.1 R, Serpula vermicularis, Fig. 7.4.7.1 F). A combination of numerous longitudinal keels and transverse ridges may form characteristic honeycomb structures as, e.g., in Metavermilia arctica (Fig. 7.4.7.1 K). Sculpturing often differs in the free distal and attached proximal parts of a tube. Tube surface may also be completely or partially pitted by numerous alveoli, e.g., Pseudovermilia fuscostriata ten Hove, 1975 (pl. 8A, B), Neodexiospira alveolata, and Paradexiospira (Spirorbides) cancellata, that may completely perforate tube keels. The lumen of serpulid tubes is circular, but Spiraserpula has unique internal tube structures, resembling longitudinal keels and crests inside the lumen (Pillai and ten Hove 1994). Tabulae or transverse tube elements may partition the oldest parts of the tube as response to tube damage in some serpulids (e.g., Pyrgopolon as Sclerostyla; ten Hove 1973). The area of tube attachment is often flattened to form peripheral flanges (e.g., Bathyvermilia islandica and Spirorbis (S.) cuneatus) and may also contain alveolar structures (e.g., Neodexiospira alveolata). When these flanges are continuously hollow or subdivided by septa inside, they are referred to as tubulae (Ippolitov et al. 2014). Structures used for embryo incubation All spirorbins incubate embryos either inside their tubes or in opercular brood chambers. The methods of embryo brooding have been used to subdivide spirorbins into six subfamilies (now tribes). Tube brooding (Fig. 7.4.7.3  A–D): Embryos positioned freely in the abdominal fecal groove—Paralaeospirini (Fig. 7.4.7.3 A; see Knight-Jones and Walker 1972); embryo positioned in a sac fixed to the thorax or to the abdomen by an epithelial stalk—Romanchellini (Fig. 7.4.7.3  B; see Knight-Jones et al. 1972); embryos adhering to one another and directly to the internal tube wall—Circeini (Fig. 7.4.7.3 C; see Knight-Jones et al. 1972); embryo string attached posteriorly to the internal tube wall by a filament—Spirorbini (Fig. 7.4.7.3 D; see Knight-Jones et al. 1972).

Opercular brooding (Fig 7.4.7.3 E–G): Embryos brooded in the reusable brood chamber formed by invagination of the operculum—Pileolariini (Fig. 7.4.7.3 E; see Knight-Jones and Thorp 1984); and embryos brooded in a cuticular brood chamber formed outside the distal part of the operculum, a new chamber is formed for each brood—Januini (Fig. 7.4.7.3 F, G; see Knight-Jones and Thorp 1984).

Body sections Body shape and regions The body of serpulins is bilaterally symmetrical even in animals that live in spirally coiled tubes, although in the genera Spiraserpula and Turbocavus, the left and the right sides of the thorax may differ by one or two parapodia. The thorax bears notopodial (dorsal) chaetae and neuropodial (ventral) uncini, whereas in the abdomen the position of chaetae and uncini is inversed; that is, the abdomen appears to be turned 180° relative to the thorax. Both thorax and abdomen are facing the substrate by the dorsal side (bearing notochaetae in thorax and uncini in abdomen). Spirorbin bodies are always asymmetrical and curved in the direction of the tube coil; their abdomen is turned relative to the thorax by approximately 90° (see Knight-Jones and Fordy 1979, figs. 1 and 3). The thoracic region of spirorbins is turned to the substrate by the dorsal side (bearing notochaetae), whereas the abdomen faces the substrate laterally. Therefore, terms such as “dorsal,” “ventral,” “right side,” and “left side” cannot be used for spirorbin morphology. Instead, the terms “facing the substrate” and “facing away from substrate,” “convex side,” and “concave side” are used. Serpulids, especially their radiolar crowns, are often very brightly colored (red, pink, purple, mauve, orange, brown, blue, yellow, or flesh-colored, tan, gray, green, or other colors forming distinct patterns; Fig. 7.4.7.2 A–C). In some Pileolariini, the posterior thorax on the side attached to the substrate has iridescent crystalline red, pink, purple patches that normally maintain their color after fixation, although sometimes changes to dark brown or black. Size The body length of the Serpulidae representatives ranges from 1 to 2 mm in many spirorbins and smaller filogranins

▸Fig. 7.4.7.1: Morphology of serpulid tubes. A, Ditrupa arietina; B, Bathyditrupa hovei; C, Apomatus globifer; D, Filograna sp.; E, Hyalopomatus biformis; F, G, Serpula vermicularis; H, Hydroides albiceps; I, Hydroides norvegica; J, Spirodiscus grimaldii; K, Metavermilia arctica; L, Neomicrorbis azoricus; M, Vitreotubus digeronimoi; N, Placostegus sp.; O, Spirobranchus polytrema; P, Spirobranchus taeniatus; Q, Ficopomatus enigmaticus; R, Janita fimbriata; S, Pseudochitinopoma beneliahuae; T, Bushiella evoluta; U, Bushiella kofiadii; V, Circeis armoricana; W, Paradexiospira vitrea, anticklockwise tube. Scale: A, 1 mm; B, 0.5 mm; C, 1 mm; D, 2 mm; E, 0.5 mm; F, G, 5 mm; H, 1 mm; J, K, 1 mm; L, 2 mm; M, 2 mm; N–S, 1 mm; T, 0.5 mm; U-W, 1 mm. From Ippolitov et al. (2014).



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Fig. 7.4.7.2: Color morphs of Spirobranchus corniculatus associated with reef corals. A, C, Lizard Island, Queensland, Australia (photo A. Semenov). B, Leyte, Philippines (photo O. Paderanga), modified from Willette et al. (2015).

(Filograna spp., Salmacina spp., and Rhodopsis) to more than 10 cm in large taxa. One of the largest serpulids, the nominal species Protula bispiralis (Savigny, 1822), constructs calcareous tubes of up to 40 cm in length and more than 1 cm in diameter. The widest known tube is that of P. superba Moore, 1909, with a reported width of 2.1 cm (Reish and Mason 2003). Radiolar crown The crown consists of radioles, each bearing rows of paired ciliated pinnules (Fig. 7.4.7.4 A). The radioles are attached to paired radiolar lobes located laterally on both sides of the mouth. The bases of the radioles may be joined with an interradiolar membrane (Fig. 7.4.7.5 E, mb A)

in, e.g., Spirobranchus (may also bear additional processes in some species), Pyrgopolon, Pomatostegus, Galeolaria, Dasynema, and Neovermilia. Spiral crowns may be present (e.g., some large Spirobranchus, Fig. 7.4.7.3 A–C, and Protula). Radiolar crowns may bear eyes that are grouped into ocelli, ocellar clusters, and compound eyes (ten Hove and Kupriyanova 2009). The most recent review is found in Bok et al. (2017). An unusual feature found on radioles is external unpaired fingerlike stylodes found in the genus Dasynema only. Operculum A modification of the distal part of a radiole, the operculum, which serves as a protective tube plug when



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Fig. 7.4.7.3: Embryo incubation in Spirorbinae. A, Paralaeospirini; B, Romanchellini; C, Circeini; D, Spirorbini; E, Pileolariini; F, G, Januini. A from Knight-Jones and Walker (1972), B–E from Knight-Jones and Vine (1972), F, G from Okuda (1934).

the animal withdraws into the tube, is present in most serpulins and in all spirorbins. The shape of the operculum varies significantly (Figs. 7.4.7.3 A–G, 7.4.7.4 B, C, 7.4.7.5 A–F, and 7.4.7.6 A–F); in some taxa (e.g., Protis, Protula, Apomatus, Hyalopomatus (Fig. 7.4.7.5 C), and some Metavermilia), opercula are simply soft transparent membranous vesicles. Normally, the operculum consists of a basal bulbous part (ampulla) and a distal part often reinforced with chitinous (Figs. 7.4.7.6 E, F) or calcareous endplates or distal caps with or without distal thorns (Fig. 7.4.7.6 A, B). Opercula are reinforced with flat or slightly concave chitinous endplates in Bathyditrupa, Ditrupa, some Filogranula spp., Janita, Marifugia, Placostegus, Pseudochitinopoma, and Chitinopoma or elongated distal caps (Vermiliopsis, Fig. 7.4.7.5 F, Semivermilia) with or without distal thorns (Pseudovermilia and some Metavermilia spp.). Ficopomatus and Rhodopsis (Fig. 7.4.7.5 B) show a large number of chitinous spines sometimes imbedded in or inserted into a chitinous base. A multitiered chitinous opercular reinforcement in Pomatostegus results in one of the most complex opercula known in Serpulidae. In Bathyvermilia, Dasynema, and Vermiliopsis labiata, the chitinous endplates are additionally reinforced by encrusted calcareous deposits. Opercular reinforcements in the form of calcareous endplates sometimes are adorned with nonmovable (Spirobranchus; Figs. 7.4.7.1 A and 7.4.7.5 E) or even very elaborate movable calcareous spines (Galeolaria, Fig. 7.4.7.6 B). Calcareous opercular reinforcement is extreme in Pyrgopolon, where both the operculum and the opercular talon (reaching deep into the peduncle) are entirely calcified.

The funnel-shaped opercula of Crucigera and Serpula are composed of numerous fused radii (Figs. 7.4.7.4 C, 7.4.7.5 A, D, and 7.4.7.6 C) and covered with thickened cuticle, whereas in species of Hydroides, the funnel is additionally topped with a verticil, a crown of chitinous spines (Fig. 7.4.7.5 D). Some taxa are nonoperculate (Floriprotis, Kimberleya, Microprotula, Paraprotis, Protula, Pseudoprotula, Salmacina, and Turbocavus). Also, normally nonoperculate species may include operculate individuals (Filogranella), and normally operculate genera may include nonoperculate species (e.g., Spirobranchus nigranucha). In serpulins and all tube-brooding spirorbins, opercular structure remains unchanged throughout the worm life, apart from ontogenetic changes during the development of the juvenile worm and/or regeneration-induced temporary changes. In tube-brooding spirorbins, the operculum usually consists of a calcified endplate with smooth surface and its outgrowth (talon) directed inside the opercular ampulla and sometimes in the opercular peduncle. In operculum-incubating spirorbins of Pileolariini and Januini, the opercular structure changes throughout the animal life. The structure of the primary operculum before the brood chamber formation is the same in that of tube-incubating groups. However, as the brood chamber develops, the opercular structure may change significantly. In most Pileolariini genera, the primary operculum is separated from the brood chamber soon after the formation is completed. Brood chambers vary from open nestlike structures (e.g., Nidificaria) to closed deep invaginations

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Fig. 7.4.7.4: General morphology of serpulids removed from their tubes. A, Lateral view of Protula sp. (photo G. Rouse). B, Lateral view of Apomatus sp. (photo F. Verbiest). C, Lateral view of Serpula vermicularis (photo F. Verbiest). D, Lateral view of a species from Vermiliopsis glandigerus–pygidialis complex, missing one radiolar lobe with operculum (photo G. Rouse), modified from ten Hove and Kupriyanova (2009).

completely covering the embryos with a pore that may open for embryos penetration and larvae release (e.g., Pileolaria, Protoleodora, and Bushiella). In Protoleodora, the primary operculum remains attached to the distal part of the brood chamber only with the distal talon end and is easily separated. In Bushiella, the brood chamber is closely associated with the primary operculum to which it remains connected. Normally, the endplate of the primary operculum is completely fused with the distal part of the chamber, and the talon is fused with the lateral chamber wall on the side facing outside the radiolar crown. In some species of Bushiella, the primary operculum attaches to the lateral wall of the chamber by the talon only, so that some small space remains between the distal endplate of the primary operculum and the distal plate of the opercular chamber. Most Januini species have cylindrical cuticular brood chambers with slightly calcified semitransparent

walls. The talon is completely fused with the first brood chamber; thus, the talon is attached to the lateral wall of brood chamber, facing away from the radiolar crown. By the time the embryos leave, the chamber separates from the operculum (e.g., Okuda 1934, fig. 10; Knight-Jones et al. 1979, fig. 4a). The distal part of the next chamber becomes the basal part of the previous, which does not form its own talon in most species. Pseudoperculum Crucigera, Hydroides, Serpula, and Spiraserpula are characterized by a club-shaped underdeveloped operculum carried on short rudimentary peduncle (pseudoperculum, Fig. 7.4.7.4 C) on the radiolar lobe opposite to the operculum. This pseudoperculum can develop into a functional operculum if the latter is lost, or two functional opercula can be found simultaneously. Vermiliopsis striaticeps is



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Fig. 7.4.7.5: Morphology of serpulid anterior ends. A, Serpula jukesii removed from tube; B, Josephella marenzelleri in tube; C, Hyalopomatus sp.; D, Crucigera tricornis; E, Spirobranchus cf. tetraceros removed from tube; F, species from Vermiliopsis glandigerus–pygidialis complex, radiolar lobe with operculum (all photos G. Rouse), modified from ten Hove and Kupriyanova (2009).

exceptional within its genus in the possession of a rudimentary operculum on a pinnulate stalk opposite the fully grown operculum. Peduncle In some serpulids, the radiole that bears the operculum is identical to others [e.g., Filograna, Apomatus, Josephella (Fig. 7.4.7.5 B), and Zibrovermilia (Fig. 7.4.7.19 E)], but in many others, the operculum is borne on a distinct peduncle, a modified thickened radiole lacking pinnules (Fig. 7.4.7.4 C). A notable exception is the genus Hyalopomatus, with the peduncle as wide as the normal radioles (Fig. 7.4.7.5 C). The genera Spirodiscus and Bathyditrupa are unusual in having thickened but pinnulated peduncles. The peduncle may gradually merge into the basal opercular ampulla (Fig. 7.4.7.5 E) or be separated from it by a constriction (e.g., Fig. 7.4.7.5 F). Below the operculum, the

peduncle may be modified to form paired lateral distal wings [e.g., Spirobranchus (Fig. 7.4.7.5 E), Galeolaria, and Pomatostegus]; other possible modifications of the peduncle are poorly documented. The peduncle in serpulins is usually inserted more or less below and between the first and the second normal radioles, outside the line of radioles. It may also be located at the base of radiolar crown, covering several radioles, or be positioned as the second modified radiole (e.g., Metavermilia). In spirorbins, the operculum-bearing radioles normally is located inside the radiolar crown, except for Protoleodora, where it is positioned outside the crown. In cross section, the peduncle is commonly cylindrical, but in some serpulids (e.g., Spirobranchus) it is nearly triangular, flattened (Bathyditrupa, Dasynema, Janita, Neovermilia, and Pomatostegus), or even characteristically flat ribbonlike (Metavermilia).

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Fig. 7.4.7.6: Opercular variability in serpulins. A, Spirobranchus coronatus showing calcareous endplate with spines. B, Operculum of Galeolaria hystrix with calcareous plates and numerous movable spines. C, Frontal view of Serpula jukesii funnel-shaped operculum with numerous radii. D, Operculum of Hydroides tuberculata made of basal funnel and distal verticil of chitinous spines. E, Multitiered operculum of Metavermilia acanthophora. F, Simple globular operculum of Neovermilia globula (all photos G. Rouse), modified from ten Hove and Kupriyanova (2009).

Collar chaetiger The first thoracic chaetiger in serpulids is the collar segment, lacking neuropodial (ventral) uncini and bearing only notopodial (dorsal) chaetae (termed collar chaetae); the latter may be absent (e.g., Ditrupa, Marifugia, Placostegus, some species of Spirobranchus). The segment is surrounded by a membranous peristomial collar, either subdivided into one larger medioventral and two smaller laterodorsal lobes (Fig. 7.4.7.4 D) or nonlobed, as in spirorbins, Ditrupa, Ficopomatus, Paraprotis, and Bathyditrupa. Distinct tongue-shaped outgrowths, the tonguelets, located between the dorsolateral and the ventral lobes of the collar, are present in Spirobranchus and Pyrgopolon. In some spirorbins, the collar may form a large lateral flap on the convex body side (e.g., Spirorbis spirorbis).

Thoracic membranes The laterodorsal collar lobes continue on both sides of the thorax into the thoracic membranes (Fig. 7.4.7.4 C, D). Spirorbin taxonomists (e.g., Knight-Jones and KnightJones 1977) did not distinguish between the thoracic membranes and the collar, but they used the term “collar” collectively for both. These membranes can be ending at the first (Ditrupa—but see Thorax, below—Josephella and Rhodopsis) or the second thoracic chaetiger (Chitinopoma, Pseudovermilia, and Semivermilia) or can continue to the midthorax (e.g., Pomatostegus and Vermiliopsis; Fig.  7.4.7.4  D), to the last thoracic chaetiger (some Spiraserpula and Metavermilia spp.), or past the end of the thorax fusing to form a ventral apron (Fig. 7.4.7.4 A, C), e.g., Galeolaria, Ficopomatus, Serpula, Hydroides, Protula, and Spirobranchus). Dorsal margins of thoracic membranes



are fused in Ficopomatus uschakovi and in the nominal spirorbin genera Neodexiospira, Romanchella, and Velorbis. The genus Floriprotis shows pockets on the inside of the thoracic membranes. Thorax The number of thoracic chaetigers is fairly constant, and in most serpulin genera, the thorax of adults consists of seven thoracic chaetigerous segments (first with notopodial collar chaetae only and six remaining with both notopodia and neuropodia). The number of thoracic segments may vary from 5 (Tanturia and Bathyditrupa) to 6 (Ditrupa; but see ten Hove and Smith (1990)—Laminatubus, Hyalopomatus, and Spirodiscus) and 10 (Kimberleya), whereas the thorax of spirorbins has only three to five segments. Some ­serpulin taxa have a variable number of thoracic chaetigers, such as Filograna and Salmacina (6–12 segments), Filogranella (11–14), Josephella (4–6), Rhodopsis (4–6), Protis and Pseudochitinopoma (6–7), and Spiraserpula (5–11). The most extreme variability is shown by Turbocavus with 7 to 19 thoracic chaetigers (Fig. 7.4.19 D). Moreover, some genera with an otherwise fixed number of thoracic segments (7) occasionally show species with a variable number of thoracic segments: for example, three Hydroides species (Hydroides bisectus and two as yet undescribed species) have seven to nine chaetigers (Imajima and ten Hove 1989: 13), and this occasionally may occur in small representatives of Serpula as well (ten Hove, unpublished observation). Spirorbins usually have only three or four thoracic chaetigerous segments (including the collar segment). Rarely, species with a four-segment thorax as adults (e.g., Paradexiospira) may have only three thoracic segments as juveniles. Amplicaria and Anomalorbis have five chaetigers, whereas Neomicrorbis, a questionable spirorbin, has “probably” seven thoracic segments (Zibrowius 1972a), whereas according to ten Hove and Kupriyanova (2009), the number of thoracic chaetigers is asymmetric, five to the left and six to the right in this taxon. Notochaetae of thoracic segments (including collar chaetae, if any) consist of a proximal smooth shaft and a distal expansion made of microfibers that looks like a hood (or striated limbus) under a compound microscope. Although notochaetae of thoracic segments are traditionally termed capillary and limbate chaetae, SEM examination shows that the limbus is made of numerous microfibers. Moreover, all thoracic chaetae are limbate but of two sizes: the smaller being called capillary but clearly “limbate” as well. In spirorbins, small capillary chaetae (often termed companion capillary) are found only on the collar segment, whereas in serpulins, they may be present in all thoracic fascicles. In addition to unmodified (small capillary and large limbate) chaetae, serpulids have a

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range of large modified (special sensu ten Hove and Kupriyanova 2009) chaetae found only in the collar fascicle and in posterior thoracic chaetigers. In some serpulins and most spirorbins, limbate chaetae are supplemented in the posterior thorax by modified chaetae. These chaetae termed Apomatus (or sickle-chaetae in spirorbins) are sigmoid to sickle-shaped, with a proximal denticulate zone (looking like fine striation under a compound microscope) and a long flat curved blade with a row of blunt regular teeth (Fig. 7.4.7.8 A). The sickle (Apomatus) chaetae are apparently secondarily absent in some spirorbins (e.g., Circeis spp. and Neodexiospira spp.), whereas only sickle-chaetae are present in the third fascicle in Paradexiospira spp. Apomatus chaetae are found exceptionally in the collar fascicle of Apomatus voightae. Turbocavus bears a unique type of thoracic chaeta, which is plicate or multifolded at the base and continues with a grooved shaft tapering to the capillary tip. The fascicle of serpulid collar chaetae may contain only capillary and large limbate chaetae (e.g., Bathyvermilia spp., Protula spp., Protoleodora spp., Bushiella (Bushiella)). In serpulins, collar chaetae may include a range of modified chaetae in addition to capillary and limbate ones. Ten Hove and Kupriyanova (2009) distinguish four types of modifications. Three basal modifications are characterized by the presence of a more or less distinct extension below the distal blade. Bayonet-type chaetae have only one or two (rarely more) large proximal bosses at the base of the distal blade (e.g., Serpula and Hydroides; Fig. 7.4.7.7 A, D). Fin-and-blade chaetae have the basal “fin” (the term is a result of initial observations under a light microscope and incorrectly assumes a structure as flat as a fish fin) made of relatively few teeth of intermediate size (Fig. 7.4.7.7 E); the fin can be separated by a distinct smooth gap from the distal blade (e.g., Chitinopoma and Protis). Spirobranchus-type chaetae have a proximal “fin” consisting of very numerous tiny hairlike spines (e.g., Spirobranchus; Fig. 7.4.7.7 C, F). The fourth type is the distal modification found in Ficopomatus-type collar chaetae that are characterized by very coarse curved teeth alongside the distal part of chaetae (Fig. 7.4.7.7 B). Most spirorbin species have only modified chaetae replacing large limbate ones in the collar segment. Both basal and distal types of modifications may be found on the same modified collar chaeta. Three types of spirorbin modified collar chaetae are distinguished (Rzhavsky et al. 2014). Chaetae with only basal modifications are finand-blade chaetae (e.g., Spirorbis), with a distinct basal fin clearly separated from the limbate blade. Chaetae with only distal modification are cross-striated chaetae found only in spirorbins (e.g., Paradexiospira (P.) violacea

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Fig. 7.4.7.7: Special collar chaetae. A–C: photos, bayonet chaetae of Hydroides (A), Ficopomatus-type chaetae (B), Spirobranchus-type chaetae (C). D–F: SEM micrographs, bayonet chaeta (D), fin-andblade chaetae (E), Spirobranchus-type chaeta (F). A–C photos E. Wong; D–F from ten Hove and Kupriyanova (2009).

Fig. 7.4.7.8: Serpulid chaetae and uncini, SEM micrographs. A, Apomatus chaetae of Filogranula; B, flat trumpet-shaped abdominal chaetae of Crucigera; C, flat geniculate abdominal chaetae of Janita; D, true trumpet-shaped abdominal chaetae of Spirobranchus; E, saw-shaped uncini of Serpula; F, rasp-shaped uncini of Marifugia. From ten Hove and Kupriyanova (2009).



and Neodexiospira pseudocorrugata). The blades of these chaetae are bent and have denticles organized into distinct long transverse rows; under a compound microscope, this looks like a cross-striation. Collar chaetae on the convex body side are usually larger and with larger denticles on the blades. Cross-striation may be vestigial, when rows are short, with three to four denticles per row (e.g., Neodexiospira lamellosa (Lamarck, 1818)) and asymmetrical, when the rows are present on one of the “lateral sides” of the chaetal blade (e.g., Circeis spirillum). Unusual modified strongly bent collar chaetae of some Circeis spp. appear to bear vestigial cross-striation on the “frontal side” of the blade only and probably represent just a variation of cross-striated chaetal type (see Knight-Jones and Fordy 1979, fig. 11). Chaetae with both distal and basal modifications (fin-and-blade cross-striated chaetae) have a combination of cross-striated blade separated from a basal denticulate fin by a smooth gap. Cross-striation may be as distinct [e.g., Pileolaria cf. berkeleyana (see Rzhavsky et al., fig. 30  I), Paradexiospira (Spirorbides) vitrea (see Rzhavsky et al., fig. 20 F)], as vestigial (e.g., Bushiella (Jugaria) atlantica (Knight-Jones, 1978)). Generally, spirorbins have the same types of large collar chaetae in fascicles on both body sides, although some species (e.g., Spirorbis (S.) tridentatus) may have finand-blade collar chaetae on the convex side of body, but limbate ones on the concave side or chaetae only from the convex side may be cross-striated (e.g., N. pseudocorrugata). In Eulaeospira spp., large chaetae of different types (limbate and fin-and-blade) may be present in the same fascicle. Thoracic neuropodia are transversal tori with specialized neurochaetae (uncini) arranged side by side in a single transverse row. Thoracic uncini are flat ovoid to subquadrangular plates bearing one or several rows of curved teeth on their edge ending with a slightly larger tooth (anterior fang or peg depending on the shape). The base of an uncinus is deeply embedded into the torus. Some species of Protula may completely lack thoracic uncini (e.g., P. bispiralis). Depending on the number of vertical rows of teeth in the uncini, they are termed saw-shaped (one row of teeth along the edge, e.g., Hydroides and Serpula; Fig. 7.4.7.8 E), rasp-shaped (several rows of teeth along the entire edge, e.g., Hyalopomatus, Placostegus, and Marifugia; Fig. 7.4.7.8 F) or saw-to-rasp-shaped (from one tooth on edge distally to a row of up to five teeth proximally near the peg, e.g., Filogranula). Juvenile specimens of otherwise “sawshaped” species may show rasp-shaped uncini, and the shape of the uncini may change from saw-shaped to raspshaped from the anterior to the posterior thorax.

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The shape of the anterior tooth of uncini was usually referred to in earlier publications as either simple or bifurcate. However, SEM examinations (ten Hove and Kupriyanova 2009) revealed that the structure is very variable. The pointed anterior tooth is termed a fang (in, e.g., Filograna, Hydroides, Neovermilia, Salmacina, and Serpula; Fig. 7.4.7.8 E) and spirorbins of the tribe Pileolariini. However, what under a compound microscope appears to be a bifurcate or blunt anterior tooth may be gouged (bluntly truncate flattened structure with lateral edges curved underneath (e.g., Pseudovermilia and Spirobranchus). Examination with SEM shows that blunt (not pointed) anterior teeth of uncini may also be either flat, rounded, spatulate (as in Galeolaria), rectangular, or even trapezoidal in appearance (Ficopomatus), bilobed to quadrilobed (as in Hyalopomatus marenzelleri); truncated, rounded, or indented anteriorly (Chitinopoma, Pyrgolopon, and Vermiliopsis); or elongated, blunt, rounded to squarish, with transverse rows of teeth continuing over almost its entire length (Apomatus and Protula). For all these “wedge”-shaped anterior teeth, ten Hove and Kupriyanova (2009) proposed the term peg (Fig. 7.4.7.8 F). Thoracic tori generally are positioned laterally on the thorax, but in some taxa, they are widely separated in front, gradually approaching one another posteriorly, so that the posterior thoracic tori may touch one another, forming a triangular depression ventrally. In some Neovermilia spp., thoracic tori are completely shifted to the ventral part of the thorax. Abdomen The number abdominal segments is variable depending on animal’s age and size; it can be as low as 10 to 30 in small species or juveniles to more than 200 segments in large species. Several anterior abdominal segments may lack chaetae and uncini, forming an achaetous abdominal zone. Some taxa have a glandular zone on the dorsal side of the last abdominal segments called the posterior glandular pad (Fig. 7.4.7.4 D). Whether or not there is a relation between glandular pads and transverse tabulae in tubes is not known. The pygidium is usually bilobed and bears a terminal slit-like anus. An abdominal segment bears a dorsal row of uncini (notochaetae) and a ventral fascicle of chaetae (neurochaetae), thus inverse of the thoracic arrangement. Abdominal chaetae are normally less numerous per bundle than the thoracic ones. The simplest forms of abdominal chaetae are capillary (Bathyditrupa) and nearly capillary (e.g., Hyalopomatus, or acicular (Paumotella). The term “trumpet-shaped chaetae” used by various authors to describe the abdominal chaetae in, e.g., Hydroides and Serpula is misleading (ten Hove and

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Kupriyanova 2009). Although the distal parts of these chaetae, when examined under a compound microscope, are widened into what in profile looks like a trumpet edged with two rows of thin teeth, examination with SEM shows that these chaetae are flat, with a single row of marginal acute teeth (Fig. 7.4.7.8 B). Therefore, they are termed flat trumpet-shaped chaetae by ten Hove and Kupriyanova (2009). On the contrary, abdominal true trumpet-shaped chaetae are distally hollow, with two parallel rows of sharp denticles (details not visible without SEM), extending into a long lateral spine (e.g., Ficopomatus, Galeolaria, Placostegus, and Spirobranchus; Fig. 7.4.7.8 D). Abdominal chaetae in older literature were often referred to as “geniculate,” the term generally defined in dictionaries as “having a kneelike joint” or “bent sharply.” The term is misleading because there is no joint between the proximal and the distal parts of the chaetae and not all of them are bent. Also, because it is hard to see with a compound microscope whether such chaetae have a single or double row of teeth bordering the blade, true trumpet chaetae have been lumped together with completely different flat geniculate abdominal chaetae (Fig. 7.4.7.8 C) having a bent blade with a single row of teeth along its edge. These “flat geniculate” chaetae are not uniform, and depending on the shape of the distal blade, four types are distinguished by ten Hove and Kupriyanova (2009): (1) sickle-shaped, fairly straight to weakly sickle-shaped chaeta with long concave edge bordered by very regular rounded teeth (e.g., Apomatus and most Protula); (2) flat triangular, with a kneelike bend and with dentition on the outside of a wide triangular distal blade (e.g., Chitinopoma and Filogranula); (3) flat narrow geniculate, as item 2, but with the blade not so sharply bent and more elongated (e.g., Filograna, Josephella, Salmacina, and Vermiliopsis); and (4) retrogeniculate chaeta, as item 3, but with a recurved hook on the outside (anterior side) of the knee, directed proximally (e.g., Neomicrorbis and Protula balboensis). Spirorbin abdominal chaetae are always flat geniculate only, usually sharply bent with denticulate blade, one to two (up to 10) per fascicle. The basal part of the blade may extend beyond the shaft of the chaeta forming a heel. The three main types of spirorbin abdominal chaetae (subtypes of flat triangular) are (1) brush-type with very short sharply narrowing blades and around 10 denticles (typical for Romanchellini; see Knight-Jones and Fordy 1979, fig. 68 E–G); (2) chaetae with large wide blades of the same width along their entire length and sharply narrowing only at the distal end, always lacking the heel (typical for Januini); and (3) pennant-shaped chaetae with the blade of the intermediate length gradually narrowing toward the distal end (Spirorbinae, Circeini, Paralaeospirini, and Pileolariini, as a rule with a heel).

In most serpulins, abdominal chaetae become progressively longer toward the pygidium, and the posterior abdominal chaetae are either true capillaries (e.g., Hydroides) or elongated and “unbent” modified chaetae. If capillary chaetae of the most posterior abdominal segments are at least an order of magnitude longer than the chaetae of anterior and middle abdominal segments, they are referred to as “long capillary chaetae.” In spirorbins, flat geniculate chaetae may be accompanied by capillary hooked chaeta that may be present on all abdominal chaetigers or only posteriorly. Long capillary chaetae are absent in spirorbins. In serpulins, saw- and/or rasp-shaped uncini vary strongly according to their position in the abdomen. Because polychaetes grow by addition of segments posteriorly, serpulids can shed their juvenile rasp-shaped uncini and replace them with saw-shaped adult uncini as they grow. Thus, the most posterior, youngest segments invariably show rasp-shaped uncini. In all spirorbins, abdominal uncini are rasp-shaped with flat or slightly rounded anterior peg. Uncini may be either symmetrically distributed along both body sides, as in Spirorbini, Januini, and Pileolariini, or their distribution may be sharply asymmetrical as in Circeini, Paralaeospirini, and Romanchellini. In the latter, abdominal uncini on the convex body side are absent or very few on two to three posterior abdominal segments.

Reproduction and development Fertilization mechanisms Serpulins are broadcast spawners, releasing eggs and sperm into the water column where fertilization and subsequent development occur (Fig. 7.4.7.9 A, B). The gametes are released through nephridiopores and are delivered with the help of ciliary beating in the fecal groove to the tube mouth, where they are ejected above the radiolar crown. Fertilization success and factors affecting it are poorly studied. Pechenik and Qian (1998) published a fertilization curve describing the effect of sperm concentration on fertilization success in Hydroides elegans. Fertilization in this species is successful over a broad range of sperm concentration, and usually >95% of eggs were fertilized within 15 min after the gametes were mixed. By contrast, high sperm concentrations (>107 sperm ml-1) are required to achieve fertilizations in gregarious Australian serpulid Galeolaria caespitosa (see Kupriyanova 2006). Fertilization takes place within 5 min and does not appear to be adversely affected by high sperm concentrations (polyspermy). Fertilization rates in this species are also



influenced by gamete age, male–female compatibility, and ambient water temperature. Sperm velocity is positively related to the fertilization success. Sperm velocity, longevity, and respiration are affected by temperature, but not by water-soluble egg extracts. The gamete traits of G. caespitosa apparently enable this gregarious serpulid to perform under conditions of high population density (Kupriyanova and Havenhand 2002, 2005). Olivia et al. (2015) examined the effect of varying (5‰–35‰) salinity, demonstrating that fertilization and larval development occur till the limit of 10‰ salinity, and spermatozoids and zygotes of Ficopomatus enigmaticus are sensitive to copper (Cu2+), cadmium (Cd2+), sodium dodecyl sulfate (SDS), and 4-n-nonylphenol (NP)Cu, Cd, SDS, and NP, whereas NP shows the highest degree of toxicity. Less is known about the fertilization biology in small-bodied brooding serpulins and spirorbins. Gee and Williams (1965) reported that in Spirorbis spirorbis, gametes are shed through the nephridioducts and fertilization occurs inside the tube. Broadcasting of sperm was previously assumed for all brooding tube dwellers. However, discovery of a spermatheca (Daly and Golding 1977, Picard 1980, Rouse 1996) suggests that fertilization is more complex in brooding species. Single spermatheca of S. spirorbis is located at the base of the radiolar crown (Daly and Golding 1977, Picard 1980). Sperm are released into the sea, collected by other individuals, and stored in their spermatheca. Sperm leaves the spermatheca during spawning and fertilizes eggs within the animal tube. Fertilization probably also occurs in the tube of the operculum-brooding spirorbins, and fertilized embryos are transferred to the opercular incubating chamber. Paired spermathecae of Salmacina sp. are situated in the base of the radiolar crown (Rouse 1996). No information is available on the efficiency of fertilization in brooding species, and the assumption that the fertilization rate for incubating species is high may be not substantiated. Spirorbins are capable of self-fertilization, although it does not occur as readily as cross-fertilization. Self-fertilization was not demonstrated in the hermaphrodite serpulid Salmacina (see Nishi and Nishihara 1993). Reproduction Sexual reproduction The Serpulidae show a range of sexuality patterns as well as reproductive and developmental mechanisms, encompassing asexual and sexual reproduction, gamete broadcast spawning and sperm storage, planktonic and parental benthic development (brooding), and feeding and nonfeeding larval development. The reproduction

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and life history of serpulids was reviewed by Kupriyanova et al. (2001). Although the sexes were traditionally considered to be separate in the group, sequential (protandric) hermaphroditism with a short intermediate stage appears to be the rule rather than an exception for most serpulins, whereas all known spirorbins are simultaneous hermaphrodites. Their anterior abdominal segments contain eggs, and the posterior segments contain sperm. However, because sperm appear to develop faster than oocytes, juveniles may function as males before they can function as females. Simultaneous hermaphroditism is less common in serpulins, and it seems to be a result of slower protandrous transition in small taxa such as Rhodopsis pusilla, Filograna, and Salmacina. In the latter genera, male gametes are usually in anterior segments, and the female ones are in posterior ones. Asexual reproduction Asexual reproduction in the Serpulidae is best known for Filograna and Salmacina, but was later described for Filogranula gracilis, Josephella marenzelleri, Rhodopsis pusilla, some species of Spiraserpula, and Filogranella elatensis. In asexually reproducing serpulids, the animal divides into two by transverse fission in the middle of the abdomen. Before the separation takes place, the new cephalic region forms in the middle part of parental specimen by the transformation of abdominal segments into thoracic ones (Fig. 7.4.7.10). Asexual reproduction typically leads to the formation of pseudocolonies of branching tubes. True gonads are absent in some serpulids (e.g., Hydroides dianthus and Ficopomatus enigmaticus) in either sex, and the germ cells are produced by a germinal epithelium associated with the blood vessels in the intersegmental septa (Clark and Olive 1973, Dixon 1981). Distinct gonads have been described in Salmacina/Filograna and in Spirobranchus triqueter (as Pomatoceros; Cotter et al. 2003). In several spirorbins, Potswald (1967) described the gonad as an organ composed of clumps of primordial germ cells arranged in two rows along the ventral nerve cord and running the length of the abdominal chaetigers. Developing gametes are released into the coelom. There is a lack of synchrony in the way gametes are produced in both sexes, with all but the prespawning mature and recently spawned individuals containing gametocytes in different stages of development. Egg size in serpulins range from 40 to 45 µm in Spirobranchus kraussii and Hydroides ezoensis to 180 to 200 µm in Chitinopoma serrula, whereas eggs in spirorbins range from 80 µm in Neodexiospira foraminosa to 230 µm in Pileolaria militaris. Species with eggs of less than 80 µm in

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Fig. 7.4.7.9: Reproduction and development in serpulids. A, Serpula jukesii releasing eggs (photo G. Rouse); B, Galeolaria caespitosa, eggs and sperm (photo E. Kupriyanova); C, Semivermilia sp., development of lecithotrophic brooded larvae (SEM photo G. Rouse).

diameter have planktotrophic larvae, and those with larger eggs are characterized by lecithotrophic development. Sperm morphology varies remarkably within Serpulidae (Rouse 1999a, b, 2005), and differences in sperm morphology reflect different modes of fertilization or sperm transfer (Fig. 7.4.7.11 A–L). Sperms

characterized by a spherical to conical head are typical for broadcast-spawning serpulids, and those with elongated heads are founds in brooding organisms. Jamieson and Rouse (1989) distinguished ect-aquasperm for broadcast-spawning species and ent-aquasperm that is released into water at some stage but is stored by the

Fig. 7.4.7.10: Asexual reproduction of Salmacina dysteri (SEM photo E. Nishi). The asexual bud and parental worm both have extended radiolar crowns. Both parent and bud still do not have the full complement of thoracic chaetigers.



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Fig. 7.4.7.11: Sperm morphology of serpulids. Broadcasting species: A, Serpula sp.; B, Spirobranchus kraussii; C, Spirobranchus corniculatus; D, Galeolaria caespitosa; E, Hydroides elegans. Brooding species: F, Paraprotis dendrova; G, Salmacina sp.; H, Chitinopoma serrula; I, Spirorbis spirorbis; J, Bushiella sp.; K, Pileolaria militaris; L, Janua pagenstecheri. Scale: A–C and E, 2 µm; D and F, 1 µm; G and H, 2 µm; I–L, 5 µm. Redrawn from Kupriyanova et al. (2001).

female before fertilization. Spherical sperm with a midpiece containing spherical mitochondria and a flagellum (ect-aquasperm) are known for such free spawners (Fig. 7.4.7.11 A–E), whereas sperm with an elongated head and midpiece (ent-aquasperm) are known for brooding serpulins such as Salmacina dysteri, Chitinopoma serrula, and Rhodopsis pusilla. Spirorbinae also have elongated sperm (Fig. 7.4.7.11 F–L). The elongated shape of the nucleus and mitochondria are attributed to sperm storage before fertilization. Paraprotis dendrova is unusual because its sperm, although slightly elongated, is very similar to that of broadcasting serpulids (Fig. 7.4.7.11 F). This species broods larvae on a modified branchial radiole and lacks spermathecae (Rouse 2005). Eggs of this species apparently attach to the brooding radiole and are fertilized by the sperm freely released into water column. Life cycles Brooding Planktonic development with feeding trochophores is well known for common and widely distributed taxa such as Crucigera, Ficopomatus, Galeolaria, Hydroides, Serpula, and Spirobranchus (Fig. 7.4.7.9 A, B). However, serpulids show a wide range of brooding methods. Tube incubation

is known for species of Filograna and for Protula apomatoides, but it is probably common for other species. Brooding in ovicells on the tube occurs in a variety of ways. For example, ovicells of Microprotula ovicellata resemble swellings encircling the distal part of the tube. Chitinopoma serrula produced pouches with twin chambers at the orifice of the tube, each with 10 to 20 larvae (Fig. 7.4.7.12 A). The ovicells in Rhodopsis occidentalis (Fig. 7.4.7.12 D) are wide inverted pouches arranged one by one along the length of the tube (Fig. 7.4.7.12 C). Pseudovermilia pacifica shows a cup- to dome-shaped ovicel over the entrance of the tube (Fig. 7.4.7.12 D). Paraprotis dendrova (Fig. 7.4.7.12 D) dendrova embryos are brooded inside the radiolar crown on an appendage with branches growing from the mouth parts (Fig. 7.4.7.12 E). Metavermilia ovata holds developing embryos inside the base of its radioles. Brooding in pockets of the thoracic membranes is known for Floriprotis sabiuraensis, whereas brooding in gelatinous masses near the tube mouth (Fig. 7.4.7.12 B) is found in Protula tubularia (reviewed by Kupriyanova et al. 2001). Spirorbinae all brood their lecithotrophic larvae either in the parental tube or in the opercular brood chambers (Fig. 7.4.7.3 A–G). Tube incubation methods vary according to the methods of embryo anchorage within the tube. Embryos lie free in the tube (Paralaeospira); they form an egg string attached to the tube by a posterior

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Fig. 7.4.7.12: Brooding in serpulids. A, Chitinopoma serrula, paired ovicells at the tube orifice (photo G. Rouse). B, Protula tubularia brooding in gelatinous masses near the tube mouth (photo R. Sanfilippo). C, Rhodopsis pusilla, single ovicells located along the tube (photo E. Nishi). D, Pseudovermilia occidentalis single ovicel at the tube entrance (photo G. Rouse). E, Paraprotis dendrova, eggs and embryos attached to a spiral radiolar rudiment (SEM photo E. Nishi).

filament (Spirorbis) and adhere to one another and to the tube wall in Circeis and Paradexiospira. They may also be attached anteriorly to a thoracic funnel-like stalk or epithelial oviducal funnel (Protolaeospira, Helicosiphon, Romanchella, Metalaeospira, and Eulaeospira). Opercular incubation is found in more than half of spirorbin species. The brood chambers of the pileolariin genera (Amplicaria, Pileolaria, Nidificaria, Vinearia, Simplaria, Protoleodora, and Bushiella) are formed by invagination of the opercular ampulla itself. Such brood chambers are used for a number of broods. The primary nonbrooding operculum is either shed after the chamber is formed (e.g., Pileolaria) or is fused to the chamber for additional embryo protection (Bushiella). When breeding ceases, the brooding chamber may be replaced by a nonbrooding operculum, which may again be later replaced by a new brood chamber. Brood chambers of the januins (Neodexiospira, Janua, Pillaiospira, and Leodora) are formed distally by the calcified opercular plate outside the opercular

ampulla. Every brood chamber is used for only one brood and is shed to liberate larvae. Larval development Developmental events in genera with planktotrophic larvae are very similar. The fertilized eggs undergo synchronous holoblastic cleavages up to the blastula stage. The uniformly ciliated blastula develops into an early trochophore with a prototroch consisting of a single ciliary equatorial band. The prototroch separates a rounded episphere from conical hyposphere. The simple gut opens with the mouth below the prototroch and the anus exiting on the opposite side. Cilia on the hyposphere are organized into the neurotroch, which runs from the ventral posterior surface to the mouth. Later, the prototroch develops three main ciliary bands: the upper and lower with shorter cilia and the middle with much longer cilia. A second ciliary ring, the metatroch, develops below the prototroch at this stage, and a band of short feeding cilia



forms between the prototroch and the metatroch. On the right side of the episphere, a cluster of red pigment cells forms an ocellus. The metatrochophore continues to grow. Next, the larva develops the left ocellus identical to the right one. After this stage, the growth is confined to the hyposphere, and the larva elongates and develops three chaetigerous segments. Before the settlement, a small fourth trunk segment is delineated and paired branchial rudiments appear posterior to the metatroch. Suspension feeding by serpulid larvae is achieved by use of the opposed band system (the prototroch and the metatroch), as described for Serpula columbiana by Strathmann et al. (1972). The long cilia of the preoral prototroch generate the major current used in feeding and locomotion, whereas the postoral metatroch is used in feeding and rejection and the food groove in transport of particles. The opposed beats of the cilia of the preoral and postoral bands result in increased movement of the preoral cilia relative to the water in the latter half of their effective stroke. Most of the clearance of particles from water occurs at this point. If the metatroch and cilia of the food groove stop beating, particles are not collected behind the prototroch but are carried posteriorly with water. The length of prototrochal cilia scales with larval body size; for example, in the larva of Hydroides elegans, the length of prototrochal cilia increased from 28 to 42 µm in early to late-stage larvae (Henderson and Strathmann 2000). Nonfeeding planktonic development reported for Protula sp. by Tampi (1960) is very similar to that of feeding larvae, but the active gut is still not formed by the threechaetiger stage. The development of brooded nonfeeding serpulid embryos is less known than that of planktotrophic larvae. Short accounts of the development of nonfeeding larvae of serpulids are given for Salmacina dysteri, Paraprotis dendrova, and Rhodopsis pusilla (Nishi and Yamasu 1992 a, b, c). The description of lecithotrophic development inside the spirorbin brooding structures is very fragmentary (Fig. 7.4.7.9 C). Development from the early trochophore to swimming competent larvae is described for Pileolaria cf. militaris, Spirorbis sp., Circeis cf. armoricana, Neodexiospira alveolata, Neodexiospira pseudocorrugata and Neodexiospira sp., and Spirorbis spirorbis (see Kupriyanova et al. 2001). These accounts suggest that the developmental events and general larval morphology are very similar for brooded and planktonic serpulid larvae. Like serpulin trochophores, early spirorbin trochophores are subdivided into a small episphere and a large hyposphere by a prototroch. The prototroch of the early spirorbin consists of two bands of cilia. Eyespots may be present or absent at the early stage. A functional mouth and anus are always absent; their future location

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can be recognized by a depression. In metatrochophores, the collar forms ventrally under the prototroch; the eyespots are present. A neurotroch consisting of transverse rows of cilia appears midventrally. In the late metatrochophore, the mouth opens, and radiolar and opercular buds develop. Some species develop very distinct white primary shell glands. A competent spirorbin larva released from the brooding chamber has three chaetigers and a terminal segment, bands of locomotory cilia (prototroch, metatroch, and neurotroch), apical cilia, eyespots, branchial and opercular buds, and a large collar. The stomodeum is open ventrally, between prototroch and collar, but the stomach is not functional and is filled with yolk. The anus is also open and surrounded by cilia. The metamorphosis in serpulids starts with in the disappearance of the prototroch and continues with differentiation of the radiolar crown in the head region, the collar, thoracic membrane, and the pygidium at the end of the abdomen. Successful attachment and construction of the tube marks the completion of normal metamorphosis. In planktotrophic larvae, the onset of metamorphosis coincides with the shift into demersal life, but it is not completed until after settlement. Tube formation depends on successful settlement, which itself depends on a number of cues. As metamorphosis starts, the behavior of planktotrophic larvae changes from pelagic swimming to a slow exploration of the bottom. This searching stage may include swimming over the bottom with the abdomen in close contact with the surface, forward crawling, quivering on the spot, repeated contacting submerged surfaces with apical tufts, and temporary attachment to the substratum by mucous threads. The larvae settle by secreting a mucous tube, which is covered later with calcareous matter produced by the ventral collar surface. The onset of metamorphosis is preceded by increased contraction of the circular muscles below the eyes to constrict a head region. The chaetal sacs enlarge, and the most anterior pair begins to turn upward. Uncini appear on the second chaetiger and later on the third. During settlement, the head is reduced and the mouth and anus move to occupy their terminal positions. The prototroch, metatroch, and feeding band disappear. The collar folds evaginate completely to form the adult configuration, and the anterior pair of chaetae becomes collar chaetae. Stiff ciliary tufts are formed on the radiolar rudiments, and all subsequently develop pinnules. The postsettlement development of the radiolar crown and the operculum, as well as the formation of additional thoracic segments, has been described in Ficopomatus enigmaticus, Hydroides elegans, Spirobranchus kraussii and Spirobranchus triqueter. The postmetamorphic development of the nonfeeding planktonic serpulin larvae of Protula tubularia and

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Salmacina dysteri does not differ significantly from that of planktotrophic larvae. Spirorbin larvae are competent to settle when released from the brood chamber, and the duration of swimming lasts up to several hours. After a short pelagic stage, larvae enter a searching stage when swimming alternates with slow crawling on the ventral side. At settlement, in some spirorbins (e. g., Simplaria potswaldi), the contents of the primary shell gland are extruded in an explosive fashion, and the calcareous secretion is molded by larval movements into a complete tube in less than 5 min. In others (e.g., Neodexiospira alveolata and Spirorbis spirorbis), the initial tube is transparent and soft, covering the body only partially, while the formation of the calcareous tube takes up to 1 day. The opercular peduncle and radiolar rudiments develop only after the formation of the initial tube. During further development, the yolk of the midgut breaks is absorbed, the anus takes the terminal position, the abdominal shell gland becomes the hindgut, the partition between the midgut and the hindgut opens, and the radiolar rudiments develop into the crown. The ventral prostomial glands, the apical tuft, and various trochs are lost. By this time, the major features of the adult, except abdominal or secondary segments, are present. The gross asymmetry, characteristic of spirorbins, develops as a result of differential growth in the achaetous zone, which corresponds to the larval abdomen. This change from a symmetrical larva to an asymmetrical preadult completes spirorbin metamorphosis (reviewed by Kupriyanova et al. 2001).

Biology and ecology Distribution Serpulidae are found worldwide, and as most polychaetes were assumed to have naturally wide, or even cosmopolitan, distribution ranges for much of the twentieth century (e.g., Hartman 1959, Day 1961). However, recent studies overwhelmingly show that “cosmopolitan” taxa represent complexes of either similar morphospecies or cryptic species (reviewed in Hutchings and Kupriyanova 2018). The review specifically mentions undeserved cosmopolitan status previously attributed to Serpula vermicularis and Hydroides norvegica. All evidence accumulated to date suggests that serpulids usually have restricted geographic distributions; thus, all taxa species with reported wide distributions should be treated as potential complexes made up of species with restricted ranges. Two general exceptions to the rule of restricted distribution ranges are deep-sea and invasive species. Ranges of deep-sea serpulids are virtually unknown; in view of

environmental conditions unchanging over wide distances, ranges can be expected to be much wider than in shallow seas, a traditional view as reported for other deepsea organisms (e.g., Briggs 1974), also supported by recent studies (e.g., McClain and Schlacher 2015, Higgs and Attrill 2015). Shallow-water serpulids include a number of biofouling taxa that are known to be easily translocated by anthropogenic means and become nonindigenous species (NIS), established in remote localities, thus significantly expanding their ranges (e.g., Ben-Eliahu and ten Hove 1992, Çinar 2006, 2013, Dittmann et al. 2009, Lewis et al. 2006, Link et al. 2009). In his global review, Çinar (2013) listed 46 species of Serpulidae that have been recorded as NIS worldwide. Moreover, biofouling is a major mode of dispersal for some Hydroides (Petengill et al. 2007). Unfortunately, even if a taxon is easily translocated and tends to become invasive, as a result of a dedicated study it may still dissolve into a complex of morphologically distinct species, several cryptic genetically distinct species, or a combination of both. Sun et al. (2017) showed that an important fouling bioinvader Hydroides dianthus (Verrill 1873), described from New England, and established in Europe, Brazil, China and Japan, is made up of two genetically distinct cryptic species within its range. Even more complicated is the situation with another supposedly invasive fouler, Hydroides brachyacantha Rioja, 1941. The species was originally described from the Pacific coasts of Mexico, and later reported from many (sub)tropical localities around the world; it is a complex of an unknown number of species that in Australia alone includes two species, both morphologically and genetically distinct from H. brachyacantha sensu stricto (see Sun et al. 2016). Another example is Ficopomatus enigmaticus (Fauvel, 1923), a cryptogenic reef-building estuarine species reported worldwide and often referred to as the “Australian tubeworm.” Styan et al. (2017) revealed the presence in Australia of three genetic groups (not formally described as species yet) with overlapping ranges, one of which is morphologically distinct from the other two. A nearly cosmopolitan distribution was attributed to the “fouling species” Spiobranchus kraussii (Baird, 1865) and Spiobranchus tetraceros (Schmarda, 1861), supposedly both being widely distributed around the world by anthropogenic means (Zibrowius 1979b, Çinar 2013). However, the most recent studies (Simon et al. 2019, Palero et al. in press) demonstrate that both nominal species represent suites of genetically distinct cryptic species, some of which may be indeed invasive, but certainly not all described yet. Serpulids are most common inhabitants of subtidal and shelf locations, but they can occur at all latitudes from intertidal to hadal depths. Spirorbins have a



worldwide distribution ranging from littoral to abyssal depths, but are most commonly found in the sublittoral zone. Some have relatively wide bathymetric ranges (e.g., Kupriyanova and Badyaev 1998). The best known and most conspicuous serpulids such as representatives of the genera Ficopomatus, Galeolaria, Hydroides, Protula, Salmacina, Serpula, Spirobranchus and Vermiliopsis are inhabitants of shallow waters, and so are representatives of less known and more cryptic genera such as, for example, Chitinopoma, Floriprotis, Josephella, Metavermilia, Pomatostegus, Pseudochitinopoma, Pseudovermilia, Rhodopsis, Semivermilia and Spiraserpula. Some genera, however, may include both subtidal and bathyal species, e.g., Apomatus, Filogranula, Neovermilia and Protula. Deep-sea serpulids are still very poorly studied. Zibrowius (1977) reviewed serpulids from the depths exceeding 2000 m correcting Hartman’s (1971) compendium of abyssal polychaetes and listed 25 species, including only one unidentifiable hadal specimen from the Kermadec Trench collected at 6620 to 6730 m (Kirkegaard 1956). Belyaev (1989) also listed two unidentified Serpulidae from 6410 to 6757 m (Aleutian Trench) and 9715 to 9735 m (Izu-Bonin Trench), the latter being the deepest record for a serpulid. Kupriyanova (1993 a, b) described six new species from the Kurile-Kamchatka Trench area alone. In their recent review, Paterson et al. (2009) reported 26 serpulid species from depths of more than 2000 m worldwide, including five species from abyssal depths greater than 3500 m, all of which described by Kupriyanova (1993 a, b). Kupriyanova et al. (2010, 2011, 2014), Kupriyanova and Nishi (2010), and Kupriyanova and Ippolitov (2015) recently provided new records and descriptions of new deep-sea serpulid taxa, but undescribed species are still numerous. Based on the above, currently reported serpulid species from bathyal and abyssal depths belong to the genera Bathyvermilia, Bathyditrupa, Filogranula, Hyalopomatus, Laminatubus, Neovermilia, Spirodiscus, Protis, Vitreotubus and Zibrovermilia (Kupriyanova et al. 2011, Kupriyanova and Ippolitov 2015), but only representatives of Bathyditrupa, Bathyvermilia, Hyalopomatus, and Protis are typical abyssal taxa also penetrating into the upper hadal zone (Kupriyanova et al. 2011, 2014). Non-operculate Protula and operculate Apomatus are often confused with nonoperculate and operculate Protis sp., so that some abyssal records of supposed Protula and Apomatus in the literature might in fact belong to Protis (Kupriyanova et al. 2014). Ecology Adult serpulids lie in the tube with their dorsum facing the substrate (on their back) and locomotion is limited

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to partial emergence from and withdrawal into the tube (Knight-Jones 1981). Animals retreat into the tube when startled by stimuli associated with predators. While in its tube, a worm is safe but cannot feed; thus, hiding has a lost-opportunity cost, given that in natural habitats good feeding conditions may not last long or recur frequently. The worms seem able to track relatively short-term changes in food availability, comparing current feeding conditions to those recently experienced. Hiding cryptic behavior is a common antipredator tactic, and animals may adjust the durations of such behavior to current benefits and costs, as they perceive them (Dill and Fraser 1997). Serpulids catch suspended food particles with the radioles that in feeding position are extended outside the tube as a crown. The radioles bear lateral pinnules with latero-frontal cilia beating toward the frontal surface of the pinnules, thereby generating a feeding current that is incurrent from below the crown (proximally) and excurrent distally above the crown (reviewed by Fauchald and Jumars 1979). Food particles are retained in a mucous filled groove between opposite pinnules and transported by cilia to the mouth (Thomas 1940). With circular whorls of radioles the incurrent and excurrent streams are clearly separated. In radioles of serpulids with spirally arranged radioles (e.g., some large Spirobranchus spp., the Christmas tree worms, and Protula spp.) shorter radioles of more distal whorls only pass water that has previously passed through every proximal whorl, thus incurrent and excurrent streams are not separated and the animals depend on ambient currents to prevent multiple refiltration of their excurrent stream (Strathmann et al. 1984). As suspension-feeders, serpulids show varying abilities in particle sorting. For Ditrupa arietina that ingests diatoms, haptophytes, bacteria and cyanobacteria, the size spectrum of particles ranges from 1 to 50 µm and the origin of the food is planktonic as well as benthic (Jordana et al. 2001). Significant differences in clearance for different components of the phytoplankton community and high biomass removal (>50% of initial standing stocks) by reefs of Ficopomatus enigmaticus suggest that the species can promote changes in plankton community structure and is capable of regulating planktonic biomass (Pan and Marcoval 2014). Results of Jordana et al. (2000) indicate the existence of pronounced seasonal variations in the feeding activity of D. arietina. Although serpulids, like most polychaetes, are predominately marine organisms, some Hydroides spp. tolerate mixohaline conditions (e.g., Mak and Huang 1982 for H. elegans), whereas representatives of the genus Ficopomatus are especially adapted to cope with a wide range of salinities and are common in brackish-water environments

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worldwide (ten Hove and Kupriyanova 2009). Closely related to Ficopomatus species is Marifugia cavatica, the only known truly freshwater serpulid that inhabits subterranean caves of the Dinaric Alps (Kupriyanova et al. 2009). Serpulids are common on hard substrata in all marine environments. Two bathyal species, Laminatubus alvini and Protis hydrothermica ten Hove and Zibrowius, 1986, are commonly found in hydrothermal vent and cold seep communities, and Kupriyanova et al. (2010) recently reported Hyalopomatus mironovi Kupriyanova, 1993a, and Protis sp. from hydrothermal vents of North Fiji. However, species of Bathyditrupa, Ditrupa, and Spirodiscus are unusual as they adapted to living unattached on soft substrate in subtidal-shelf (Ditrupa) or bathyal-abyssal (Bathyditrupa and Spirodiscus) environments. Many serpulids are notorious opportunistic foulers capable of colonizing any available substrate, including man-made surfaces and other organisms, such as shells of molluscs and crustacean carapaces, as well as algae (mostly Spirorbinae); however, some have very specific habitat requirements. Such habitat selectivity is a result nonrandom larval settlement and juvenile survival. Larval settlement of serpulid larvae is affected by both nonspecific (ambient temperature, salinity, dissolved oxygen and light intensity, physical properties of the substratum, such as its color and roughness) and substratum-specific cues (reviewed by Kupriyanova et al. 2001). Substrate-specific settlement results from active selection by settling larvae, and the settlement cues are mostly chemical in nature. Three main types of substrate-specific settlement are associative settlement, settlement on microbial films, and gregarious settlement. Although a large number of serpulids is found in coral reefs on dead coral rubble (e.g., Bailey-Brock 1985: Fiji; Nishi 1996: Okinawa, Japan; Kupriyanova et al. 2015: Queensland, Australia), only some, such as Floriprotis, Pseudovermilia, Spirobranchus, and Vermiliopsis spp., are found in association with live corals (Martín and Britayev 1998, 2018). Some Spirobranchus species are reported to be obligate associates of corals to the extent that their successful settlement occurs only on live corals (e.g., Hunte et al. 1990, Marsden 1987, Marsden et al. 1990), although recent observations indicate that while they have a preference for corals, they will survive outside (Perry et al. 2018). Spirorbins are commonly found in specific epiphytic associations with macrophytes, and their settlement can be stimulated by algal extracts (Williams 1964, Gee 1965). The presence of a bioorganic film has been long recognized as a prerequisite for larval settlement in serpulids. Bacterial films of various age and composition have different effects on larval settlement (reviewed by Kupriyanova

et al. 2001). Chan et al. (2014) further showed that the application of organic nutrient-rich soil extract induced larval settlement of S. cf. kraussii within 24 h, suggesting that the extract promoted the growth of an inductive biofilm from microbiota present on the larvae. Many serpulid larvae settle in response to the members of their own species to form dense conspecific aggregations. Such gregarious settlement relies on chemical cues associated with the body of live adults (Toonen and Pawlik 1996, Bryan et al. 1997). Both adult-associated chemical cues and bacterial films may affect settlement simultaneously. Toonen and Pawlik (1994) found that two types of larvae of H. dianthus settle in two different ways: one type colonizes uninhabited substrata (founders), whereas the other settles only in response to conspecific-associated cues (aggregators). If founders were removed, the remaining aggregators delayed settlement without acceptable conspecific-associated clues (desperate larvae). Above-mentioned dense serpulid aggregations can be formed as a result of not only gregarious larval settlement but also asexual reproduction, or in some cases a combination of both. Asexual budding results in branching “pseudocolonies” (sensu Nishi and Nishiura 1994) in Filograna/Salmacina and possibly in Filogranella (Hoeksema and ten Hove 2011). Gregarious larval settlement may also lead to dense aggregations of tubes resulting in intertidal belts (e.g., Galeolaria caespitosa, Galeolaria geminoae, and Spirobranchus kraussii) or in the formation of subtidal reefs as in Ficopomatus enigmaticus (reviewed in Dittmann et al. 2009), some Serpula spp. (e.g., Moore et al. 1998), or Galeolaria hystrix (Smith et al. 2005). For a detailed review of serpulid “colonies,” see ten Hove and van den Hurk (1993). Economic importance Serpulidae is one of the most economically important groups of marine annelids as the family includes notorious members of fouling communities and common bioinvaders that travel on ship’s hulls (Thorp et al. 1987, Zibrowius 1991, 2002, Lewis et al. 2006). Gregarious species (commonly of the genera Hydroides, Ficopomatus, and less so of Spirobranchus) can form dense colonies of calcareous tubes on underwater structures such as aquaculture nets, seawater intake pipes (Qiu and Qian 1997), ship hulls and buoys (Wang and Huang 1993), as well as on commercial molluscs (Arakawa 1971). Fouling by gregarious serpulids results in decreasing ship speed, blocking of water pipes, increasing the weight and drag of buoys, and damaging aquaculture infrastructure (Arakawa 1971, BenEliahu and ten Hove 1992, Wang and Huang 1993, Chandra Mohan and Aruna 1994). These impacts lead to high economic costs associated with the removal of tubes from



artificial structures, as well as reduced prices for fouled molluscs sold for human consumption. Although fouling by Ficopomatus enigmaticus negatively affects ships, buoys, harbor structures, and power plant intake pipes, the species also played a fundamental role in the maintenance of water quality of a marina near Cape Town, South Africa (reviewed by Dittmann et al. 2009). Similar possible positive effects of F. enigmaticus feeding have also been discussed by Leung and Cheung (2017), who suggested that the nuisance fouling species can be turned into a natural resource to counter algal blooms. Fossil record Although the fossil record of annelids in general is poor, Serpulidae is a notable exception, as they have the best fossil record among all annelids, being represented mainly by tubes, and, to a lesser degree, by calcified opercula (reviewed in Radwańska 1994b, Gatto and Radwańska 2000). Some recent genera have very distinct tubes (e.g., Janita, Vitreotubus, Neomicrorbis, Placostegus, and Ditrupa) easily recognizable in fossil state (Ippolitov et al. 2014). In others (e.g., Bathyvermilia, part of Filogranula, Semivermilia, Pseudovermilia, Pyrgopolon, and Spiraserpula), tube morphology is important for species distinction, but reliable generic attribution based on tubes alone is difficult because of the high intrageneric variability. Moreover, tubes of large groups (e.g., Apomatus/Protula, Hyalopomatus, Spirobranchus, and Serpula–Hydroides) often show little or no interspecific variability or have a very simple morphology, making their recognition in fossil state problematic. Such from a paleontological point of view, “problematic” genera comprise approximately 55% of recent nonspirorbin serpulids. In Spirorbinae, the situation is even worse, as usually no recent genera, except for the very distinct Neomicrorbis, can be confidently determined by tube morphology alone. The “stumbling block” of understanding serpulid fossil record is obtaining reliable taxonomic interpretations of fossil tubes based on morphology. Luckily, serpulid tubes demonstrate a high variety of ultrastructures and diverse mineralogy, which can be used as new tools for decrypting the fossil record (see Ippolitov et al. 2014, also Figs. 7.4.7.13, 7.4.7.14). Vinn et al. (2008) recognized four main groups of tube ultrastructures in serpulids according to the orientation of calcium carbonate crystals: (1) isotropic structures (the crystallization axis lacks uniform orientation; Fig. 7.4.7.13 A–E), (2) semioriented structures (the crystallization axis has semiuniform orientation; Fig. 7.4.7.3 F, G), (3) oriented prismatic structures (the crystallization axis has a uniform orientation and is continuous through growth increments; Fig. 7.4.7.13 H, I, M–O), and (4) oriented complex structures

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(the crystallization axis of the crystals has a uniform orientation that is not continuous through successive growth increments; Fig. 7.4.7.13 J–L). In total, 13 distinct ultrastructures (Vinn et al. 2008) are currently recognized in recent serpulids (Figs. 7.4.7.3, 7.4.7.4). Ultrastructure can potentially be used to distinguish serpulid taxa and even to verify linking fossils with recent taxa (Kupriyanova and Ippolitov 2015), and thus, they may be crucially important for further interpretation of fossil record and serpulid evolution. The first comprehensive overview of serpulid tube mineralogy by Bornhold and Milliman (1973) provides data for more than 100 specimens belonging to 30 species of 15 genera. The study found correlations of tube mineralogical composition neither with environmental factors nor with taxonomy. However, data on mineralogical composition have been used to test the generic affiliation of serpulids (Ferrero et al. 2005) and to distinguish species within a single genus (e.g., Bornhold and Milliman 1973; followed by ten Hove 1974: 47). Calcite and aragonite are rarely present in equal qualities within one tube, and calcite–aragonite ratio may significantly vary not only among species but also within a species and even within a single specimen during ontogeny (Bornhold and Milliman 1973, Chan et al. 2015). Vinn et al. (2008) found some correlation between mineralogy and ultrastructure. Ancient Ediacaran (580–542 Ma) and Paleozoic (542–252 Ma) rocks contain diverse tubicolous fossils that were erroneously interpreted as serpulids. Cloudina, the most famous tube-building metazoan common in the late Ediacaran Period (549–541 Ma), has been affiliated with serpulids (Germs 1972, Glaessner 1976, Hua et al. 2005). Tube morphology and ultrastructure suggest that Cloudina is not closely related to serpulids (Vinn and Zatoń 2012a). The type of asexual reproduction and presence of a closed tube base in Cloudina is compatible with the hypothesis of an animal of cnidarian affinities (Hua et al. 2005, Vinn and Zatoń 2012a). Paleozoic (541–252 Ma) rocks, especially lower Cambrian around 540 Ma, contain tubular fossils of uncertain affinity, including two fossil groups, Cornulitida and Microconchidae, traditionally described as serpulids. Including them in serpulid fossil record resulted in a long-held controversy regarding the geological age of calcareous polychaetes and in wrong interpretations of evolutionary patterns within the Serpulidae by both zoologists (e.g., Pillai 1970, Knight-Jones 1981) and paleontologists (Jäger 1993: 101). Cornulitids are mostly small (2–5 mm in diameter) marine calcareous tubular fossils ranging from the Middle Ordovician to the Carboniferous (470–300 Ma). Vinn and Zatoń (2012b) place them within the Lophothrochozoa. Microconchids is a Spirorbis-like extinct group of

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Fig. 7.4.7.13: Tube ultrastructure diversity of serpulid tubes. A–E, isotropic structures: A, Serpula crenata, cross section of irregularly oriented prismatic structure (IOP); B, Pseudovermilia madracicola, cross section of spherulitic irregularly oriented prismatic structure (SIOP); C, Neovermilia falcigera, cross section of irregularly oriented platy structure (IOPL); D, Laminatubus alvini, cross section of homogeneous angular crystal structure (HAC); E, Pomatostegus stellatus, cross section of homogeneous rounded crystal structure (HRC). F, G, semioriented structures: F, Protula diomedeae, cross section of semiordered irregularly oriented prismatic structure (SOIOP); G, Pyrgopolon ctenactis, outer tube layer, cross section of semiordered spherulitic irregularly oriented prismatic structure (SOSIOP). H, I and M–O, oriented prismatic structures: H, Spiraserpula caribensis, outer tube layer, longitudinal section of spherulitic prismatic structure (SPHP); I, Vitreotubus digeronimoi, longitudinal section of simple prismatic structure (SP). J–L, oriented complex structures: J, Hydroides dianthus, longitudinal section of lamellofibrillar structure (LF); K, Floriprotis sabiuraensis, inner layer, cross section of spherulitic lamellofibrillar structure (SLF); L, Spirobranchus giganteus, outer layer, longitudinal section of ordered fibrillar structure (OF). M–O, Ditrupa arietina, regularly ridged prismatic structure (RRP): M, tube external surface; N, external tube layer, longitudinal section; O, lateral surface of a RRP structure prism with ridges. From Ippolitov et al. (2014).



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Fig. 7.4.7.14: Schematic presentation of serpulid tube ultrastructures. A, irregularly oriented prismatic (IOP) structure; B, spherulitic irregularly oriented prismatic (SIOP) structure; C, irregularly oriented platy (IOPL) structure; D, homogeneous angular crystal (HAC) structure; E, rounded homogeneous crystal (RHC) structure; F, semiordered irregularly oriented prismatic (SOIOP) structure; G, semiordered spherulitic irregularly oriented prismatic (SOSIOP) structure; H, spherulitic prismatic (SPHP) structure; I, simple prismatic (SP) structure; J, lamellofibrillar (LF) structure; K, spherulitic lamellofibrillar (SLF) structure; L, ordered fibrillar (OF) structure. Regularly ridged prismatic structure (RRP, see Fig. 7.4.7.2 M–O) is similar to SP structure. Abbreviations: H, horizontal section; L, longitudinal section; T, transverse section. From Ippolitov et al. (2014).

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lophophorates, ranging from the Late Ordovician to the Middle Jurassic (458–164 Ma) that inhabited all aquatic environments (Zatoń et al. 2012). Because of their small size (usually 20 teeth in profile, up to 7 teeth in a row; anterior peg blunt, slightly gouged underneath. Achaetous anterior abdominal zone short. Posterior capillary chaetae present. Posterior glandular pad absent. Remarks: WoRMS (accessed 09112018) lists three taxa under this genus: its type species Filogranella elatensis; Filogranella aberrans, a nomen dubium; and Filogranella prampramiana, a taxon inquirendum (additional material checked by one of us, HAtH). Filogranella aggregations have been mentioned from various locations around the world (see ten Hove and Kupriyanova 2009 for details), and some colonies have specimens with opercula with flat chitinous endplates on a flat peduncle inserted as the second dorsal radiole. Apparently, it is a complex of related species that needs to be revised. Filogranula Langerhans, 1884 Type species: Filogranula gracilis Langerhans, 1884 (six species) Diagnosis: Tube white, opaque, with elaborate peristomes; keel present. Granular overlay absent. Operculum with chitinous endplate, may have spines in the center. Peduncle cylindrical, smooth, without wings; inserted as the second dorsal radiole on one side. Opercular constriction present or absent. Pseudoperculum absent. Radioles arranged in semicircles, up to seven per lobe. Interradiolar membrane and stylodes absent. Radiolar eyes may be present. Mouth palps not observed. Seven thoracic chaetigerous segments. Collar generally nonlobed (may be trilobed) with entire edge, continuous with short thoracic membranes, ending at the second thoracic chaetiger.

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Tonguelets absent. Collar chaetae fin-and-blade and limbate. Apomatus chaetae present. Thoracic uncini sawshaped or saw-to-rasp-shaped with 12 to 14 teeth in profile, up to 5 teeth in a row above anterior peg, blunt, gouged underneath (e.g., dental formula P:5:3:3:2:1:1:1:1:1:1:1:1:1). Triangular depression absent. Abdominal chaetae short, flat triangular with wide distal denticulate blade; abdominal uncini rasp-shaped. Achaetous anterior abdominal zone present. Long posterior capillary chaetae present. Posterior glandular pad absent. Remarks: See remarks to Chitinopoma and Chitinopomoides Floriprotis Uchida, 1978 Type species: Floriprotis sabiuraensis Uchida, 1978 (monotypic) Diagnosis: Tube white, opaque, circular in cross section, normally completely embedded into living corals; granular overlay absent. Operculum and pseudoperculum absent. Radioles arranged (semicircular to) short pectinately, up to 20 per lobe. Interradiolar membrane present. Stylodes absent. Radiolar eyes absent. Mouth palps absent. Seven thoracic chaetigerous segments. Collar trilobed with entire edge, tonguelets absent. Thoracic membranes long, apron present. A pair of pockets on the inner side of each thoracic membrane, between the second and the third thoracic segments. Collar chaetae bayonet, with elongate rounded teeth at base of very short blade, and limbate. Apomatus chaetae absent. Thoracic uncini of Serpula type, with four to five teeth and pointed fang. Triangular depression present. Abdominal chaetae flat trumpet-shaped with denticulate edge as in Serpula. Abdominal uncini similar to thoracic ones, saw-shaped with four to five teeth anteriorly, but rasp-shaped (dental formula F:1:1:2:3:3:3:4:3) posteriorly, with one tooth proximally above fang to three teeth per row distally, seven to eight teeth in profile. Long posterior capillary chaetae present. Posterior glandular pad absent. Remarks: The species has the chaetation pattern typical for Crucigera–Hydroides–Serpula–Spiraserpula and is a symbiont of corals in the Indo-West Pacific (ten Hove and Kupriyanova 2009). Preliminary molecular data also support placement of Floriprotis in this clade (Kupriyanova et al. in preparation) Galeolaria Lamarck, 1818 Type species: Galeolaria caespitosa Lamarck, 1818 (three species) Diagnosis: Tube white or pink, opaque, with two longitudinal keels, trapezoidal in cross section. Granular overlay absent. Operculum rather flat ampulla with distal calcareous plate, armed with elaborate movable spines. Peduncle thick, triangular in cross section, with distal

wings; inserted almost mediodorsally, covering the base of up to three to four dorsal radioles; constriction absent. Pseudoperculum absent. Radioles arranged almost in spirals (1.25 whorl), up to 42 per lobe. Stylodes and radiolar eyes absent. Interradiolar membrane present. Mouth palps absent. Seven thoracic chaetigerous segments. Collar trilobed, collar edge entire, smooth, occasionally with frilly edge. Tonguelets absent. Thoracic membranes forming apron. Collar chaetae small, limbate. Apomatus chaetae absent. Thoracic uncini saw-shaped with 7 to 10 teeth, anterior peg stout, rounded to spatulate. Triangular depression absent. Abdominal chaetae true ­trumpet-shaped, smoothly bent, with two rows of denticles separated by a hollow groove and extended into a long lateral spine. Abdominal uncini with 11 to 15 teeth, anterior peg stout, rounded, posterior ones rasp-shaped with two to three rows. Long posterior capillary chaetae absent. Posterior glandular pad absent. Remarks: The genus Galeolaria is endemic to southern Australia and New Zealand, with G. caespitosa beings gregarious and intertidal, whereas G. hystrix is in general solitary and subtidal, but sometimes forming “reefs” (Smith et al. 2005). Halt et al. (2009) examined specimens of G. caespitosa across the intertidal zone of southern Australia using morphological and molecular data to assess the taxonomic status of this morphospecies. They demonstrate that G. caespitosa comprises two cryptic species and described a new species Galeolaria gemineoa. Also, a previously sequenced Australian specimen of G. hystrix is not in the same clade as the New Zealand samples and requires reinvestigation (Smith et al. 2012). Hyalopomatus Marenzeller, 1878 Type species: Hyalopomatus claparedii Marenzeller, 1878 (14 species) Diagnosis: Tube white, opaque, sometimes with external hyaline layer, but granular overlay absent; (semi)circular in cross section. Tabulae may be present. Operculum globular, soft, without distinct endplate or consisting of proximal ampulla with slightly chitinized distal cap; well separated from peduncle by constriction; sometimes operculum absent. Peduncle very thin, cylindrical, smooth, without wings; inserted outside branchial crown proper in front of the first dorsal radiole on one side. However, for Hyalopomatus langerhansi, we observed “between base of first and second radiole.” Pseudoperculum absent. Arrangement of radioles short pectinate, up to 15 pairs of radioles. Interradiolar membrane absent. Radiolar eyes rarely present. Stylodes absent. Mouth palps present. Six thoracic chaetigerous segments. Collar trilobed, tonguelets absent. Thoracic membranes short, ending at the first or the second thoracic chaetiger. Collar chaetae



fin-and-blade, or without gap between fin and blade and thus with uniform distal denticulate wing, and limbate. Apomatus chaetae absent (contrary to Ben-Eliahu and ten Hove 1989). Thoracic uncini rasp-shaped with numerous small teeth, approximately 20 in profile, up to nine teeth in a row above peg; anterior peg made of two rounded lobes with a shallow incision in between, flat or slightly gouged in the middle. Triangular depression absent. Abdominal chaetae thought to be “almost capillary with only tip flat narrow geniculate with pointed teeth;” (ten Hove and ­Kupriyanova 2009: 50); however, recent SEM shows them (at least partly?) with pointed teeth arranged in two rows, thus true trumpet-shaped (e.g., Kupriyanova and Ippolitov 2015). Abdominal uncini rasp-shaped, similar to thoracic ones, but their anterior peg with three to four flat rounded lobes. Achaetous anterior abdominal zone may be present. Posterior capillary chaetae present, but see above. Posterior glandular pad absent. Remarks: The poorly known genus Hyalopomatus is a typical deep-sea (bathyal and abyssal) taxon. Hyalopomatus madreporae Sanfilippo, 2009 from the central Mediterranean and Hyalopomatus dieteri Kupriyanova and Ippolitov, 2015 from New Caledonia were added since the review of ten Hove and Kupriyanova (2009), bringing the number of species to 14. It is currently being revised by Kupriyanova et al. (in preparation) Hydroides Gunnerus, 1768 Type species: Hydroides norvegica Gunnerus, 1768 (more than 100 species) Diagnosis: Tube white (sometimes bluish), more or less circular to trapezoidal (with flattened upper surface) in cross section, peristomes and shallow longitudinal ridges may be present, no distinct keels. A granular overlay may be present. Operculum two-tiered, composed of basal funnel of fused radii and distal verticil (crown) of chitinized spines. Peduncle cylindrical, smooth, without wings, may or may not be separated from opercular funnel by a constriction; formed from the second dorsal radiole on one side. Pseudoperculum present. Arrangement of radioles in semicircles, up to 33 per lobe. Radiolar eyes absent. Interradiolar membrane generally absent, rarely present. Stylodes absent. Mouth palps absent. Seven thoracic chaetigerous segments, exceptionally nine. Collar trilobed, tonguelets absent. Thoracic membranes long, forming ventral apron. Collar chaetae bayonet and limbate. Apomatus chaetae absent. All uncini saw-shaped with relatively few (up to seven) teeth; anterior fang simple pointed. Triangular depression present. Abdominal chaetae flat trumpet-shaped with denticulate edge. Achaetous anterior abdominal zone absent. Posterior capillary chaetae present. Posterior glandular pad absent.

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 247

Remarks: Hydroides is the largest serpulid genus, with a mainly tropical to subtropical distribution. Species in the genus are distinguished by well-differentiated opercula and less so by differences in chaetal and tube structure. Bastida-Zavala and ten Hove (2002, 2003) published revisions of the Hydroides species from the Western Atlantic region, respectively, Eastern Pacific region and Hawaii. Also, Bastida-Zavala and ten Hove (2002) provided a historical review of taxonomic studies of the genus. Sun et al. (2015) revised the genus in Australia, Sun (2017) provided a comprehensive overview of the genus on global scale, and Sun et al. (2018) provided the first major molecular phylogeny of the genus based on half of all known morphospecies. Janita Saint-Joseph, 1894 Type species: Omphalopoma spinosa Langerhans, 1884, = junior synonym of Serpula fimbriata delle Chiaje, 1822 (questionably monotypic) Tube white, subcircular in cross section, with five longitudinal winding keels. Granular overlay absent. Operculum almost inverted bell-shaped, ending in simple thick brown concave endplate; opercular base surrounded by three fleshy processes, one triangular and two rounded ones. Peduncle cylindrical, slightly dorsoventrally compressed and wrinkled; inserted below and between the first and the second normal radioles (below second in larger specimens). Pseudoperculum absent. Arrangement of radioles short pectinate, up to 12 radioles per lobe. Interradiolar membrane and stylodes absent. Radiolar eyes present. Mouth palps present. Seven thoracic chaetigerous segments. Collar pentalobate, medioventral lobe divided by a deep median and two shallow incisions. Tonguelets absent. Thoracic membranes short, ending at the second thoracic chaetiger. Collar chaetae of Spirobranchus-type, acicular and limbate. Apomatus chaetae present. Thoracic uncini saw-shaped with up to 16 teeth, anterior peg blunt, questionably gouged. Triangular depression absent. Anterior abdominal uncini sawshaped, posterior rasp-shaped, with approximately 13 teeth in profile, 3 to 5 teeth per row. Abdominal chaetae flat narrow geniculate, with a more or less crenulated edge to the blade. Achaetous anterior abdominal zone very short or absent. Long posterior capillary chaetae absent. Posterior glandular pad present. Remarks: The attributed distribution of this species in (sub)tropical Atlantic, Mediterranean, Indo-West Pacific (ten Hove and Kupriyanova 2009) is unlikely, so Janita fimbriata is likely a species complex. Josephella Caullery and Mesnil, 1896 Type species: Josephella marenzelleri Caullery and Mesnil, 1896 (questionably monotypic)

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 7.4 Sedentaria: Sabellida/Spionida

Diagnosis: Tube white, opaque, circular in cross section, with small peristomes; tube diameter approximately 0.1 mm. Granular overlay absent. Operculum delicate membranous cup with a flat distal surface surmounted by a marginal crown of fine teeth joined by a transparent membrane. Peduncle second nonmodified pinnulate radiole. Pseudoperculum absent. Radioles arranged in semicircles, up to three per lobe. Interradiolar membrane absent. Radiolar eyes absent, a pair of red ocellar clusters at the base of collar. Stylodes absent. Mouth palps absent. Five thoracic chaetigerous segments. Collar nonlobed. Tonguelets absent. Thoracic membranes short, ending at the first chaetiger. Collar chaetae limbate. Apomatus chaetae present. Uncini rasp-shaped, with 10 to 12 teeth seen in profile, 4 teeth in a row distally to 7 above the peg. Anterior peg gouged, widened into a rectangular to trapezoid base, flat, but with sharp angles that sometimes curve underneath (thus giving a bifurcate appearance under compound microscope). Triangular depression absent. Abdominal chaetae flat narrow geniculate with pointed denticulate edge. Abdominal uncini with 9 to 10 teeth in a row. Achaetous anterior abdominal zone long. Posterior capillary chaetae absent. Posterior glandular pad absent. Remarks: This tiny serpulid, known from numerous circum(sub)tropical, temperate locations around the world (see ten Hove and Kupriyanova 2009), is likely a species complex. Kimberleya Pillai, 2009 Type species: Kimberleya hutchingsae Pillai, 2009 (monotypic) Diagnosis: Tube white, almost circular in cross section, with free anterior end, coiled upon itself. Surface with fine transverse markings and granular overlay, especially along ridges and laterally; anteriorly a pair of faint, broad, smooth, longitudinal ridges; a shallow lateral longitudinal groove recognizable along each side. Operculum absent. Radioles arranged semicircularly; interradiolar membrane absent. Thoracic membranes ending in apron. Thorax with 10 chaetigers. Special collar chaetae absent. Apomatus chaetae present; uncinal tori occur from the 3rd to the 10th chaetigers; thoracic and anterior abdominal uncini rasp-shaped, their most anterior uncinal process simple and elongated; anterior abdominal chaetae geniculate. Remarks: Kimberleya hutchingsae that lacks uncini on the second thoracic chaetiger and has 10 thoracic chaetigers is similar to Membranopsis inconspicua, a species with 9 thoracic chaetigers that is most likely synonymous with Salmacinopsis setosa Bush, 1910 (see ten Hove and Kupriyanova 2009). Salmacinopsis was referred to Protula

setosa by Perkins (1998: 95). Moreover, specimens with or without thoracic uncini may occur within a single population of Protula tubularia (see ten Hove and Pantus 1985). Because the generic name had not been formally synonymized yet, we mention it in this account, but K. hutchingsae is likely to belong to the genus Protula. Laminatubus ten Hove and Zibrowius, 1986 Type species: Laminatubus alvini ten Hove and Zibrowius, 1986 (monotypic) Diagnosis: Tube white, more or less triangular in cross section, with large undulating longitudinal keel; consisting of two layers: an inner opaque layer and an outer (not granular) hyaline one. Operculum globular, with bulbous proximal ampulla and more or less flattened distal endplate with thickened cuticle. Peduncle cylindrical, gradually merging into opercular ampulla, constriction absent; inserted to the left side, proximal from the first and the second normal radioles. Pseudoperculum absent. Radioles not connected by interradiolar membrane, arranged into slightly ascending spiral of up to two whorls. Up to 33 radioles per lobe. Stylodes and radiolar eyes absent. Mouth palps not observed. Six thoracic chaetigerous segments. Collar with medioventral and two laterodorsal lobes, continuous with thoracic membranes, forming apron. Tonguelets absent. Collar chaetae Spirobranchus-type and limbate. Apomatus chaetae absent. All uncini saw-shaped with five to seven teeth, anterior fang simple, pointed. Thoracic tori converging posteriorly, forming triangular depression. Abdominal chaetae long, with hollow trumpet-shaped tip, smoothly bent. Posterior chaetae become longer, but posterior capillary chaetae absent. Posterior glandular pad absent. Remarks: Laminatubus alvini is a bathyal species commonly found in the periphery of hydrothermal vents communities. Marifugia Absolon and Hrabĕ, 1930 Type species: Marifugia cavatica Absolon and Hrabĕ, 1930 (monotypic) Diagnosis: Tube white, opaque, circular in cross section; irregular longitudinal keel and collar like rings may be present. Thin hyaline granular overlay of tube present. Operculum fig-shaped to inverse conical, with (or without) chitinous endplate. Peduncle flattened cylindrical, smooth, without distal wings, gradually merging into opercular ampulla; inserted just below and between the first and the second dorsal radioles on the left side (in large specimen almost covering base of branchial lobe). Pseudoperculum absent. Radioles arranged in semicircles, up to six per lobe. Interradiolar membrane, radiolar



eyes, and stylodes absent. Mouth palps not found. Six thoracic chaetigerous segments. Collar nonlobed but with low medioventral projection. Thoracic membranes narrow but forming apron. Tonguelets absent. Collar chaetae absent. Thoracic chaetae limbate, Apomatus chaetae absent. Thoracic uncini saw-to-rasp-shaped, with about eight teeth in profile, up to four in a row above blunt almost square shallowly gouged anterior peg (dental formula P:4:3:2:1:1:1:1:1). Triangular depression absent. Abdominal chaetae true trumpet-shaped, long, smoothly bent, with hollow tip bordered with pointed teeth. Posterior abdominal capillaries not observed. Uncini saw-to-rasp-shaped; anterior peg simple rounded. Achaetous anterior abdominal zone, long posterior capillary chaetae and glandular pad absent. Remarks: Marifugia cavatica is unique in being the world’s only freshwater serpulid, of marine origin, inhabiting subterranean waters of the Dinaric karst of the former Yugoslavia. Kupriyanova et al. (2009) summarized data on the ecology, distribution, and reproduction of the species and based on phylogenetic analysis of molecular data, placed Marifugia as a sister group to a clade of the brackish-water genus Ficopomatus. Metavermilia Bush, 1905, sensu Zibrowius 1971 Type species: Vermilia multicristata Philippi, 1844 (15 species) Diagnosis: Tube white, opaque, peristomes may be present, as well as several longitudinal keels, sometimes denticulate. Granular overlay generally absent. Operculum with chitinous, noncalcified endplate, sometimes with complex multitiered structures, or endplate may be absent. Peduncle flattened, ribbon-like, without distal wings; formed from the second dorsal radiole on one side. Constriction may be present. Pseudoperculum may be present. Radioles arranged in semicircles to short pectinate, up to 18 per lobe. Interradiolar membrane and stylodes absent. Radiolar eyes may be present. Mouth palps absent. Seven thoracic chaetigerous segments. Collar trilobed, tonguelets between ventral and lateral collar lobes absent. Length of thoracic membranes variable, ending at thoracic segments 3 to 7, sometimes forming ventral apron on anterior abdominal segments. Collar chaetae limbate. Apomatus chaetae present. Thoracic uncini sawshaped with up to 15 teeth, anterior peg blunt, rounded. Triangular depression absent. Abdominal chaetae with flat narrow geniculate blade with rounded teeth; uncini saw- or rasp-shaped. Achaetous anterior abdominal zone absent. Posterior capillary chaetae and glandular pad present. Remarks: Nishi et al. (2007) provided the first taxonomic review of the genus since Zibrowius (1971). Metavermilia

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 249

zibrowii Bailey-Brock and Magalhaes, 2012, was added to Metavermilia since the review of ten Hove and Kupriyanova (2009). Microprotula Uchida, 1978 Type species: Microprotula ovicellata Uchida, 1978 (monotypic) Diagnosis: Tube white, opaque, circular in cross section, proximal part irregularly coiled and attached to substrate, distal erect, and free. Granular overlay absent. Globular ovicells around erect distal part of the tube. Operculum and pseudoperculum absent. Arrangement of radioles semicircular, up to four per lobe. Interradiolar membrane and stylodes absent; 8 to 12 pairs of red ocellar clusters present on both sides of each radiole. Mouth palps absent. Seven thoracic chaetigerous segments. Collar well developed, with four weakly expressed lobes. Tonguelets absent. Thoracic membranes narrow, but forming apron. Collar chaetae limbate. Apomatus chaetae present. Thoracic and abdominal uncini rasp-shaped, Protula-type, up to approximately 20 teeth in profile, up to 6 in a row; anterior peg elongated, blunt, questionably gouged. Triangular depression absent. Abdominal chaetae sickle-shaped with blunt teeth. Achaetous anterior abdominal zone short. Long posterior capillary chaetae present. Posterior glandular pad absent. Remarks: The taxon is morphologically similar to small representatives of the genus Protula (hence the name). The major reason of its elevation into a separate genus has been the presence of tube ovicells used to brood embryos. Microprotula may not have a phylogenetic basis, as some Protula species do show incubation of embryos (Kupriyanova et al. 2001), admittedly not in special brood chambers but in gelatinous masses. The type material was reexamined by EK in 2007. Neovermilia Day, 1961 Type species: Neovermilia capensis Day, 1961 (six species) Diagnosis: Tube white, opaque, triangular to subcircular in cross section, medial keel may be present. Granular overlay absent, although hyaline inner (bordering lumen) and hyaline outer layers may be present. Tabulae occasionally present. Operculum globular, soft proximally, at most with slightly chitinized, or sclerotized, or calcified cap. Operculum absent in one species. Peduncle subcylindrical to triangular, wrinkled (annulated), sometimes with small distal laterodorsal “winglets” (flattened parts of the peduncle), constriction present; inserted at base of the first to the fourth normal radioles. Pseudoperculum absent (but see remarks). Radioles arranged in semicircles to short spiral (1.5 whorls), up to 50 per lobe. Interradiolar

250 

 7.4 Sedentaria: Sabellida/Spionida

membrane present (that is, radioles fused basally for approximately 1/20th of their length). Stylodes absent. Radiolar eyes not observed. Mouth palps absent. Seven thoracic chaetigerous segments. Collar trilobed, tonguelets between ventral and lateral collar lobes absent. Thoracic membranes forming ventral apron across anterior abdominal segment. Collar chaetae limbate. Apomatus chaetae absent. Thoracic uncini saw-shaped with five to six teeth above pointed anterior fang; saw-to-rasp-shaped in one species. Triangular depression absent, but rows of thoracic tori converge, completely touching one another medioventrally. Abdominal chaetae long, true trumpet-­ shaped, smoothly bent, with hollow end bordered by two rows of pointed teeth. Abdominal uncini similar to thoracic ones, with seven teeth above fang. Achaetous anterior abdominal zone absent. Posterior capillary chaetae and glandular pad absent. Remarks: The genus includes both shallow-water and bathyal species. The type species, Neovermilia capensis, is known from False Bay, South Africa, and whether all six attributed species, especially bathyal ones, really belong to this genus is unclear. Omphalopomopsis Saint-Joseph, 1894 Type species: Omphalopoma langerhansi Marenzeller, 1885 (monotypic) Diagnosis: Tube subcylindrical, white, opaque, with three denticulate keels and an occasional low collar-like ring. Granular overlay not observed. Operculum bulbous with slightly convex brilliantly white calcareous endplate. Peduncle cylindrical, broadening, and wrinkled toward opercular ampulla, constriction present; without wings, but two small swellings near ampulla insertion unknown. Pseudoperculum absent. Up to 25 pairs of radioles, arranged in two circles/short spires. Interradiolar membrane absent. Radiolar eyes, stylodes, and mouth palps not observed. Seven thoracic chaetigerous segments. Collar trilobed, well developed, especially medioventrally; thoracic membranes wide till the third segment, extending beyond the last thoracic chaetiger, but apron absent. Tonguelets unknown. Collar chaetae with numerous hairlike processes basally (Spirobranchus-type) and limbate. Apomatus chaetae present from chaetiger 3. Thoracic uncini saw-shaped, with seven to eight teeth above anterior pointed fang. Triangular depression unknown. Abdominal chaetae flat narrow geniculate, longer posteriorly. Uncini saw-shaped anteriorly with seven teeth and fang, rasp-shaped posteriorly. Achaetous zone not known. Long posterior capillary chaetae present. Posterior glandular pad not observed. Remarks: The taxon was known only from the holotype deposited in the Natural History Museum of Vienna,

NHMW A.N.14552, Inv. no. 2054. A new record of the species is provided by Bailey-Brock and Magalhaes (2012), used for an update of the diagnosis above. Paraprotis Uchida, 1978 Type species: Paraprotis dendrova Uchida, 1978 [one (two?) species] Diagnosis: Tube white, opaque, circular in cross section, without longitudinal keels. Granular overlay not observed. Operculum and pseudoperculum absent (or soft globular operculum may be present on the second unmodified radiole in Paraprotis pulchra). Arrangement of radioles semicircular or short pectinate, up to six per lobe (up to 32 per lobe in P. pulchra). Interradiolar membrane absent. Radiolar eyes (ocellar clusters) present. Stylodes absent. Mouth palps absent, but a spiral projection for brood attachment originates from the right side of the mouth. Collar nonlobed, tonguelets absent. Thoracic membranes narrowing at the third chaetiger but continuing to the seventh thoracic chaetiger, a narrow apron is probably present (neither Uchida’s description nor an additional specimen SAM E3591 give a definite answer). Seven thoracic chaetigerous segments. Collar chaetae limbate. Apomatus chaetae absent. Thoracic uncini of Protis-type, saw-shaped with approximately 10 teeth, anterior fang with pointed tip. Thoracic triangular depression not observed. Anterior abdominal chaetae flat narrow geniculate with a row of sharp teeth along its free margin. Abdominal uncini similar to thoracic ones but rasp-shaped. Achaetous anterior abdominal zone present, short (two to four segments). Long posterior capillary chaetae present. Posterior glandular pad not observed. Remarks: Imajima (1979) described Protis pulchra from Japan. Both species have a similar chaetation pattern; however, some specimens of P. pulchra have a thin globular operculum. Also, P. pulchra has a well-developed trilobed collar, an interradiolar membrane, and uniformly wide thoracic membranes unlike Paraprotis dendrova, with its poorly developed nonlobed collar, bright ocellar clusters on its radioles but lacking an interradiolar membrane, and thoracic membranes that narrow at the third thoracic chaetiger. Spiral brooding projections typical for P. dendrova have not been mentioned for P. pulchra. Because of all the differences, P. pulchra apparently does not belong to the genus Paraprotis (fide ten Hove 1984), which is also supported by molecular sequence data (Kupriyanova et al. in preparation). Paumotella Chamberlin, 1919 Type species: Paumotella takemoana Chamberlin, 1919 (monotypic) Diagnosis: Tube unknown. Operculum inverse conical, the distal chitinous endplate slightly depressed, without processes. Opercular peduncle smooth, flattened circular



in cross section, with long basal lateral wing; insertion just outside radioles, covering base of four to five radioles. Pseudoperculum absent. Arrangement of radioles in semicircles, up to 21 per lobe. Interradiolar membrane absent. Radiolar eyes not found in preserved material, stylodes absent. Mouth palps present. Seven thoracic chaetigerous segments. Collar trilobed, with entire edge. Thoracic membranes narrowing abruptly between the fourth and the fifth segments, where they end; no apron. Tonguelets absent. Collar chaetae limbate. Apomatus chaetae present. Thoracic uncini saw-shaped, with 12 teeth above rounded peg. Thoracic triangular depression present. Anterior and median abdominal regions with stout, moderately curved, acute, slightly compressed acicular chaetae; posteriorly long capillaries with distal limbus; uncini rasp-shaped, with approximately 10 teeth in profile, 2 to 3 teeth in a row above peg. Achaetous anterior abdominal zone short, two to three segments only. Posterior glandular pad absent. Remarks: Because the original description of this monotypic genus was not up to the present standards, a new description was given by ten Hove and Kupriyanova (2009). The characteristic features of the genus, according to Chamberlin (1919), are the abdominal chaetae that are neither denticulate nor geniculate, but acicular. From the fact that Fauchald (1977: 145) attributes wings to the opercular peduncle, a character not mentioned by Chamberlin (1919), ten Hove and Kupriyanova (2009) infer that he probably saw the holotype. However, but for the presence of the absolutely unique abdominal chaetae, the taxon could easily be mistaken for a species of the genus Vermiliopsis. Placostegus Philippi, 1844 Type species: Serpula tridentata Fabricius, 1780 [seven (six?) species] Diagnosis: Tube triangular in cross section, with denticulate keels, transparent or semitransparent, often only attached to substratum at the base, collar-like rings absent. Granular overlay absent. Operculum inverse conical, with chitinous cup-shaped endplate. Peduncle cylindrical, smooth, without wings, gradually merging into operculum, at most with shallow constriction; inserted at base of radioles on one side between the first and the second normal radioles and maximally covering base of the first three radioles. Pseudoperculum absent. Radioles arranged in semicircles, up to 24 per lobe; interradiolar membrane, radiolar eyes, and stylodes absent. Mouth palps present. Six thoracic chaetigerous segments. Collar tri- to pentalobed, collar edge may be almost laciniate; tonguelets between ventral and lateral collar lobes present. Thoracic membranes long, forming ventral apron across anterior abdominal segment. Collar chaetae absent; collar region with girdle of reddish

7.4.7 Serpulidae Rafinesque, 1815 

 251

ocelli. Apomatus chaetae absent. All uncini subrectangular, rasp-shaped with >20 teeth in profile, and up to 8 small teeth in a row; anterior peg wide, flat, bluntly truncate, almost rectangular. Thoracic triangular depression absent. Abdominal chaetae true trumpet-shaped, with distal hollow triangular blade, abruptly bent. Achaetous anterior abdominal zone present. Long posterior capillary chaetae may be present. Posterior glandular pad absent. Remarks: Placostegus is one of several serpulid genera with an entirely vitreous tube. Placostegus has one evident diagnostic autapomorphy—the belt of bright red ocelli (Fig. 7.4.7.2  N) in the region where in other genera collar-chaetae are found. The type species, Placostegus tridentatus, has been reported from the Atlantic Ocean, Mediterranean Sea, and Indo-West Pacific (see ten Hove and Kupriyanova 2009), which is an unlikely distribution suggesting that the nominal taxon is a species complex. The suggestion is supported by preliminary DNA sequence data (Kupriyanova et al. in preparation). Pomatostegus Schmarda, 1861 Type species: Pomatostegus macrosoma Schmarda, 1861, junior synonym of Terebella stellata Abildgaard, 1789 (three species) Diagnosis: Tube white, opaque, semicircular to roughly triangular in cross-section, with up to five longitudinal keels; granular overlay absent. Operculum a flat ampulla covered with chitinous disk bearing a column with several serrated disks alternating with circlets of spines proximally and closely applied to each disk. Peduncle flatly triangular in cross-section with broad laterodistal wings along its entire length; inserted to the left or right at the basis of the branchial lobe, constriction absent. Pseudoperculum absent. Arrangement of radioles in (semi)circles, up to 90 per lobe. Interradiolar membrane present. Radiolar eyes present. Stylodes absent. Mouth palps absent. Seven thoracic chaetigerous segments. Collar tri- to pentalobed, well developed with an entire smooth margin. Tonguelets absent. Thoracic membranes short, ending just posterior to the second row of uncini (segment 3). Collar chaetae Spirobranchus-type, with basal pilose fin and distal blade, and limbate. Apomatus chaetae present. Thoracic uncini saw-shaped, with 9 to 13 teeth, anterior peg blunt. Thoracic tori meet ventrally in larger specimens; in juveniles, the ventral space between thoracic tori narrowing toward last rows that almost fused, leaving a triangular depression. Abdominal chaetae flat narrow geniculate, with long blade. Abdominal uncini smaller than thoracic ones, with about eight teeth in profile, three teeth in a row. Achaetous anterior abdominal zone absent. Long posterior capillary chaetae absent, but posterior chaetae longer. Posterior glandular pad absent.

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 7.4 Sedentaria: Sabellida/Spionida

Remarks: The taxon is currently being revised (BastidaZavala, personal communication). Protis Ehlers, 1887, emend. Rzhavsky et al. 2013 Type species: Protis simplex Ehlers, 1887 (seven accepted species, one nomen dubium, and one taxon inquirendum) Diagnosis: Tube white, opaque, with or without keels, flaring peristomes absent. Granular overlay absent. Operculum absent or one or more membranous globular opercula present on normal pinnulate radiole. Arrangement of radioles pectinate, up to 20 per lobe. Interradiolar membrane absent. Radiolar eyes not observed. Stylodes absent. Mouth palps absent. Seven (six in Protis akvaplani Rzhavsky, Kupriyanova and Sikorski, 2013) thoracic chaetigers. Collar trilobed with entire edge, tonguelets absent. Thoracic membranes typically to the end of thorax (midthorax in P. akvaplani) and usually forming ventral apron. Collar chaetae fin-and-blade and limbate. Apomatus chaetae present. Thoracic uncini saw-shaped with about six teeth, anterior fang simple pointed. Triangular depression absent. Abdominal chaetae flat narrow geniculate with rounded teeth. Abdominal uncini rasp-shaped in all segments, with up to six teeth in profile, approximately five to seven teeth in a row above fang. Achaetous anterior abdominal zone absent. Long posterior capillary chaetae present. A posterior glandular pad may be present. Remarks: Protis is one of the typical deep-sea (bathyal and abyssal) serpulid groups (along with Bathyditrupa, Bathyvermilia, and Hyalopomatus), also penetrating into the hadal zone (Kupriyanova et al. 2014). The taxonomy of the genus is challenging because chaetae, uncini, and tubes are very similar and opercula, if present, are undifferentiated. Protis akvaplani differs from other species of the genus by its tube with a high longitudinal keel, six thoracic chaetigerous segments, and short thoracic membranes ending after the third chaetiger. Whether Protis spp. found at 5670 to 9735 m (see Kupriyanova et al. 2014) belong to one or several species remains unknown. Protula Risso, 1826 Type species: Protula rudolphi Risso, 1826, junior synonym of Serpula tubularia Montagu, 1803 (18 accepted species, 1 subspecies, and 7 taxa inquirenda) Diagnosis: Tube white, opaque, may be up to 2 cm across and 40 cm long, (semi)circular in cross section, longitudinal keels and flaring peristomes absent. Operculum and pseudoperculum absent. Radioles arranged in two semicircles to a spire of up to six whorls, up to 320 per lobe (Protula superba). Interradiolar membrane present. Radiolar eyes may be present. Stylodes absent. Mouth palps present. Seven thoracic chaetigerous segments (nine in Protula setosa). Collar trilobed, tonguelets absent.

Thoracic membranes long and wide, with undulating edge, forming ventral apron across anterior abdominal segments. Collar chaetae limbate. Apomatus chaetae present. Thoracic and abdominal uncini rasp-shaped with approximately 30 teeth in profile, up to six rows of teeth above and continuing onto elongated rounded peg. Thoracic triangular depression absent. Abdominal chaetae sickle-­shaped, with finely denticulate blades, may be retrogeniculate in some taxa. Achaetous anterior abdominal zone absent. Long posterior capillary chaetae present. Posterior glandular pad present. Remarks: The genus Protula is the most problematic serpulid taxon, and it has been pointed out that the phylogenetic basis for this genus is ill-defined (see ten Hove and Kupriyanova 2009). This is illustrated as well by WoRMS (09112018): with seven taxa inquirenda against 18 accepted species and 1 subspecies, which probably should be elevated to full specific rank. Pseudochitinopoma Zibrowius, 1969, emend. Kupriyanova et al. 2012 Type species: Hyalopomatopsis occidentalis Bush, 1905 (five species) Diagnosis: Tube white opaque, with longitudinal keel, subtriangular or triangular in cross section, with occasional scooped peristomes. Hyaline granular overlay may be present. Operculum inverse conical with distal chitinous shallow cap. Peduncle circular to rounded triangular in cross section, about twice as wide as radiole, without wings or pinnules, separated from ampulla by constriction; inserted at base of left branchial lobe, in front of the first radiole or almost midway between branchial lobes. Pseudoperculum absent. Radioles in semicircles to short pectinate arrangement, with up to 10 radioles per lobe, interradiolar membrane absent. Radiolar eyes absent. Mouth palps absent. Six or seven thoracic chaetigerous segments. Collar trilobed, tonguelets between median and laterodorsal lobes absent. Thoracic membranes short, ending at the chaetiger 2. Collar chaetae fin-andblade, with a distal limbate zone and a proximal wing not well separated, and limbate chaetae. Apomatus chaetae absent. Thoracic uncini saw-shaped, with approximately 12 teeth above gouged peg. Triangular depression absent. Abdominal chaetae true trumpet-shaped, narrow and smoothly bent, with long lateral tip. Abdominal uncini rasp-shaped, with 12 to 14 teeth in profile, 3 to 6 teeth in a row above gouge-shaped peg. Achaetous anterior abdominal zone absent. Long posterior capillary chaetae and posterior glandular pad absent. Remarks: Kupriyanova et al. (2006) provided preliminary molecular evidence that Pseudochitinopoma and Chitinopoma are not closely related. Kupriyanova et al. (2012)



revised this poorly known genus. Based on examination of the type material, they referred Ficopomatus capensis Day, 1961, to Pseudochitinopoma and described two new species, Pseudochitinopoma amirantensis from the Seychelles and Pseudochitinopoma beneliahuae from Western Australia and the Red Sea. Pseudoprotula Pillai, 2009 Type species. Pseudoprotula kimberleyensis Pillai, 2009 (monotypic) Diagnosis: Tube unknown. Operculum and pseudoperculum absent. Radioles arranged in two semicircles. Interradiolar membrane unknown. Radiolar eyes unknown. Stylodes absent. Mouth palps not mentioned in original diagnosis. Seven thoracic chaetigerous segments. Collar trilobed, tonguelets absent. Thoracic membranes terminating on the fifth thoracic chaetiger, apron absent. Special collar chaetae absent. Apomatus chaetae present. Thoracic uncini rasp-shaped, their most anterior tooth simple and elongated. Thoracic triangular depression not evident in Pillai’s fig. 2H. Abdominal chaetae unknown. Achaetous anterior abdominal zone apparently absent. Long posterior capillary chaetae unknown. Posterior glandular pad present. Remarks: Pillai (2009) erected the genus Pseudoprotula simply based on the absence of an apron in P. kimberleyensis. The description of the species based on two specimens is very cursory, not up to modern standards, with a number of important characters missing. Abdominal chaetae are called “geniculate,” an umbrella term lumping a number of completely different chaetal types as shown by ten Hove and Kupriyanova (2009). Because the generic name had not been formally synonymized yet, we mention it here, but P. kimberleyensis is likely to belong to the genus Protula Risso, 1826. Pseudovermilia Bush, 1907 Type species: Spirobranchus occidentalis McIntosh, 1885 (10 species) Diagnosis: Tube white (in one species with transverse brown bands), opaque, with longitudinal keel(s), subtriangular or triangular in cross section; generally with regular ornamentation of ribs, pits, or teeth. Double or single brooding scoops may be present. Granular overlay absent. Operculum consisting of bulbous ampulla terminated by chitinous endplate or cap, usually with spine(s). Pseudoperculum absent. Peduncle smooth, cylindrical, without wings, clearly separated from ampulla by constriction; inserted just below and between the first and the second radioles on one side. Arrangement of radioles pectinate, up to 17 per lobe, interradiolar membrane absent. Radiolar eyes not known. Stylodes absent. Filiform mouth palps present. Seven thoracic chaetigerous segments. Collar with

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unpaired medioventral lobe and two laterodorsal lobes continuous with short thoracic membranes, continuing to the second thoracic chaetiger. Tonguelets between ventral and lateral collar lobes absent. Collar chaetae limbate. Apomatus chaetae present from the second or the third chaetiger onward. Thoracic uncini saw-shaped, with 9 to 17 teeth above gouged peg (seemingly bifurcate). Triangular depression absent. Abdominal chaetae flat narrow genic­ ulate, with rounded teeth on edge. Abdominal uncini raspshaped with 9 to 13 teeth in profile view, up to 6 teeth in a row above gouged peg. Short achaetous anterior abdominal zone may be present. Long posterior capillary chaetae present. Posterior glandular pad may be present. Remarks: The original diagnosis of Bush (1905) was emended by Zibrowius (1970b) and further emended by ten Hove (1975). Pyrgopolon de Montfort, 1808 Type species: Pyrgopolon mosae de Montfort, 1808 (a Cretaceous taxon; three Recent species) Diagnosis: Tube white or pinkish/red, opaque, generally with longitudinal ridges and/or transverse rims; tabulae may be present. Cross-section semicircular to trapezoidal, erect part polygonal. A hyaline, granular overlay may be present. Operculum funnel-shaped, with numerous radial ridges on distal inner side; operculum and peduncle entirely calcified, with an extremely long calcareous talon embedded into the tissue of peduncle that is inserted medially. Pseudoperculum absent. Radioles arranged in semicircles, up to 38 per lobe, united by interradiolar membrane for one-fourth to one-half of their length, surrounding pair of well-developed mouth palps. Radiolar eyes not observed, but the brim of skin around the operculum scalloped, due to a circle of compound eyespots. Stylodes absent. Seven thoracic chaetigerous segments, although collar chaetae generally missing. Collar with large, bilobed ventral part; tonguelets between lateral and ventral collar lobes present. Thoracic membranes very wide anteriorly, narrowing at the third or fourth segment, and united ventrally on the first abdominal segment forming an apron. Collar chaetae (if present) Spirobranchus-like and limbate. Apomatus chaetae absent. Thoracic uncini saw-shaped, with eight to nine teeth, anterior peg bluntly truncated, indented anteriorly. Thoracic tori almost touching ventrally in posterior thoracic segments of larger specimens, leaving a clear triangular depression. Abdominal chaetae almost capillary, with short hollow true trumpet-shaped tips, smoothly bent and with double row of pointed teeth extending in long lateral spine. Abdominal uncini rasp-shaped with 8 to 11 teeth in profile, 2 to 3 teeth in a row. Achaetous anterior abdominal zone absent. Short capillary chaetae present posteriorly. Posterior glandular pad, if present, hardly visible.

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 7.4 Sedentaria: Sabellida/Spionida

Remarks: The distinguishing feature (autapomorphy) of the genus is the funnel-shaped calcareous operculum continuing into a calcareous peduncle (talon). Sclerostyla Mörch, 1863 has been synonymized with fossil Pyrgopolon by Jäger (1993, 2004). Although very common in the Caribbean, the taxon is poorly known, and ten Hove’s (1973) revision remains the most comprehensive source of information about this genus. Rhodopsis Bush, 1905 Type species: Rhodopsis pusilla Bush, 1905 (two species) Diagnosis: Tube white, circular in cross section, thin walled, not increasing in diameter, distal part sometimes erect, unattached, with peristomes; granular overlay absent. Animals with tube diameter 12) in profile, two to three teeth per row (dental formula P:3:3:3:2:2:1:1:1:1:1:1:1:1); anterior peg gouged (Spirobranchus-type). Abdominal chaetae short, with flat triangular denticulate blade. Thoracic triangular depression absent. Abdominal uncini similar to thoracic ones. Achaetous



anterior abdominal zone absent. Long posterior capillary chaetae absent. Posterior glandular pad absent. Remarks: The Recent genus Spirodiscus Fauvel, 1909 was synonymized with the fossil Nogrobs de Montfort, 1808 by Jäger (2004), which was followed by ten Hove and Kupriyanova (2009). Kupriyanova and Nishi (2011) summarized all published to date material and provided new records of this enigmatic bathyal serpulid. Kupriyanova and Ippolitov (2015) revised deep-sea serpulids with tetragonal (and secondary octagonal) tubes and compared their tube ultrastructures with those of morphologically similar fossil tubes. Because comparisons showed significant ultrastructural differences between Recent and Mesozoic species, they concluded that the genus Spirodiscus should be reinstated. Revision of Recent material by Kupriyanova and Ippolitov (2015) revealed three species with tetragonal tubes: one belonging to the genus Bathyditrupa, B. hovei, and two to the genus ­Spirodiscus, S. grimaldii and S. groenlandicus (McIntosh, 1877), the latter species previously known only from empty tubes, as Ditrupa groenlandica. Tanturia Ben-Eliahu, 1976 Type species: Tanturia zibrowii Ben-Eliahu, 1976 (monotypic) Diagnosis: Tube unknown, tiny specimens (0.9–2.17 mm in length) were extracted from vermetid reefs. Operculum globular to inverse conical ampulla covered with flat to convex chitinous endplate. Peduncle smooth, without distal wings, inserted as the second radiole; constriction absent. Pseudoperculum absent. Arrangement of radioles in semicircles, up to three per lobe. Interradiolar membrane and stylodes absent, radiolar eyes not observed. Mouth palps unknown. Five thoracic chaetigerous segments. Collar trilobed, with two deep lateral incisions; tonguelets absent. Thoracic membranes unknown. Collar chaetae fin-and-blade, with well-separated distal limbate zone and proximal wing, and limbate. Apomatus chaetae present from the third chaetiger. Thoracic uncini saw-torasp-shaped with approximately 15 teeth in profile, up to 4 teeth in a row above peg (dental formula P:4:3:3:1:2:1:1:1: 1:1:1:1:1:1:1; peg bifurcate under compound microscope but blunt, almost trapezoidal in SEM). Triangular depression absent. Abdominal chaetae with flat triangular blades with blunt teeth. Abdominal uncini rasp-shaped, with seven teeth in profile, up to eight fine teeth in row above blunt apparently bifurcate (gouged?) anterior fang. Posterior capillary chaetae absent. Posterior glandular pad not observed. Remarks: This monotypic genus is known so far only from 14 specimens (type series) collected from vermetid reefs near Elat, Red Sea.

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Turbocavus Prentiss et al., 2014 (Fig. 7.4.7.19 A, B) Type species: Turbocavus secretus Prentiss et al., 2014 (monotypic) Diagnosis: Tubes concentrically coiled, occurring in tight aggregations affixed to undersides of rocks. Tube diameter up to 2 mm, individual coil diameter up to 25 mm. Tabulae not observed. Tubes white opaque and circular in cross-section, external surface smooth to fine granular or with transverse growth striations. Internally some tubes with a pattern of three tube wall perforations between adjacent whorls. Thorax with 7−19 chaetigers; abdominal achaetigerous zone as long as thorax; abdomen up to 335 chaetigers. Radiolar crown with up to 19 pairs of radioles arranged pectinately; operculum or pseudoperculum absent. Stylodes, interradiolar membrane, mouth palps absent. Radiolar eyes present. Collar trilobed, one median ventral and two dorsal lobes continuous with thoracic membranes forming apron across abdominal achaetigerous zone. Thoracic chaetae limbate. Apomatus chaetae absent. Collar chaetae plicate at base and grooved tapering to a capillary tip. Thoracic uncini rasp-shaped with approximately 40 teeth in profile, and (1)2 rows of teeth apically to five to six rows above and continuing onto elongated (rounded to) rectangular peg (dental formula P:5:5:4:4 … … 2:2:2:1). Abdominal uncini rasp-shaped with round/rectangular peg and up to 30 transverse rows of seven teeth, decreasing to four teeth per row distally (dental formula P:6:6:6:5 … … 4:4:3:2). Anterior abdominal chaetae flat narrow geniculate. Posterior chaetae long capillaries. Ventral glandular pad triangular. Remarks: The taxon found in shallow waters of the Caribbean Sea has 7 to 19 thoracic chaetigers and bears a unique type of thoracic chaeta, which is plicate or multifolded at its base and continues with a grooved shaft tapering to the capillary tip. Furthermore, Turbocavus lacks an operculum, special collar chaetae or Apomatus chaetae. Vermiliopsis Saint-Joseph, 1894 Type species: Vermilia multivaricosa Mörch, 1863, new name for Vermilia infundibulum sensu Philippi, 1844 (16 accepted species, 3 taxa inquirenda, and 1 nomen dubium) Diagnosis: Tube white, opaque, circular to subquadrangular in cross section; generally with three to seven longitudinal keels and peristomes. Granular overlay absent. Operculum an inverse conical ampulla, with flat to conical chitinous endplate, sometimes a partitioned cap. Peduncle wrinkled, cylindrical, separated from opercular ampulla by a constriction; without distal wings, but a proximal wing may be present. Peduncle ontogenetically formed from the second dorsal radiole on one side, but in adults at base of branchial crown covering three to

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 7.4 Sedentaria: Sabellida/Spionida

six normal radioles. Pseudoperculum generally absent (but present as the underdeveloped second radiole in V. striaticeps). Radioles arranged in (semi)circles, up to 20 per lobe. Interradiolar membrane absent. Radiolar eyes (single pigmented ocelli) along dorsal side of rhachis. Stylodes absent. Mouth palps may be present. Seven thoracic chaetigerous segments. Collar trilobed, tonguelets absent. Thoracic membranes short, continuing to the third to fifth thoracic chaetigers. Collar chaetae limbate. Apomatus chaetae present. Thoracic uncini saw-shaped with up to 10 to 15 teeth above blunt indented peg. Triangular depression present. Abdominal chaetae flat narrow geniculate, with a more or less crenulated edge (rounded teeth) to the blade. Abdominal uncini rasp-shaped, anterior peg blunt. Achaetous anterior abdominal zone absent. Long

posterior capillary chaetae present. Posterior glandular pad present. Remarks: Many species included in Vermiliopsis by various authors and catalogued by Hartman (1959: 608–609) have been later referred to the genera Metavermilia, Bathyvermilia, Pseudovermilia, Semivermilia, and Neovermilia by Zibrowius (1971, 1973a), ten Hove (1975), and most recently Kupriyanova and Nishi (2010). The traditional “Vermiliopsis infundibulum Philippi” from the Mediterranean contains two species “Vermiliopsis infundibulum Philippi s. str.” and Vermiliopsis striaticeps Grube, 1862 (Zibrowius 1973b: 44–45, ten Hove 1975: 57–58; Bianchi 1981: 74–75). Both the genus Vermiliopsis and the species infundibulum are ill-defined, and the designation of a neotype is unavoidable. The binomen V. infundibulum

Fig. 7.4.7.19: Turbocavus secretus: A, animal with 16 thoracic chaetigers removed from its tube; B, radiolar crown. Zibrovermilia zibrowii: C, tetragonal tubes with denticulate edges; D, thorax; E, radiolar crown with operculum. A, B, from Prentiss et al. (2014); C–E, from Kupriyanova and Ippolitov (2015).



generally has been used for Mediterranean–Lusitanian forms, and only rarely for Indo-Pacific forms normally identified as Vermiliopsis glandigera Gravier, 1906, or Vermiliopsis pygidialis Willey, 1905. A neotype from the Mediterranean needs to be designated in the context of a muchneeded revision of the problematic genus. Vitreotubus Zibrowius, 1979a Type species: Vitreotubus digeronimoi Zibrowius, 1979a (monotypic) Diagnosis: Tube entirely vitreous, more or less quadrangular in cross section by its two ample undulating lateral keels, and with a longitudinal row of teeth (Fig. 7.4.7.2 M). Granular overlay absent. Operculum inverse conical with chitinous diabolo-like endplate. Peduncle smooth, cylindrical, merging gradually into operculum, without wings, inserted as the first radiole (at base of left radiolar lobe, in line with the first radiole). Pseudoperculum absent. Arrangement of radioles short pectinate, up to 11 per lobe. Interradiolar membrane and stylodes absent. Radiolar eyes not observed. Mouth palps present. Seven thoracic chaetigerous segments. Collar trilobed. Median lobe of collar with scalloped edge and lateral projections, separated from lateral lobes by deep incision (tonguelets absent), latter continuous with thoracic membranes extending all along the thorax, but narrow in the posterior segments, forming ventral apron. Collar chaetae Spirobranchus-type and simple limbate. Apomatus chaetae absent. Thoracic uncini saw-shaped with six to seven teeth above pointed fang. Triangular depression present. Abdominal chaetae true trumpet-shaped, with two rows of pointed teeth bordering hollow groove and extended into a long lateral spine. Abdominal uncini saw-shaped with approximately 6 teeth anteriorly, rasp-shaped with approximately 10 teeth in profile, and 3 to 4 teeth in a row posteriorly. Posterior capillary chaetae absent, but geniculate chaetae long at the end of abdomen. Posterior glandular pad absent. Remarks: The monotypic genus was originally described from fossil records and Recent material from the bathyal zone of the Azores and the Indian Ocean (Zibrowius 1979a); more recent records are given by ten Hove (1994). It has a very characteristically shaped transparent tube. Zibrovermilia Kupriyanova and Ippolitov, 2015 (Fig. 7.4.7.16 A–C) Type species: Zibrovermilia zibrowii Kupriyanova and Ippolitov, 2015 (monotypic) Diagnosis: Tube white opaque, quadrangular in cross section; with four denticulate keels, distal parts circular in cross section, without ringlike peristomes. Operculum an

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inverse conical ampulla, with chitinous endplate; borne on the second normal pinnulated radiole. Pseudoperculum absent. Radioles arranged pectinately, interradiolar membrane absent. Radiolar eyes not observed. Stylodes absent. Mouth palps not observed. Seven thoracic chaetigerous chaetigers, including six uncinigerous. Collar trilobed, tonguelets between ventral and lateral collar parts absent. Thoracic membranes short, ending at the second to third thoracic chaetigers. Collar chaetae limbate, of two sizes. Apomatus chaetae present. Thoracic uncini rasp-shaped with up to 15 teeth in profile and four to five teeth in frontal view above blunt peg. Triangular depression absent. Abdominal chaetae flat narrow geniculate, blade with a more or less crenulated edge (rounded teeth). Abdominal uncini rasp-shaped, anterior peg blunt. Long posterior capillary chaetae present. Posterior glandular pad absent. Remarks: The assignment of Zibrovermilia zibrowii to a new monospecific genus by Kupriyanova and Ippolitov (2015) is a result of a unique combination of characters. Although the tube of Z. zibrowii is quadrangular in cross-section and the peduncle is pinnulated like that in Spirodiscus and Bathyditrupa, the similarities end here. The operculum-bearing radiole in Z. zibrowii is similar to other radioles, not modified into a thick peduncle as in Spirodiscus and Bathyditrupa, and the tubes are large and thick-walled, with denticles on the edges. The new species is similar to Bathyvermilia gregrousei Kupriyanova and Ippolitov (2015) in having seven thoracic segments, thoracic Apomatus chaetae, and very typical Bathyvermilia or Vermiliopsis-type abdominal chaetae. However, thoracic uncini of this genus are raspshaped, not saw-shaped as in Vermiliopsis and Bathyvermilia, and pinnulated peduncles are not found either in these genera. When molecular data on phylogenetic position of the species become available, the taxonomic position of Zibrovermilia may have to be reconsidered. Spirorbinae Chamberlin, 1919 Tube spirally coiled dextrally or sinistrally; body asymmetrical, abdomen turned over thorax 90° in achaetigerous zone between thorax and abdomen; thorax adjoins to substratum dorsally; three to five (seven?) thoracic chaetigers; collar chaetae simple or with special fin-and blade chaetae; thoracic sickle (Apomatus) chaetae usually present in three to five thoracic chaetigers; abdominal chaetae flat geniculate; embryos incubated in tube or in opercular brood chamber; larvae lecithotrophic, pelagic stage brief or absent. Tribe Circeini Knight-Jones, 1978 Diagnosis: The embryos stick to one another and then directly to the inner side of the tube; accordingly, the

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only type of operculum throughout life time is an endplate, usually with a talon. Other important features are as follows: (1) thoracic uncini wide rasp-shaped, with 3 to 15 longitudinal rows of teeth and blunt anterior peg; (2) abdominal uncini distributed quite asymmetrically, on convex side body side they may be present on last chaetigers only or absent altogether; (3) abdominal chaetae flat geniculate, pennant shaped (blade width decreases gradually toward the tip), usually with a thick projecting heel; the length of their blade is no longer than blade length of largest collar chaetae; (4) abdominal companion capillary hooked chaetae may be present only on the last abdominal chaetigers; and (5) larvae without white attachment glands. Circeis Saint-Joseph, 1894 Type species: Circeis armoricana Sаint-Jоsерh, 1894 (six species) Diagnosis: Tubes usually dextral (anticlockwise), but in some species may be regularly or occasionally sinistral (clockwise); margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae bent (usually strongly), modified with vestigial lateral cross-striation or cross-striated from “frontal side” of blade, not visible laterally under a dissecting microscope; sickle-chaetae absent; three thoracic chaetigers. Remarks: The genus includes species distributed in the Northern Hemisphere only. Most of them are arcto-boreal, whereas others are boreal Atlantic or Pacific. General depth range is from the intertidal zone to 550 m, although most of them prefer intertidal and upper subtidal zones and only one reaches a bathyal depth (Knight-Jones et al. 1991, Rzhavsky 1992a, b, 1992 (1994), 1998, Rzhavsky et al. 2014, Ippolitov and Rzhavsky 2015b). Paradexiospira Caullery and Mesnil, 1897 Type species: Spirorbis violaceus Levinsen, 1884 [three (four?) species] Diagnosis: Tubes dextral, one species occasionally may be coiled sinistrally. Margins of collar and thoracic membrane not fused over thoracic groove. Large collar chaetae bent, cross-striated or fin-and-blade cross-striated. Only sickle (Apomatus-type) chaetae present on the third thoracic chaetigers. Four thoracic chaetigers in adults (juveniles rarely with only three chaetigers). Remarks: The genus includes three (four?) species distributed in the North Hemisphere only, from the intertidal zone to 242 m (Ippolitov and Rzhavsky 2015b). All species are arcto-boreal, excluding a potential undescribed species recorded only from Oregon (Knight-Jones et al. 1979).

Tribe Januini Knight-Jones, 1978 Diagnosis: Embryos brooded in inverted opercular brood chamber formed outside the opercular ampulla; each brood chamber used only for one brood and molting needed for embryo release; the first brood chamber developing under primary endplate bearing talon; every next brood chamber developing under previous one, so that bottom of the first brood chamber becoming secondary distal plate typically lacking talon. Other important features are as follows: (1) thoracic uncini narrow, rasp-shaped with four to eight longitudinal rows of teeth throughout most length of uncinus and a pointed (rarely trifurcate) anterior peg; (2) abdominal uncini distributed symmetrically on both sides of the body; (3) abdominal chaetae flat geniculate, wide bladed, and coarsely serrated, projecting heel usually absent or vestigial, sometimes noticeable; blade length longer than or equal to that of collar chaetae; (4) abdominal companion capillary hooked chaetae absent; and (5) larvae with a pair white attachment glands on thorax. Janua Saint-Joseph, 1894 Type species: Spirorbis pagenstecheri Quatrefages, 1866, accepted as Janua heterostropha (Montagu, 1803) (monotypic) Diagnosis: Tubes typically dextral, sinistral forms rare. Talon of distal plate of primary operculum small and peripheral; lateral brood chamber walls uncalcified and transparent; the first brood chamber with talon on lateral wall facing away from radiolar crown, subsequent chambers lacking talons. Brood chambers cup-shaped. Collar and thoracic membrane margins not fused over thoracic groove. Large collar chaetae bent, limbate, with finely serrated blades; sickle-chaetae present. Always three thoracic chaetigers. Remarks: Monotypic genus with Janua heterostropha (Montagu, 1803) as only species, of which the type species of Janua, J. pagenstecheri (Quatrefages 1866), is a junior synonym. Widely distributed in both Hemispheres and all oceans from the Atlantic sector of the Arctic Ocean to southern shores of Australia, Africa, and South America. Usually known from the intertidal zone to 30 m depth (rarely up to 200 m). Leodora Saint-Joseph, 1894 Type species: Spirorbis laevis Quatrefages, 1865 (two species) Diagnosis: Tubes coiling sinistral; endplate of primary operculum flat with peripheral pin-shaped talon; brooding specimen have simultaneously two to three cup-shaped



or cylindrical brood chambers. Each has calcareous endplate bearing pin-shaped talon; lateral brood chamber walls uncalcified and transparent; collar and thoracic membrane margins not fused over thoracic groove. Large collar chaetae bent, limbate, with finely serrated blades; sickle-chaetae absent; three thoracic chaetigers. Remarks: Currently, the genus includes only two species. The type species is a nomen dubium. Generic diagnosis is based on the only other species, Leodora knightjonesi de Silva, 1965, described from the Mediterranean Sea. This species is known from the tropical waters of Sri Lanka (Indian Ocean), Australia and Hawaii (Pacific Ocean), and West Indian (Atlantic Ocean) from the intertidal zone to a depth of 1 to 2 m (de Silva 1965, Bailey 1970, Vine et al. 1972). Neodexiospira Pillai, 1970 Type species: Spirorbis pseudocorrugatus Bush, 1905 (nom nov. pro Spirorbis corrugatus Caullery and Mesnil, 1897, non Montagu, 1803) [10 (11?) species] Diagnosis: Tubes typically dextral, sinistral forms rare; talon of distal plate of primary operculum of different sizes and peripheral; lateral brood chamber walls calcified and semitransparent distally but transparent proximally; the first brood chamber with talon on lateral wall facing away from radiolar crown, subsequent chambers lacking talons; brood chambers cylindrical and somewhat curved; collar and thoracic membrane margins fused over thoracic groove; large collar chaetae bent, limbate, usually with finely serrated blades; in some species, blades more coarsely serrated and cross-striated; sickle-­ chaetae absent; three thoracic chaetigers. Remarks: The genus includes 10 (11?) species (two nominal species probably are synonyms). Known in all oceans, excluding the Arctic, and distributed from boreal to subantarctic waters. All species live from the intertidal zone to 20 to 30 m depth, although sometimes they may reach 150 m. Pillaiospira Knight-Jones, 1973 Type species: Janua (Pillaiospira) trifurcata Knight-Jones, 1973 (two species) Diagnosis: Tubes coiling dextral (anticlockwise); talon of distal plate of primary operculum peripheral; lateral brood chamber walls calcified and semitransparent distally and transparent proximally; the first brood chamber with talon on lateral wall facing away from radiolar crown, subsequent chambers lacking talons. Brood chambers cylindrical or short-cylindrical; collar and thoracic membrane margins not fused over thoracic groove or partially fused in juveniles; large collar chaetae bent, limbate, with finely serrated blades; sickle-chaetae absent; three thoracic chaetigers.

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Remarks: The genus includes two species known from the upper subtidal zone of southeastern Australia and South Africa (Knight-Jones 1973, Knight-Jones and KnightJones 1974). Tribe Paralaeospirini Knight-Jones, 1978 Diagnosis: The egg string is incubated in the parent’s tube, being attached neither to the tube wall nor to the body of a parent; accordingly, the only type of operculum throughout lifetime is an endplate, usually with a talon. Other characteristic features are as follows: (1) narrow saw-torasp-shaped thoracic uncini, each starting with one row of large teeth posteriorly and ending with three rows of large teeth in front of blunt anterior peg; (2) abdominal uncini distributed asymmetrically: they are absent from the convex side of body, or present only on last chaetigers; (3) abdominal chaetae flat geniculate, pennant shaped (blade width decreases gradually toward tip), usually with a thick projecting heel; the length of their blade is no longer than blade length of largest collar chaetae; (4) abdominal companion capillary hooked chaetae may be present only on last abdominal chaetigers; and (5) larvae without white attachment glands. Paralaeospira Caullery and Mesnil, 1897 Type species: Spirorbis (Paralaeospira) aggregata Caullery and Mesnil, 1897 (10 species) Diagnosis: Sinistral tubes; margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae bent, with basal fins and distal serrated blades without cross-striation; simple limbate and sickle-chaetae in the third thoracic fascicles; four thoracic chaetigers. Remarks: The genus includes 10 species distributed mainly in the south temperate belt and Antarctic (Knight-Jones and Knight-Jones 1984), although Paralaeospira malardi Caullery and Mesnil, 1897 is known only from boreal waters of the northeastern Atlantic (Knight-Jones and KnightJones 1977, Knight-Jones et al. 1991). Depth range is from the intertidal zone to 110 m (Ippolitov and Rzhavsky 2014). Tribe Pileolarini Knight-Jones, 1978 Diagnosis: Embryos brooded within chamber (or cup) formed by invagination of opercular ampulla and used for more than one brood. With two types of opercula, one only an endplate with a talon and another brooding chamber of various structures (from open cup to completely closed chamber sometimes fused with primary opercular endplate when closed). Other important features are as follows: (1) thoracic uncini (saw-to-rasp-shaped) starting with one row of teeth posteriorly to three rows before

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blunt anterior peg; (2) abdominal uncini distributed symmetrically; (3) abdominal chaetae flat geniculate, pennant shaped, usually with a thick (optically dense) projecting heel; its blade length usually somewhat shorter than that of largest collar chaetae, its width decreases gradually toward tip; (4) abdominal companion capillary hooked chaetae usually present on most chaetigers; and (5) larvae with single abdominal white attachment gland. Amplicaria Knight-Jones, 1984 Type species: Amplicaria spiculosa Knight-Jones, 1973 (monotypic) Diagnosis: Tubes sinistral (clockwise); talon of endplate small and peripheral; distal plate retained and developing walls to protect the brood, cup below remaining open, shallow and calcified only proximally, providing no distal calcification; opercular peduncle inserted between the first and the second radioles on the left side; margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae fin-and-blade, coarsely serrated, without cross-striation; sickle-chaetae present in the third and fourth thoracic fascicles; five thoracic chaetigers. Remarks: The species is known from Australia, New Zealand, and Tonga (Knight-Jones 1984), from the intertidal zone to 10 m. Bushiella Knight-Jones, 1973 Type species: Spirorbis evolutus Bush, 1905 [13 (14?) species] Diagnosis: Tubes sinistral (clockwise); talon of opercular endplate peripheral or almost peripheral and flattened, generally large; endplate retained and fused to brood chamber by talon and primary opercular plate (completely or partial) or only by talon; brood chamber a deeply invaginated sac totally enclosing embryos except for a pore capable of opening and closing; lining of brood chamber forming a calcified dome distally, but not calcified proximally or on the side bearing a pore; opercular peduncle inserted between the first and the second radioles on the left side, so that the noncalcified part of chamber positioned near the center of radiolar crown; margins of collar and thoracic membranes not fused over thoracic groove; posterior edges of thoracic membranes reaching end of the third chaetiger; large collar chaetae limbate or modified fin-and-blade with finely or moderately serrated blades usually lacking cross-striation; sickle-­ chaetae present in the third thoracic fascicles; three thoracic chaetigers. Remarks: The genus includes 13 (14?) species, the status of the one species is unclear, from the Northern Hemisphere. Arctic, arcto-boreal, or boreal Atlantic or Pacific

species, known from the intertidal zone up to a depth of 636 m, although they prefer intertidal and sublittoral zones (Knight-Jones and Knight-Jones 1977, Knight-Jones et al. 1979, Rzhavsky 1993, 1992 (1994), Knight-Jones et al. 1991). One of the Arctic species, Bushiella (Jugaria) kofiadii Rzhavsky, 1988, is known from depths of 58 to 550 m, usually more than 250 m (Rzhavsky et al. 2014). The bathymetric range of the Atlantic Bushiella (Jugaria) atlantica Knight-Jones, 1978, is unknown, but it may exceed 1500 m. Nidificaria Knight-Jones, 1984 Type species: Spirorbis clavus Harris, 1969 (eight species) Diagnosis: Tubes sinistral (anticlockwise); talon of endplate pin-shaped eccentric, but not peripheral; endplate of primary operculum not fused with brood chamber and usually shed after chamber development; brood chamber as an open nest or semiclosed chamber with large lateral hole, slightly calcified proximally and sometimes extend distally; opercular peduncle inserted between the first and the second radioles on the left side; large collar chaetae bent, modified fin-and-blade and cross-striated, with coarse blade margin serration; sickle-chaetae present in the third thoracic fascicles; three thoracic chaetigers. Remarks: This poorly studied genus includes about eight species (some names probably are synonyms). Most species found in shallow subtropical and subantarctic (antarctic?) waters, whereas the type species has been described from the Mediterranean Sea (Harris 1969). Nidificaria levensteinae (Bailey-Brock and Knight-Jones, 1977) was collected from abyssal depths (4370–6096 m) in the North Pacific (Bailey-Brock and Knight-Jones 1977). Pileolaria Claparède, 1868 Type species: Pileolaria militaris Claparède, 1868 (21 species) Diagnosis: Tubes sinistral (clockwise); talon of endplate usually small (excluding quite special talon of P. militaris) slightly eccentric, but not peripheral; distal plate of primary operculum not fused with brood chamber and usually shed after chamber development; brood chamber a deeply invaginated sac totally enclosing embryos except for a pore capable of opening and closing; lining of brood chamber forming a calcified dome distally, but not calcified proximally or on pore bearing side; opercular peduncle inserted between the first and the second radioles on the left side, so that the noncalcified part of chamber positioned near the center of radiolar crown; margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae bent, modified fin-and-blade and usually cross-striated, with coarse blade margin serration; sickle-chaetae present in the third thoracic fascicles; three thoracic chaetigers.



Remarks: The genus includes at least 21 species (probably the widely distributed nominal taxon Pileolaria berkeleyana Rioja, 1942 is a complex of cryptic species). Generally, the species are distributed in all oceans of both Hemispheres, from the Atlantic zone of the Arctic to the Antarctic coast (Knight-Jones et al. 1979, Knight-Jones and Knight-Jones 1984, Rzhavsky 2010), although species of the genus mainly prefer subtropical and tropical waters (Knight-Jones and Knight-Jones 1984). Some species live intertidally and in the subtidal zone, whereas others reach 258 m. Protoleodora Pillai, 1970 Type species: Spirorbis asperatus Bush, 1905 (four species) Diagnosis: Tubes sinistral (clockwise); talon of primary opercular endplate subcentral or almost peripheral, flattened, large; primary operculum attached to distal part of developed brood chamber only by talon’s tip, so often shed; trace of primary operculum attachment usually present; brood chamber a deeply invaginated sac totally enclosing embryos, except for a pore capable of opening and closing; calcified distally, but not proximally or on side bearing a pore; forming a soft-walled pouch extending posteriorly in dorsal groove of thorax and capable of accommodating very large broods (up to 150 embryos per brood), but usually not visible when nonbrooding; opercular peduncle arises outside circle of radioles; margins of collar and thoracic membranes not fused over thoracic groove; margins of thoracic membranes from convex side of body extending posteriorly and reaching at least the first abdominal chaetiger or further; limbate collar chaetae bent, with finely or moderately serrated blades; sickle-chaetae present in the third thoracic fascicles; three thoracic chaetigers. Remarks: The four species are known from the intertidal zone up to 320 m deep in boreal waters of the Pacific Ocean (mainly off the Asian coast). Two of the species were recorded from the Pacific sector of the Arctic Ocean (Rzhavsky 1992b, 1992 (1994), Knight-Jones et al. 1991). Simplaria Knight-Jones, 1984 Type species: Spirorbis pseudomilitaris Thiriot-Quiévreux, 1965 (three species) Diagnosis: Tubes sinistral (clockwise); talon of endplate small slightly eccentric, but not peripheral; endplate of primary operculum not fused with brood chamber and shed after chamber development; brood chamber a deeply invaginated sac totally enclosing embryos except for a pore capable of opening and closing; lining of brood chamber forming a calcified dome distally, but not calcified proximally or on pore bearing side; opercular

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peduncle inserted between the first and the second radioles on the left side, so that the noncalcified part of chamber positioned near the center of radiolar crown; margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae bent, modified finand-blade and usually cross-striated, with coarse blade margin serration; sickle-chaetae absent; three thoracic chaetigers. Remarks: The species are distributed in both Hemispheres in the Pacific, Atlantic, and Indian Oceans, intertidally and in shallow waters, mainly in subtropical and tropical areas (Vine 1977, Knight-Jones 1978, 1984, KnightJones et al. 1979). Vinearia Knight-Jones, 1984 Type species: Spirorbis koehleri Caullery and Mesnil, 1897 (three species) Diagnosis: Tubes sinistral (clockwise); talon of endplate small and peripheral, sometimes multiplate; endplate retained and developing walls to protect the brood, cup below remaining open, shallow and calcified only proximally, providing no distal calcification; opercular peduncle inserted between the first and the second radioles on the left side; margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae finand-blade, coarsely serrated, without cross-striation; sickle-chaetae present in the third and fourth thoracic fascicles; five thoracic chaetigers. Remarks: The genus includes three species known from shallow waters off the subtropical and tropical zones (Knight-Jones 1984). Tribe Romanchellini Knight-Jones, 1978 Diagnosis: Embryos incubated inside the parent’s tube in a sac, being attached to the thorax or to the abdomen by an epithelial stalk, sometimes poorly developed; accordingly, the only type of operculum throughout life time is an endplate with a talon, rarely without talon. Other important features: (1) thoracic uncini have different morphologies (usually they are rasp-shaped with three to seven longitudinal rows of teeth thought most length of uncinus, rarely two to three rows or saw-to-rasp-shaped, one species with 12 to 15 rows of teeth; anterior peg flat and often gouged, looking bifurcate under a light microscope, sometimes anterior flat peg fluted, looking serrated or wavy (Vine, 1972, fig. 1F; Knight-Jones and Fordy 1979, fig. 84); (2) abdominal uncini distributed asymmetrically, absent from the convex side of body, or present only on last chaetigers; (3) abdominal chaetae flat geniculate, brush-type with very short sharply narrowing blades and approximately 10 denticles; (4) abdominal capillary

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hooked chaetae may be present on the last chaetigers; (5) larvae usually without white abdominal attachment gland (the gland was described only for Protolaeospira striata (Quievreux, 1963) while larvae unknown for many Romanchellini).

Remarks: The species has been recorded off subantarctic islands and archipelagos of the South Atlantic and Indian Oceans, New Zealand, south coast of Australia, and some sites off the Antarctic coast. Known depth range is from the intertidal zone to 158 m, usually up to 50 m.

Eulaeospira Pillai, 1970 Type species: Spirorbis (Laeospira) orientalis Pillai, 1960 (two species) Diagnosis: Tubes sinistral (clockwise); margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae bent, without cross-striation, modified fin-and-blade as well as limbate in the same fascicle; fin-and-blade chaetae more common on the convex side of body; sickle-chaetae absent; three thoracic chaetigers. Remarks: The genus includes two species [three if one counts Eulaeospira sp. tentatively described based on only one specimen from the Adelie Land (Rzhavsky 1997)]. Distributed in tropical and subtropical regions of both Hemispheres of the Indo-Pacific and probably in the subantarctic area (Eulaeospira sp.). Known from subtidal zone up to 20 to 25 m, excluding the questionable Eulaeospira sp., which was recorded at the depth 135 m.

Protolaeospira Pixell, 1912 Type species: Spirorbis (Protolaeospira) ambilateralis Pixell, 1912 (12 species) Diagnosis: Tubes usually sinistral (clockwise), in some species regularly dextral (anticlockwise); margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae bent, modified fin-and-blade (at least from the convex side of body), cross-striated or not; sickle-chaetae present in the third fascicles; four thoracic chaetigers. Remarks: Although distribution ranges of many Protolaeospira species are unclear, in general, representatives of the genus are distributed in all oceans of the Southern Hemisphere from the Antarctic coast to the subtropical zone (Knight-Jones and Knight-Jones 1984, 1991, 1994). Some species also were recorded from both coasts of the North Pacific Ocean from subtropical/tropical and boreal waters (Knight-Jones et al. 1979) and one species from boreal–tropical waters of the north-eastern and west-southern Atlantic (Knight-Jones and Knight-Jones 1994). Depth ranges from the intertidal zone to bathyal depths.

Helicosiphon Gravier, 1907 Type species: Helicosiphon biscoeensis Gravier, 1907 (two species) Diagnosis: Tubes sinistral (clockwise); margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae limbate without cross-striation; sickle-­chaetae absent; four thoracic chaetigers. Remarks: Pillai (2009) established the genus Knightjonesia for the species Helicosiphon platyspira Knight-Jones, 1978. In his opinion, the species differs by having a somewhat winged opercular peduncle. We see no reasons for establishing a new genus on the basis of this doubtful feature and are of the opinion that this species should remain within the genus Helicosiphon. Both species recorded off subantarctic islands and archipelagos of the South Atlantic and South Indian Oceans and some localities off the Antarctic coast. The depth ranges from the intertidal zone up to 355 m. Metalaeospira Pillai, 1970 Type species: Spirorbis pixelli Harris, 1969 (nom. nov. pro Spirorbis antarcticus Pixell, 1913) (four species) Diagnosis: Tubes sinistral (clockwise); margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae limbate without cross-striation; sickle (Apomatus) chaetae present in the third fascicle; four thoracic chaetigers.

Romanchella Caullery and Mesnil, 1897 Type species: Spirorbis (Romanchella) perrieri Caullery and Mesnil, 1897 (eight species) Diagnosis: Tubes usually sinistral (clockwise) or rarely dextral (anticlockwise); margins of collar and thoracic membranes fused over the thoracic groove; large collar chaetae bent, not modified; sickle-chaetae present in the third fascicle; three thoracic chaetigers. Remarks: The genus includes eight species distributed in all oceans of the Southern Hemisphere usually in subtropical/tropical waters, some species reach the Antarctic coast. Depth range is from the intertidal zone to 200 m. Tribe Spirorbini Chamberlin, 1919 Diagnosis: The egg string is incubated inside the parent’s tube, being attached posteriorly by a thread to inner tube wall; accordingly, the only type of operculum throughout life time is an endplate with a talon. Other important features are as follows: (1) thoracic uncini rasp-shaped, with three to four (five to six in smallest uncini) longitudinal rows of teeth and usually blunt anterior peg; (2) abdominal uncini distributed fairly symmetrically on both sides of the body; (3) abdominal chaetae flat geniculate,



pennant shaped (blade width decreases gradually toward tip), usually with a thick projecting heel; the length of their blade is no longer than blade length of largest collar chaetae; (4) abdominal capillary hooked chaetae usually appearing on last abdominal chaetigers; and (5) larvae have a single white abdominal attachment gland. Spirorbis Daudin, 1800 Type species: Spirorbis borealis Daudin, 1800 (= Serpula spirorbis Linnaeus, 1758) (14 species) Diagnosis: Tube usually sinistral (clockwise), but may be dextral (anticlockwise), and several species have both dextral and sinistral tubes; margins of collar and thoracic membranes not fused over thoracic groove (excluding species of monotypic subgenus Velorbis); large collar chaetae bent, modified fin-and-blade or fin-and-blade cross-striated; simple limbate and sickle-chaetae in the third thoracic fascicles; three thoracic chaetigers. Remarks: The genus includes 14 species. Most species of Spirorbini can be divided into two distinct biogeographic groups. Representatives of the first group are known from boreal and subtropical waters of the Atlantic (mainly off European coasts) and may also reach the Atlantic sector of the Arctic (Knight-Jones et al. 1991). Members of the second group are distributed over the Pacific coast of North America from boreal/subtropical to tropical zone (Knight-Jones et al. 1979). Two species belonging to the latter group are also recorded off islands and archipelagos located in tropical and subtropical waters of both Hemispheres in the Pacific and Atlantic (Knight-Jones et al. 1979). Three species of Spirorbis are restricted to their type localities in subtropical or tropical waters and cannot be placed with certainty into any of the above biogeographic groups (Ippolitov and Rzhavsky 2015a). General depth range is from the intertidal zone to 100 m, some species live only intertidally (Ippolitov and Rzhavsky 2015a). Insertae sedis Method of incubation is unknown. Anomalorbis Vine, 1972 Type species: Anomalorbis manuatus Vine, 1972 (monotypic) Diagnosis: Tube dextral (anticlockwise); margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae bent, limbate, finely serrated, without cross-striation; sickle-chaetae absent; five thoracic chaetigers. Remarks: This monotypic genus was described based on one specimen. Judging from the opercular structure and the asymmetrical distribution of the abdominal uncini, this is not an opercular-brooding species. There are

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three tribes with asymmetry in distribution of abdominal uncini—Circeini, Romanchellini, and Paralaeospirini, but some details of A. manuatus morphology (five thoracic chaetigers and structure of abdominal chaetae, with strongly bent distal part of axis and teeth beginning at a distance from the axis; see Knight-Jones and Fordy 1979, Fig. 68, B) are unusual and do not allow placing this species in any tribe. Crozetospira Rzhavsky, 1997 Type species: Crozetospira dufresnei Rzhavsky, 1997 (monotypic) Diagnosis: Tubes sinistral (clockwise); margins of collar and thoracic membranes not fused over thoracic groove; large collar chaetae fin-and-blade, coarsely serrated, with cross-striation; sickle-chaetae present in the third fascicle; three thoracic chaetigers. Remarks: Judging from the opercular structure and the asymmetrical distribution of the abdominal uncini, this is not an opercular-brooding species. There are three tribes with asymmetry in distribution of abdominal uncini— Circeini, Romanchellini, and Paralaeospirini, but none have genera combining all the features found in this monotypic genus (Knight-Jones and Fordy 1979; Rzhavsky 1991). As Circeini are known only from the Northern Hemisphere (Knight-Jones et al. 1991) and Romanchellini have characteristic brushlike abdominal chaetae, the genus was provisionally placed in the Paralaeospirini. However, it could be the only monotypic genus of Paralaeospirini with cross-striated collar chaetae. The species is known from the Crozet Islands in southern Indian Ocean only at depths 105 to 566 m (Rzhavsky 1997). Neomicrorbis Rovereto, 1904 Type species: Serpula crenatostriata Münster in Goldfuss, 1831 (fide Regenhardt 1961: 89) (monotypic) Diagnosis: Tube transparent (vitreous), circular in cross section, with numerous longitudinal keels consisting of small denticles. Tube spiral, either dextral or sinistral. Granular overlay absent. Operculum with distal calcareous plate and large talon projecting into proximal ampulla, merging into peduncle without constriction. Peduncle second radiole on the right side, two small distal wings. Pseudoperculum absent. Arrangement of radioles semicircular, 10 radioles left, 7 right. Interradiolar membrane, radiolar eyes, and stylodes absent. Mouth palps absent. Number of thoracic chaetigers asymmetric, five to the left and six to the right. Collar nonlobed, tonguelets and length of thoracic membranes not known. Collar chaetae fin-and-blade and limbate. Apomatus chaetae present in

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 7.4 Sedentaria: Sabellida/Spionida

posterior thoracic segments. Thoracic uncini saw-shaped with 12 to 15 teeth and rounded peg. Thoracic depression not known. Abdominal chaetae retrogeniculate. Abdominal uncini rasp-shaped with 14 to 17 teeth in profile, 3 to 5 in a row. Long anterior achaetous abdominal zone. ­Posterior capillary chaetae present. Posterior glandular pad absent. Remarks: Neomicrorbis belongs to Spirorbinae (likely Paralaeospirini) because of its incomplete chaetal inversion, typical for spirorbins. Zibrowius (1972a) regards it as something intermediate between a “serpulid” and a spirorbin.

Acknowledgments This work was supported by an Australian Biological Resource Study (ABRS) grant to EKK. We thank A.  Ippolitov, E. Nishi, O. Paderanga, N. Prentiss, A.  Semenov, K.  Vasileiadou. F Verbiest, E. Wong, and especially G. Rouse for providing serpulid photos, as well as T. Ternova for help with Fig. 7.4.7.11.

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tant distinctifs que naturels des ordres, familles et genres, avec la description des espèces. Description de l’Égypte, Histoire Naturelle, Paris I (3), l’Imprimerie Royale: 3–128. Saint-Joseph, M., de (1894): Les annélides polychètes des côtes de Dinard. Annales des Sciences Naturelles 17(1): 1–395. Sanfilippo, R. (2009): New species of Hyalopomatus Marenzeller, 1878 (Annelida, Polychaeta, Serpulidae) from Recent Mediterranean deep-water coral mounds and comments on some congeners. Zoosystema 31: 147–161. Schmarda, L.K. (1861): Neue wirbellose Thiere beobachtet und gesammelt auf einer Reise um die Erdr [sic] 1853 bis 1857 von Ludwig K. Schmarda. Erster Band. Turbellarien, Rotatorien und Anneliden. Zweite Hälfte. Wilhelm Engelmann, Leipzig, 164 pp. Schmidt, W. (1950): Neue Serpula-Arten aus dem Naturhistorischen Museum Wien. Annalen des Naturhistorishen Museums in Wien 57: 159–162. Schmidt, W. (1951): Neue Serpulidae aus dem tertiären Wiener Becken. Annalen des Naturhistorishen Museums in Wien 58: 77–84. Schmidt, W. (1955): Die Tertiären Würmer Österreichs. Österreichische Akademie der Wissenschaften. MathematischNaturwissenschaftliche Klasse. Denkschriften 109: 1–121. Senowbari-Daryan, B., Link, M. & Işintek, I. (2007): Filograna minor nov. sp. (worm tube) from the Middle Triassic (Anisian) reef boulders of the Karaburun Peninsula, Western Turkey. Turkish Journal of Earth Sciences 16: 1–9. Silva, P.H.D.H., de (1965): New species and records of Polychaeta from Ceylon. Proceedings of the Zoological Society of London 144(4): 537–563. Simon, C., Niekerk, H. van, Burghardt, I., Hove, H.A. ten, & Kupriyanova, E.K. (2019): Not out of Africa: Spirobranchus kraussii kraussii (Baird, 1865) is not a global fouling and invasive serpulid of Indo-Pacific origin. Aquatic Invasions 14: 221–249. Smith, R.S. (1991): Relationships within the order Sabellida (Polychaeta). In: Petersen, M.E. & Kirkegaard, J.B. (Eds.). Proceedings of the 2nd International Polychaete Conference, Copenhagen 1986. Ophelia Supplement 5: 249–260. Smith, A.M., McGourty, C.R., Kregting, L. & Elliot, A. (2005): Subtidal Galeolaria hystrix (Polychaeta, Serpulidae) reefs in Paterson Inlet, Stewart Island, New Zealand. New Zealand Journal of Marine and Freshwater Research 39: 1297–1304. Smith, A.M., Henderson, Z.E., Kennedy, M., King, T. M. & Hamish Spencer, G. (2012): Reef formation versus solitariness in two New Zealand serpulids does not involve cryptic species. Aquatic Biology 16: 97–103. Smith, A.M., Riedi, M.A. & Winter, D.J. (2013): Temperate reefs in a changing ocean: skeletal carbonate mineralogy of serpulids. Marine Biology 160: 2281–2294. Stimpson, W. (1854): Synopsis of the marine invertebrata of Grand Manan: or the region about the mouth of the Bay of Fundy, New Brunswick. Smithsonian Contributions to Zoology 6: 1–67. Strathmann, R.R., Jahn, T.L. & Fonseca, J.R.C. (1972): Suspension feeding by marine invertebrate larvae: clearance of particles by ciliated bands of a rotifer, pluteus, and trochophore. Biological Bulletin 142: 505–519. Southern, R. (1921): Polychaeta of the Chilka Lake and also of fresh and brackish waters in other parts of India. Memoirs of the Indian Museum 5: 563–659. Stiller, F. (2000): Polychaeta (Annelida) from the Upper Anisian (Middle Triassic) of Qingyan, south-western China. Neues

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Jahrbuch für Geologie und Paläontologie, Abhandlungen 217: 245–266. Styan, C.A., McCluskey, C.F., Sun, Y. & Kupriyanova, E.K. (2017): Cryptic sympatric species across the Australian range of the global estuarine invader Ficopomatus enigmaticus (Serpulidae, Annelida). Aquatic Invasions 12 (1): 53–65. Sun, Y. (2017): Taxonomy, barcoding and phylogeny of Hydroides (Serpulidae, Annelida), the largest genus of notorious fouling and invading calcareous tubeworms. PhD thesis, Macquarie University, Sydney, Australia. Sun, Y., Kupriyanova, E.K. & Qiu, J. W. (2012): CO1 barcoding of Hydroides: a road from impossible to difficult. Invertebrate Systematics 26(6): 539–547. Sun, Y., Wong, E., Hove, H.A. ten, Hutchings, P.A., Williamson, J.E. & Kupriyanova, E.K. (2015): Revision of the genus Hydroides (Annelida: Serpulidae) from Australia. Zootaxa 4009(1): 1–99. Sun, Y., Wong, E., Tovar-Hernandez, M., Williamson, J. & Kupriyanova, E.K. (2016): Is Hydroides brachyacantha (Serpulidae, Annelida) a widely-distributed species? Invertebrate Systematics 30: 41–59. Sun, Y., Wong, E., Keppel, E., Williamson, J., Kupriyanova, E.K. (2017): A global invader or a complex of regionally distributed species? Clarifying the status of an invasive calcareous tubeworm Hydroides dianthus (Verrill, 1873) using barcoding. Marine Biology 164: 28-1–28-12. Sun, Y. Wong, E., Williamson, J E., Hutchings, P A., Ahyong, S.T. & Kupriyanova, E.K. (2018): Barcoding and multi-gene based phylogeny and biogeography of the globally distributed calcareous tubeworm genus Hydroides Gunnerus, 1768 (Annelida, Serpulidae). Molecular Phylogenetics and Evolution 127: 732–745. Tampi, P.R.S. (1960): On the early development of Protula tubularia (Montagu), (family Serpulidae, Polychaeta). Journal of the Marine Biological Association of India 2: 53–56. Taylor, P.D. & Vinn, O. (2006): Convergent morphology in small spiral worm tubes (‘Spirorbis’) and its palaeoenvironmental implications. Journal of the Geological Society 163: 225–228. Thomas, J.G. (1940): Pomatoceros, Sabella and Amphitrite. Liverpool Marine Biology Committee Memoirs 33: 1–87. Thorp, C.H. (1975): The structure of the operculum in Pileolaria (Pileolaria) granulata (L.) (Polychaeta, Serpulidae) and related species. Journal of Experimental Marine Biology and Ecology 20: 215–235. Thorp, C.H. & Sergove, F. (1975): The opercular molt in Spirorbis spirorbis (L.) and S. pusilloides Bush (Polychaeta: Serpulidae). Journal of Experimental Marine Biology and Ecology 19: 117–143. Thorp, C.H., Pyne, S., & West, S.A. (1987): Hydroides ezoensis Okuda, a fouling serpulid new to British coastal waters. Journal of Natural History 21: 863–877. Thiriot-Quiévreux, C. (1965): Déscription de Spirorbis (Laeospira) pseudomilitaris n. sp. Polychète Spirorbinae, et de sa larve. Bulletin du Muséum d’Histoire Naturelle, Paris (Ser. 2) 37(3): 495–502. Toonen, R.J. & Pawlik, J.R. (1994): Foundations of gregariousness. Nature 370: 511–512. Toonen, R.J. & Pawlik, J.R. (1996): Settlement of the gregarious tube worm Hydroides dianthus (Polychaeta: Serpulidae): cues for gregarious settlement. Marine Biology 126: 725–733. Tovar-Hernández, M.A., Villalobos, T.F., Kupriyanova, E.K. & Sun, Y. (2016): A new fouling Hydroides (Serpulidae, Sabellida,

Annelida) from southern Gulf of California. Journal of the Marine Biological Association of the United Kingdom 96 (3): 693–705. Verrill, A.E. (1873): VIII. Report upon the invertebrate animals of Vineyard Sound and the adjacent waters, with an account of the physical characters of the region. Report of the United States Commission of Fish and Fisheries, 757 pp. Vine, P. J. (1972): Spirorbinae (Polychaeta: Serpulidae) from the Red Sea, including description of a new species. Zoological Journal of the Linnean Society 51(2): 177–201. Vine, P.J. (1977): The marine fauna of New Zealand: Spirorbinae (Polychaeta: Serpulidae). New Zealand Oceanographic Institute Memoir 68: 1–66. Vine, P.J., Bailey-Brock, J.H. & Straughan, D. (1972): Spirorbinae (Polychaeta, Serpulidae) of the Hawaiian Chain. Part 2. Hawaiian Spirorbinae. Pacific Science 26(2): 150–182. Vinn, O. (2011): The role of an internal organic tube lining in the biomineralization of serpulid tubes. Carnets de Géologie/ Notebooks on Geology—Letter 2011/01: 13–16. Vinn, O. & Wilson, M.A. (2010): Sabellid-dominated shallow water calcareous polychaete tubeworm association from the equatorial Tethys Ocean (Matmor Formation, Middle Jurassic, Israel). Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 258: 31–38. Vinn, O. & Zatoń, M. (2012a): Inconsistencies in proposed annelid affinities of early biomineralized organism Cloudina (Ediacaran): structural and ontogenetic evidences. Carnets de Géologie CG2012_A03. Vinn, O., ten Hove, H.A., Mutvei, H. & Kirsimäe, K. (2008): Ultrastructure and mineral composition of serpulid tubes (Polychaeta, Annelida). Zoological Journal of the Linnean Society 154: 633–650. Uchida, H. (1978): Serpulid tube worms (Polychaeta, Sedentaria): from Japan with the systematic review of the group. Bulletin of the Marine Park Research Stations 2: 1–98. Wang, J., & Huang, Z. (1993): Fouling polychaetes of Hong Kong and adjacent waters. Asian Marine Biology 10: 1–12. Willette, D.A., Iñiguez, A.R., Kupriyanova, E.K., Starger, C.J., Varman, T., Toha, A.H., Maralit, B.A. & Barber, P.H. (2015): Christmas tree worms of Indo-Pacific coral reefs: untangling the Spirobranchus corniculatus (Grube, 1862) complex. Coral Reefs 34: 899–904. Willey, A. (1905): Report on the Polychaeta collected by Professor Herdman, at Ceylon, in 1902. In: Herdman, W.A. (1905). Report to the government of Ceylon on the pearl oyster fisheries of the Gulf of Manaar. London, Royal Society, 4, Supplementary Report 30: 243–342. Williams, J.B. (1964): The effect of extracts of Fucus serratus in promoting the settlement of larvae Spirorbis borealis (Polychaeta). Journal of the Marine Biological Association of the United Kingdom 44: 397–414. Zatoń, M., Vinn, O. & Tomescu, M. (2012): Invasion of freshwater and variable marginal marine habitats by microconchid tubeworms—an evolutionary perspective. Geobios 45: 603–610. Zibrowius, H. (1969a): Review of some little known genera of Serpulidae (Annelida Polychaeta). Smithsonian Contributions to Zoology 42: 1–22. Zibrowius, H. (1969b): Quelques nouvelles récoltes de Serpulidae (Polychaeta Sedentaria) dans le Golfe de Gabès et en Tripolitaine. Description de Vermiliopsis pomatostegoides n. sp. Bulletin de l’Institut d’Océanographie et Pêche, Salammbô 1: 123–136.

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Zibrowius, H.W. (1970): Serpulidae (Annelida Polychaeta) des campagnes du “Skagerak” (1946) et du “Faial” (1957) au large de Portugal. Boletim da Sociedade Portuguesa de Ciências Naturais 12: 117–131. Zibrowius, H. (1971): Revision of Metavermilia Bush (Polychaeta, Serpulidae), with descriptions of three new species from off Portugal, Gulf of Guinea and Western Indian Ocean. Journal of the Fisheries Research Board of Canada 28: 1373–1383. Zibrowius, H. (1972a): Un espèce actuelle du genre Neomicrorbis Rovereto (Polychaeta, Serpulidae) découverte dans l’étage bathyal aux Açores. Bulletin du Muséum d’Histoire Naturelle 33: 423–430. Zibrowius, H. (1972b): Mise au point sur les espèces Méditerranéennes de Serpulidae (Annelida Polychaeta) décrites par Stefano delle Chiaje (1822–1829, 1841–1844) et Orionzo Costa (1861). Téthys 4: 113–126. Zibrowius, H., (1973a): Revision of some Serpulidae (Annelida Polychaeta) from abyssal depths in the Atlantic and Pacific, collected by the “Challenger” and Prince of Monaco Expeditions. Bulletin of the British Museum (Natural History) 24: 427–439. Zibrowius, H. (1973b): Serpulidae (Annelida Polychaeta) des côtes ouest de l’Afrique et des Archipels Voisins. Musée Royal de l’Afrique Centrale, Tervuren, Belgique: Annales, Série 8, Sciences Zoologiques 207: 1–93. Zibrowius, H. (1977): Review of Serpulidae (Polychaeta) from depths exceeding 2000 meters. In: Reish, D.J. & Fauchald, K. (Eds.). Essays on polychaetous annelids in memory of Dr. Olga Hartman. Allan Hancock Foundation, Los Angeles, California, pp. 289–305. Zibrowius, H. (1979a): Vitreotubus digeronimoi n. g., n. sp. (Polychaeta Serpulidae) du Pléistocène inférieur de la Sicile et de l’étage bathyal des Açores et de l’Océan Indien. Téthys 9(2): 183–190. Zibrowius H. (1979b) Serpulidae (Annélida Polychaeta) de l´Océan Indien arrivés sur le côques de bateaux à Toulon (France, Méditerranée). Rapport et procès verbaux des réunions, CIESM 25–26(4): 133–134. Zibrowius, H. (1991): Ongoing modification of the Mediterranean marine fauna and flora by the establishment of exotic species. Mésogée 51: 83–107. Zibrowius, H. (2002): Assessing scale and impact of ship-transported alien fauna in the Mediterranean? In: Briand, F. (Ed.). CIESM Workshop Monograph no. 20, Istanbul, 6–9 November 2002. Alien marine organisms introduced by ships in the Mediterranean and Black Sea. CIESM, Monaco, pp. 63–68. Ziegler, V. (1984): Family Serpulidae (Polychaeta, Sedentaria) from the Bohemian Cretaceous Basin. Sborník Národního Muzea v Praze 39B: 213–254.

Günter Purschke

7.5 Sedentaria: Opheliida/ Terebellida/Clitellata: incertae sedis 7.5.1 Hrabeiellidae Christoffersen, 2012 Introduction Hrabeiellidae is a monotypic taxon comprising one of only two described terrestrial nonclitellate annelid species, Hrabeiella periglandulata Pizl and Chalupsky, 1984

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(Fig. 7.5.1.1 A–C). The other terrestrial species is Parergodrilus heideri Reisinger, 1925 (see chapter Parergodilidae Vol.  1, p. 237). Both species have meiofaunal dimen­ sions; H.  periglandulata reaches approximately 2 mm in length and mature individuals have 15 segments (Pizl and Chalupsky 1984, Rota 1998). H. periglandulata has an oligochaete-like appearance without anterior or posterior appendages. The ­parapodia are reduced to four bundles of chaetae with flattened blades of only one type (Fig. 7.5.1.1 D, E). Since its first description, similarities with oligochaetous Clitellata were recognized (Pizl and Chalupsky 1984, Rota and Lupetti 1996, Purschke 1999, 2000, 2003). These similarities include a small prostomium lacking appendages such as antennae or palps, absence of parapodia, short and simple chaetae, a smooth cuticular surface without kinocilia, simultaneous hermaphroditism, a dorsal pharynx, a brain situated behind the prostomium with single circumesophageal connectives, a subepidermal ventral nerve cord with ill-defined ganglia, and filiform spermatozoa (Purschke 2000, 2003). However, the absence of a typical clitellum, the different structure and position of the genital organs as well as the ultrastructure of the spermatozoa and chaetae were regarded as clear objections to the placement of H. periglandulata within Clitellata (Pizl and Chalupsky 1984, Rota and Lupetti 1996, 1997, Rota 1998, Purschke 1999, 2000). Although also similar to the other terrestrial polychaete species mentioned previously, P. heideri, there is no evidence of a close relationship, either from molecular or from morphological data (Rota 1998, Purschke 1999, 2006, Rota et  al. 2001, Struck et al. 2002, Jördens et al. 2004); instead, the similarities must be interpreted as having evolved by convergence due to similar selection pressures in similar habitats, as suggested by Purschke (1999). Although this view is generally accepted and beyond discussion now; in certain reviews, they are still treated in a single chapter (e.g., Rouse and Pleijel 2001). Due to its aberrant morphology and occurrence as well as to their similarities with enchytraeids, it is not surprising that of H. periglandulata was first detected (Graefe 1977) and finally described by oligochaete researchers (Pizl and Chalupsky 1984). For several years, the species was only known from Europe but recently it has also been found in Asia (Korea) (Rota and de Jong 2015). Morphology External morphology With a cylindrical body without any appendages, H. periglandulata resembles an oligochaete on first sight (Fig. 7.5.1.1 A–C). Due to the limited number of segments, the animals are comparatively stout, and with body dimensions of 1.5 mm to 2 mm by 0.1 to 0.15 mm, they are

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Fig. 7.5.1.1: Hrabeiella periglandulata. Habitus and internal organization. A, drawing of whole specimen with characteristic arrangement of epidermal glands; B, internal organization from histological sections; C, living adult animal, photomontage; D, typical arrangement of chaetae in left half of a segment; E, enlargement of two chaetae in frontal and lateral view. Abbreviations: b, brain; ch, chaeta; dph, dorsal pharynx; egl, epidermal gland; gl, presumed cocoon gland; i, intestine; moo, mature oocyte; ne, nephridium; oo, oocyte; pb, penial bulb; pgl, prostate gland; st, stomach; sv, seminal vesicle; te, testis; vnc, ventral nerve cord. A, B, redrawn from Pizl and Chalupský (1984); C–E, LM micrographs: K. Rainer, Osnabrück, Germany.

shorter than most oligochaete species. However, certain members of Enchytraeidae, such as Marionina eleonore Rota, 1995, have similar body dimensions (Rota 1998). Similar to oligochaetous Clitellata, the body surface is without locomotory cilia and sensory cells form indistinct buds with cilia only arising slightly above the cuticle (Purschke 1999; fig. 6). Thus, in the SEM, the body surface appears rather smooth except for the pores of the gland cell openings (Fig. 7.5.1.2 A). The body of Hrabeiella is composed of prostomium, peristomium, usually 14, rarely 15, segments, and pygidium (Pizl and Chalupsky 1984, Rota 1998, Purschke 1999, 2006).1All segments bear chaetae, and except for the peristomium, each segment is composed of two more or less indistinct rings (Figs. 7.5.1.1 A, C and 7.5.1.2 A). The chaetae are arranged in four pairs of ventrolateral bundles, typical parapodia are lacking. Usually, there are two or three chaetae per bundle and, only occasionally, four chaetae were encountered per bundle (Pizl and Chalupsky 1984, Rota and Lupetti 1996). There is only one type of chaeta. The chaetae have a shovel-like structure and consist of a shaft bearing a distally flattened part (Figs. 7.5.1.1 D, E and 7.5.1.2 A–F) (Pizl and Chalupsky 1984, Jans and Römbke 1989, Rota and Lupetti 1996, Erséus and Rota 1998, Rota 1998, Purschke 1999, Dózsa-Farkas and Schlaghamerský 2013). The chaetae are 30 to 35 µm long, the shaft measures 21 to 26 µm including

1 It should be noted that in the original description the segments were counted as usual in oligochaetes starting with the prostomium as I, peristomium as II, 1st chaetiger as III and ending with the pygidium as XVI.

a 7- to 9-µm-long section attached to the posterior facing smooth side of the shovel-like part (Fig. 7.5.1.2 D–F). The shaft has a diameter of approximately 1.5 µm and tapers toward its pointed distal end, whereas the flattened part is up to 7 µm wide. The ultrastructure of the chaetae reveals that the shaft is composed of tubules (Fig. 7.5.1.2 F) as typical of annelid chaetae (Hausen 2005) but distally it appears more or less solid and electron-dense (Fig. 7.5.1.2 E, F). The shovel-like part gives off numerous densely arranged fibers or bristles so that each chaeta resembles a handled brush (Rota and Lupetti 1996, Erséus and Rota 1998, Purschke 1999). Approximately 120 to 150 bristles, 130 to 150 nm in diameter, can be counted on cross-sections of the chaetae (Rota and Lupetti 1996; Fig. 7.5.1.2 E). The shovel-like part is less electron-dense than the shaft and comprises a hollow core. TEM and SEM investigations of the chaetae have been carried out by Rota and Lupetti (1996) and Purschke (1999), revealing an almost identical fine structure. Other investigators using only SEM could not reproduce the brushlike appearance of the shovel-like part (Jans and Römbke 1989, Dózsa-Farkas and Schlaghamerský 2013). However, it seems to be the consensus that these differences are a result of the fixation method applied. Anatomy The body wall comprises a cuticle, epidermis, ECM, circular, and longitudinal muscle fibers followed by a thin coelothelium (Rota and Lupetti 1996). However, the muscle layer is not continuous and consists of isolated fibers; in the gaps, the ECM directly borders the coelothelium. The



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Fig. 7.5.1.2: Hrabeiella periglandulata. External morphology and morphology of the chaetae. A–D, SEM micrographs; E, TEM micrograph. A, ventrolateral view of anterior end with small prostomium (pr), peristomium (pe), first chaetiger (ch1) and second chaetiger, segment borders indistinct and marked by arrows; note comparatively smooth body surface and openings of numerous gland cells (arrowheads). B, two bundles of chaetae of midbody segment, frontal side with brushlike surface; C, frontal side; D, abfrontal side showing smooth part with extension of chaetal shaft, arrow points to tip of shaft; E, cross-section with base of shovel-like part and shaft of chaeta; F, oblique longitudinal section with follicle cells (fc) and musculature; follicle cells without cuticular lining (arrows); arrowheads, attachment zone of chaeta to follicle cell; asterisk, apical thickening of chaetal shaft. Abbreviations: ch1, first chaetiger; chb, chaetal brush; chs, chaetal shaft; cpm, chaetal promotor muscle; cptm, chaetal protractor muscle; crm, chaetal remotor muscle; cu, cuticle; ec, epicuticle; ecm, extracellular matrix; ep, epidermis; fc, follicle cell; mo, mouth; pe, peristomium; pr, prostomium; tf, tonofilaments. Micrographs: A–D, W. Mangerich, Osnabrück.

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cuticle is comparatively thick (1.6–2.1 µm) and comprises a basal cuticle without distinct collagen fibers, a thin epicuticle covered by a layer of epicuticular projections and a glycocalix (Fig. 7.5.1.2 E, F; Rota and Lupetti 1998, Purschke 1999). In contrast to aquatic annelids, this cuticle is only penetrated by very few microvilli. The cuticle forms a smooth surface only interrupted by the gland cell ­openings (Fig. 7.5.1.2 A), the chaetal follicles, and the nuchal pit. The epidermis consists of supporting cells, secretory cells, and a few types of receptor cells (Rota and Lupetti 1996, Purschke 1999). In contrast to aquatic polychaetes of comparable small body size, the supportive cells are without kinocilia, and collar receptors are lacking as well (Rota 1998, Purschke 1999). These features may be adaptations to the terrestrial environment (Purschke 1999). The only cilia penetrating the cuticle are those of the receptor cells forming small buds. Their cilia extend above the body surface for just a few nanometers. The gland cells may structurally be assigned to at least three types; the granular cells sensu Rota and Lupetti (1996) are responsible for the white-spotted appearance of living individuals under incident light. All gland cell bodies bulge deeply into the body cavity. The circular musculature comprises a few separated fibers; in the gaps, gland cell bodies are located. The longitudinal musculature is stronger and arranged in 12 bundles of fibers likewise separated by the cell bodies of the gland cells (Rota and Lupetti 1996). Other important musculature comprises the protractors and retractors as well as promotor and remotor muscle fibers of the chaetae and pharynx (Figs. 7.5.1.2 F and 7.5.1.3 A, B) (Rota and Lupetti 1996, Purschke 1999, 2003). The gut system is lined by a thin myoepithelium (Fig. 7.5.1.6). Frequently, spaces of the intestinal blood sinus can be observed in the ECM (Rota and Lupetti 1996, Rota 1998). The alimentary canal is made up of a ventral mouth opening in the peristomium, buccal cavity, dorsal pharynx, esophagus, stomach, intestine, rectum, and terminal anus (Figs. 7.5.1.1 B, 7.5.1.2 A, and 7.5.1.3 A; Pizl and Chalupsky 1984, Rota and Lupetti 1996, Rota 1998, Purschke 2003). The mouth opening leads to an unciliated buccal cavity, which gives rise to the dorsal pharynx in the first chaetiger. The dorsal pharynx is followed by the ciliated anterior part of the esophagus. The buccal cavity and anterior ­esophagus are lined by a thin cuticle indicative of their ectodermal origin. The dorsal pharynx, situated in the first and second chaetiger, comprises a densely ciliated pad, four pairs of glandular lobes, and a prominent system of protractor and retractor muscles attached to the epithelium of the pad (Purschke 2003). From the glandular lobes, the gland cells send processes ventrally that open between

the ciliated cells of the pad. The anterior esophagus is followed by a short part without a cuticle, which opens into the spacious stomach in chaetiger 3. In chaetiger 7, it gives rise to the coiled intestine, which expands into a heavily ciliated anal cavity in the pygidium. The entire gut system is connected to the body wall by dorsal and ventral mesenteries (Rota and Lupetti 1996, Rota 1998). It is ciliated throughout and the epithelial cells additionally bear a well-developed brush border of microvilli. At least in the stomach, two cell types can be distinguished; typical epithelial cells and cells appearing dark in the light microscope and electron-dense in TEM (Fig. 7.5.1.6). These cells might be storage cells. The nervous system is comparatively simple but, unlike many other small annelids, brain and ventral nerve cord are situated subepidermally (Purschke 2016). It comprises an anterior brain and a chain of ventral ganglia connected by short connectives (Pizl and Chalupsky 1984, Rota and Lupetti 1996, Rota 1998, Purschke 1999, 2000, 2003; Figs. 7.5.1.3 A and 7.5.1.4). In contrast to the situation typical of polychaetes, the brain lies in the peristomium and is connected to the body wall by two anterior prolongations containing part of the neuronal somata. Other attachment structures are formed by the nuchal organs, which are located deeply inside the body and lie beside the brain and the circumesophageal connectives (Figs. 7.5.1.4 and 7.5.1.5 C). Most of the somata of the brain are present in a pair of larger posterior prolongations. The neuropil is u-shaped and anteriorly gives rise to the circumesophageal connectives. The reason for the peculiar arrangement most likely is related to the small size of the prostomium, which more or less is represented by a layer of epidermal cells (Purschke 1999). The circumesophageal connectives are not divided into dorsal and ventral roots, unite behind the mouth and form a unineurlian ventral cord (see Purschke 2016) in which the paired neurite bundles are indistinguishable and form a single structure (Figs. 7.5.1.4 and 7.5.1.6). The first ganglion is situated in chaetiger 1 and the chain of ganglia extends to the last chaetiger (Figs. 7.5.1.1 B, 7.5.1.3 A, 7.5.1.4, and 7.5.1.6). The gut is innervated by two pairs of stomatogastric nerves that originate close together from the circumesophageal connectives (Fig. 7.5.1.3 A). The larger pair is situated dorsally and innervates the dorsal pharynx and the dorsolateral regions of the foregut. The pair of smaller nerves emanates somewhat more ventrally and innervates the ventral regions of the gut system. Sensory organs are poorly developed and no sense organs were observed and mentioned in the species’ description (Pizl and Chalupsky 1984). Although focusing on the ultrastructure of the body wall and the



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Fig. 7.5.1.3: Hrabeiella periglandulata. Dorsal pharynx (dph), anterior part of foregut and nervous system. A, schematic reconstruction of anterior end in sagittal view: prostomium (pr), peristomium (pe); first (ch1), second (ch2), and third chaetigers; segment borders marked by arrows; note brain (b) situated in the peristomium and attached to the prostomial epidermis by a small strand of tissue (arrowhead). Foregut comprises buccal cavity (bc), dorsal pharynx (dph), esophagus (es), and stomach (st). B, cross-section of dorsal pharynx showing ciliated pad (cip) in the resting position, stomodeal epithelium lined by a thin cuticle, muscle fibers (phmu) attached to the ciliated epithelium and gland cells (pgl) located dorsally, TEM. Abbreviations: b, brain; bc, buccal cavity; bw, body wall; cc, circumesophageal connective; ch1, first chaetiger; ch2, second chaetiger; cip, ciliated pad; cu, cuticle; cuf, cuticular fold; dph, dorsal pharynx; g1, first ganglion in vnc; mo, mouth; es, esophagus; pe, peristomium; pgl, pharyngeal gland; phl, pharyngeal lumen; phmu, pharyngeal muscles; pr, prostomium; sn1,2, stomatogastric nerve 1, 2; st, stomach; step, stomodeal epithelium; vnc, ventral nerve cord. A, modified from Purschke (1999).

chaetae, isolated receptor cells were mentioned by Rota and Lupetti (1996). In a survey on sensory structures, several types of ciliated receptor cells were found to be distinguished by the number of cilia and whether they penetrate the cuticle or remain inside the cuticle (Purschke 1999). However, two types of sense organs are also present: nuchal organs and photoreceptor-like ciliated sense organs (Fig. 7.5.1.5 A–D; Purschke 1999, 2000). Because the nuchal organs are internalized, they are almost invisible from the exterior (Fig. 7.5.1.5 A, B) and, as such, it is not surprising that they have not been found in initial investigations. In SEM, a small opening

is usually visible but can hardly be distinguished from gland cell openings and only occasionally do the tips of a few motile cilia extend to the outside. The nuchal organs are made up of unciliated supportive cells forming the nuchal pit, which houses motile cilia originating from basally located supportive cells. Here, a small olfactory chamber exists in which the sensory cilia of a few primary receptor cells can be found (Fig. 7.5.1.5 C; Purschke 1999, 2000). The receptor cells run posteriorly beside the brain and their axons enter the brain posteriorly. The organs are composed of only a few cells; six receptor cells and three to four

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Fig. 7.5.1.4: Hrabeiella periglandulata. Brain, anterior part of nervous system and position of main sensory organs. Schematic reconstruction from serial TEM observations: dorsal brain (b) with single roots of circumesophageal connectives (rcc), anterior (aso) and posterior (pso) expansions of somata, nuchal organs internalized composed of nuchal pit (nup), receptor (rcnu), and supportive cells (suc); photoreceptor-like ciliary sense organs (cso) embedded in anterior somata of the brain. Abbreviations: anu, axons of nuchal organ; aso, anterior somata of brain; b, brain; bc, buccal cavity; cc, circumesophageal connective; cso, ciliary sensory organ; g1, first ganglion in vnc; np, neuropil of brain; nup, nuchal pit; onu, opening of nuchal organ; pso, posterior somata of brain; rcc, root of cc; rcnu, receptor cells of nuchal organ; sdnu, sensory dendrites of nuchal organ; sn1, stomatogastric nerve 1; sonu, receptor cell somata of nuchal organ; suc, supportive cells of nuchal organ; vnc, ventral nerve cord. Modified from Purschke (2000).

ciliated supportive cells have been counted. To some extent, the situation is similar to the marine parergodrilid Stygocapitella subterranea whereas its terrestrial relative Parergodrilus heideri does not have nuchal organs at all (see chapter ­Parergodrilidae Vol. 1, p. 237).

The pair of photoreceptor-like ciliary sense organs is situated in the anterior groups of brain somata (Fig. 7.5.1.4). The organs consist of three cells; a glial supportive cell and two receptor cells (Fig. 7.5.1.5 D; Purschke 2000, 2003). These cells form an internal cavity containing approximately 50 unbranched cilia with modified axonemes. Similar sense structures have been reported from certain polychaetes and microdrile oligochaetes (see Purschke 2003, 2016). Due to structural similarities, ­photoreception (Purschke 2016) has been discussed as a possible function but experimental evidence is still lacking. Phaosomes as typical of Clitellata (Purschke 2016) have not been described and are most likely lacking. The body cavity of Hrabeiella is a true coelom; the epidermis is lined by an ECM followed by muscle fibers and a thin coelothelium. This lies directly on the ECM where the muscle grid is interrupted (Rota and Lupetti 1996, Rota 1998). The gut is surrounded by a myoepithelium, which continues in the mesenteries. In contrast to the original description (Pizl and Chalupsky 1984), Rota (1998) reported the presence of incomplete septa. Free coelomocytes are absent. A blood vascular system is present; main vessels include a dorsal and a ventral vessel united by a prominent loop between pharynx and stomach (see figs. 1 and 2 D in Purschke 2003). These are accompanied with a well-developed blood sinus of the gut system (e.g., fig. 7.14.6.6 and fig. 26 in Rota and Lupetti 1996). The wall of the vessels is formed by the ECM followed by peritoneal cells. In front of the stomach, the dorsal vessel is rather spacious and forms a heartlike structure (Pizl and C ­ halupsky 1984, Purschke unpubl. obs.). Inside the spacious anterior part of the dorsal vessel, a few cells are present which are attached to the wall of the vessel and may constitute a heart body. Starting in chaetiger 2 and ending in chaetiger 12, paired metanephridia are present in almost every segment (Fig. 7.5.1.1 B; Pizl and Chalupsky 1984, Rota 1998). It is impossible to determine, from these descriptions, which segments lack nephridia (see Rouse and Pleijel 2001). The organs are characterized by long and convoluted ducts terminating in wide atria that are either close together or form a common structure. The openings are indistinct and not observable in light microscopy. The ultrastructure of the excretory system is still unknown.

Reproduction and development Hrabeiellla periglandulata is a simultaneous hermaphrodite (Pizl and Chalupsky 1984, Rota and Lupetti 1997,



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Fig. 7.5.1.5: Hrabeiella periglandulata. Sensory organs. A–C, nuchal organ; D, photoreceptor-like ciliary sense organ. A, anterior end in lateral view with prostomium (pr) and peristomium (pe); boxed area: nuchal pit and enlarged in B. B, opening of nuchal pit with a few cilia projecting outside. C, reconstruction of nuchal organ; nuchal organ composed of unciliated supportive cells (usuc) forming the wall of nuchal pit (nup) and ciliated supportive cells (csuc) and bipolar primary sensory cells (anu, sdnu, sonu). Ciliated supportive cells line olfactory chamber (oc); after TEM observations. D, reconstruction of photoreceptor-like ciliary sense organ comprising two receptor cells (sc1, sc2) and a glial supportive cell (gsuc); numerous unbranched cilia (sci) project into an internalized cavity. Abbreviations: anu, axons of nuchal organ; b, brain; coel, coelothelium; csuc, ciliated supportive cells; cu, cuticle; ecm, extracellular matrix; ep, epidermis; gsuc, glial supportive cell; mo, mouth; nsc, nucleus of sensory cell; nup, nuchal pit; oc, olfactory chamber; onu, opening of nuchal organ; pe, peristomium; pr, prostomium; sb, sensory bulb; sc1, 2, sensory cell 1, 2; sci, sensory cilia; sd, sensory dendrite; sdnu, sensory dendrites of nuchal organ; son, soma of adjacent neuron; sonu, somata of nuchal organ; usuc, unciliated supportive cells. A, B, SEM micrographs (W. Mangerich, Osnabrück); C, D modified from Purschke (2000).

Rota 1998, Purschke 2006). The male organs lie in chaetiger 5. The paired organs comprise testes, unequally developed seminal vesicles, and ciliated ducts. The ducts run ventrally and open in a common midventral penial bulb associated with a prominent prostate gland (Fig. 7.5.1.6). Female organs are unpaired and consist of an ovary in chaetigers 12 and 13 followed by an ovisac simultaneously containing only one vitellogenic oocyte. Depending on the degree of maturity, the ovisac may extend to the last chaetiger. The oocytes contain unusually large yolk droplets (Rota 1998). Although in the original description, accessory glands were not reported, Rota (1998) described

paired voluminous structures that might represent glands associated with the female organs. Seminal receptacles are lacking. Spermatozoa develop on typical cytophores within the seminal vesicles (fig. 7.14.6.6) but only spermatozoa have been investigated using electron microscopy (Rota and Lupetti 1997, Purschke 2006). Mature spermatozoa are filiform with an elongated conical acrosome. The nucleus is elongated as well with an asymmetric tip extending into the acrosomal region. The midpiece is made up of a single threadlike mitochondrion and seven accessory rods ­surrounding the axoneme. These are accompanied by numerous additional smaller

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so-called accessory tubules. Thus, sperm morphology is completely different from clitellates (see, e.g., ­Jamieson 2006). Mode of fertilization and copulation as well as egg deposition are unknown, although the species may be cultured successfully in a thin layer of soil on agar (Rota 1998). Occasionally, couples of individuals lying close together have been observed; suggesting mating. The smallest individuals observed possessed five chaetigers (Rota 1998).

Biology and ecology Data on the ecology and biology of H. periglandulata are comparatively scarce and primarily consist of faunistic data (see above). Most likely, the species feeds on decayed organic matter (Jans and Römbke 1989). The gut contains a mixture of amorphous humus particles and mineral soil grains, which is typical for saprophagous inhabitants of mineral soils. The animals prefer slightly acid soils and apparently avoid basic soils. There seems to be no preference to a certain type of vegetation (e.g., Jans and Römbke 1989, Dózsa-Farkás and Schlaghamerský 2013). In certain localities, abundance may be very high and up to 16,700 individuals per square meter have been recorded (Jans and Römbke 1989). Data on the life cycle and reproductive periods do not exist. Distribution Hrabeiella periglandulata occurs in fresh, slightly acidic, and well-drained soils preferring the upper mineral layer ranging from meadows to different types of forests (beech, fir, spruce) (Jans and Römbke 1989, Rota 1998). Originally described from South Bohemia (Czech Republic) (Pizl and Chalupsky 1984), H. periglandulata is now known from numerous locations in Europe including the South of Sweden (Erséus and Rota 1998), Denmark (DózsaFarkas and Schlaghamerský 2013), Germany (Graefe 1977, 1989, 1990, 1993a, b, Jans and Römbke 1989, Purschke 1999, Haag et al. 2009, Dózsa-Farkas and Schlagmerský 2013), Czechia (Schlagmerský and Sídova 2007, 2009), Poland (Dumnicka  and Rozen 2002), Hungary (DózsaFarkas and Schlagmerský 2013), Romania (Dózsa-Farkas and Schlaghamerský 2013), Austria (Bauer 2003), Italy (Rota and Lupetti 1996, 1997, Rota 1998, Ascher et al. 2012), and Spain (Dózsa-Farkas and Schlaghamerský 2013). To date, there is only one record outside Europe: Dózsa-Farkas and Hong (2010) reported the species as Hrabeiella sp. from Korea. The lack of records outside Europe is probably due to less intense sampling activities rather than to true absence.

Fig. 7.5.1.6: Hrabeiella periglandulata. Cross-section through chaetiger 5 with male genital organs; only left seminal vesicle (sv), testis (te), and prostate gland (pgl) visible; coelomic cavity (coe) almost entirely occupied by internal organs; epithelium of stomach (epst) formed by two cell types, electron-dense basal cells (asterisks) and digestive cells with well-developed brush border of microvilli and cilia; arrowheads point to blood spaces of the intestinal sinus (TEM). Abbreviations: coe, coelom; cu, cuticle; cy, cytophore with developing spermatids; egl, epidermal gland; ep, epidermis; epst, epithelium of stomach; lst, lumen of stomach; pgl, prostate gland; spf, flagella of mature sperm; spn, nuclei of mature sperm; sv, seminal vesicle; te, testis; vnc, ventral nerve cord. Micrograph K. Rainer, Osnabrück, Germany; modified from Purschke (2006).

Phylogeny and taxonomy Although described by Pizl and Chalupsky not earlier than in 1984, H. periglandulata was first mentioned in the literature by Graefe (1977) as Adenodrilus. Since that time, structural similarities with Clitellata and Parergodrilidae were recognized and the phylogenetic significance of these common characters were discussed (Graefe 1977, Pizl and Chalupsky, 1984, Jans and Römbke 1989, Erséus and Rota 1998, Rota and Lupetti 1997, 1998, Rota 1998, Purschke 1999, 2000, 2003, 2006, Zrzavy et al. 2009, Christoffersen 2012). However, until today, the phylogeny and systematic position of Hrabeiella is still unresolved, enigmatic, and somewhat controversial. First phylogenetic studies using molecular markers (18S rDNA) could not solve its position but rejected a closer relationship to Parergodrilidae (Rota et al. 2001). Likewise, a closer relationship to Clitellata was not found. As a result, the view of convergent evolution of Hrabeiella based on morphological data was put forward. Thus, the absence of a typical clitellum, the different structure and position of the genital organs as well as the ultrastructure of the spermatozoa and chaetae were regarded as clear

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objections for the placement of H. periglandulata within Clitellata (Rota and Lupetti 1996, 1997, Rota 1998, Purschke 1999, 2000). However, after a study of the dorsal pharynx and internal ciliated cerebral sense organs, a possible relationship between Hrabeiella and Clitellata was brought back into discussion (Purschke 2003). Interestingly, a molecular study using 18S, 28S rDNA, and COI sequences could neither reject nor support a sister group relationship of Hrabeiella and Clitellata (Jördens et al. 2004). Although the two clustered together in certain analyses, this placement did not receive sufficient statistical support but convergent evolution of the former and Parergodrilidae was highly supported. Whereas such a relationship could not be maintained in the study by Rousset et al. (2007), Zrzavy et al. (2009) likewise found a stable relationship of Hrabeiella (together with Aphanoneura) as sister to ­Clitellata. Nevertheless, this initiated a morphological ­analysis by Christoffersen (2012), who found Hrabeiella and Clitellata (the latter named Euclitellata by him) as sister groups. This clade was named Dorsopharyngea according to the most striking possible synapomorphy, the dorsal pharynx. In fact, there exist several subtle correspondences in its fine structure and most importantly such a pharynx is unknown in any other annelid (Tzetlin and Purschke 2005). This is further supported by a corresponding structure of the nervous system and the cerebral sense organs (Jördens et al. 2004). Whereas other hypotheses presented in the study of Christoffersen (2012) have been disproven by molecular phylogenomic analyses, such as his supposed taxon composition of Clitellata sensu lato (e.g., Struck et al. 2011, 2015, Weigert et al. 2014, Laumer et al. 2015, Weigert and Bleidorn 2016), at present, the hypothesized sister group relationship of Hrabeiella and Clitellata cannot be ruled out. Further studies preferably using phylogenomic data seem to be necessary to resolve the relationship of Hrabeiella (see Struck 2012). Individuals from different localities seem to be morphological identical when viewed under the light microscope. Whereas Rota and Lupetti (1996) and Purschke (1999) described the chaetae from Italian and German populations as having the same ultrastructure, the observations by Jans and Römbke (1989) and Dózsa-Farkas and Schlaghamerský (2013) revealed a different ultrastructure, especially with respect to the brushlike appearance of the anterior-facing side of the distal part. Whereas the former authors argued that these differences might be the result of fixation procedures rather than true differences, Dózsa-Farkas and Schlaghamerský (2013) discussed whether these differences are genuine structures and might be indicative for the existence of more than one species. Although the European populations of

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H. periglandulata might be a complex of cryptic species, this hypothesis has to be tested using molecular ­fingerprints. Hrabeiellidae Christoffersen, 2012 Type species: Hrabeiella periglandulata Pizl and ­Chalupsky, 1984 Diagnosis: Small, cylindrical, enchytraeid-like animals. Prostomium, peristomium, 14 or 15 chaetigerous segments and rounded pygidium. Palps, antennae, parapodia, and pygidial cirri absent. Body not differentiated into regions. Chaetae more or less simple, distally shovel-like arranged in two paired rows of ventrolateral bundles. Epidermis without locomotory cilia; whitish transparent, with conspicuous epidermal glands arranged in longitudinal and transverse rows, visible as white spots in living individuals; eyes absent, nuchal organs internalized; hermaphroditic, male organs in chaetigers 5 and 6, female organs in chaetigers 11 and 12, gonoducts present (Pizl and Chalupsky 1984, Rota and Lupetti 1996, 1997, Rota 1998, Erseus and Rota 1998, Purschke 1999, 2000, 2003). Hrabeiella Pizl and Chalupsky, 1984 Type species: Hrabeiella periglandulata Pizl and ­Chalupsky, 1984. Monotypic. Remarks: The existence of several cryptic species in the Northern Hemisphere and in Europe is discussed (­Dózsa-Farkas and Schlaghamerský 2013).

References Ascher, J., Sartori, G., Graefe, U., Thornton, B., Ceccherini, M.T., Pietramellara, G. & Egli, M. (2012): Are humus forms, mesofauna and microflora in subalpine forest soils sensitive to thermal conditions? Biology and Fertility of Soils 48: 709–725. Bauer, R. (2003): Characterization of the decomposer community in Austrian pasture and arable field soils with respect to earthworms and potworms (Annelida: Lumbricidae and Enchtraeidae). Newsletter on Enchytraeidae 8: 41–50. Christoffersen, M.L. (2012): Phylogeny of basal descendants of cocoon-forming annelids (Clitellata). Turkish Journal of Zoology 36: 95–119. Dózsa-Farkas, K. & Hong, Y. (2010): Three new Hemienchytraeus species (Enchytraeidae, Oligochaeta, Annelida) from Korea, woth first records of other enchytraeids and terrestrial polychaetes (Annelida). Zootaxa 2406: 29–56. Dózsa-Farkas, K. & Schlaghamerský, J. (2013): Hrabeiella periglandulata (Annelida: “Polychaeta”)—do apparent differences in chaetal ultrastructure indicate the existence of several species in Europe? Acta Zoologica Academiae Scientiarum Hungricae 59: 143–156. Dumnicka, E. & Rozen, A. (2002): The first record of the terrestrial polychaete Hrabeiella periglandulata Pizl & Chalupsky, 1984,

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in Poland, with a note on anatomy and ecology. Fragmenta Faunistica, Warszawa 45: 1–7. Erseus, C. & Rota, E. (1998): Havsbostmaskar pa torra land. Fauna och Flora Arg 93: 97–104. Graefe, U. (1977): Adenodrilus Graefe (in press) and Parergodrilus Reisinger: two aberrant Annelida in forest soils. P. Cent. Pir. Biol. Exp. 9: 25. Graefe, U. (1989): Einfluss von sauren Niederschlägen und Bestandeskalkungen auf die Enchytraeidenfauna in Waldböden. Verhandlungen der Gesellschaft für Ökologie 17: 597–603. Graefe, U. (1990): Untersuchungen zum Einfluss von Kompensationskalkung und Bodenbearbeitung auf die Zersetzerfauna in einem bodensauren Buchenwald- und Fichtenforst-Ökosystem. In Gehrmann, J. (ed.) Umweltkontrolle am Waldökosystem. Forschung und Beratung Reihe C, Münster 48: 232–241. Graefe, U. (1993a): Die Gliederung von Zersetzergesellschaften für die standortökologische Ansprache. Mitteilungen der Deutschen Bodenkundlichen Gesellschaft 69: 95–98. Graefe, U. (1993b): Veränderungen der Zersetzergesellschaften im Immissionsbereich eines Zementwerkes. Mitteilungen der Deutschen Bodenkundlichen Gesellschaft 72: 531–534. Haag, R., Stempelmann, I. & Haider, J. (2009): Bodenbiologische Untersuchungen auf Bodendauerbeobachtungsflächen in Nordrhein-Westfalen im Zeitraum 1995–2007. Landesamt für Natur, Umwelt und Verbraucherschutz Nordrhein-Westfalen, Essen: http://www.lanuv.nrw.de/boden/pdf/Bericht_Bio_ BDF_30_11_09.pdf. Hausen, H. (2005): Chaetae and chaetogenesis in polychaetes (Annelida). Hydrobiologia 535/536: 37–52. Jamieson, B.G.M. & Ferraguti, M (2006): Non-leech Clitellata. In Rouse, G., Pleijel, F. (eds.) Reproductive Biology and Phylogeny of Annelida. Science Publishers, Enfield: 235–392. Jans, W. & Römbke, J. (1989): Funde eines terrestrischen Polychaeten (Annelida) in Wäldern Baden-Württembergs. Carolinea 47: 158–162. Jördens, J., Struck, T. & Purschke, G. (2004): Phylogenetic interference regarding Parergodrilidae and Hrabeiella periglandulata (“Polychaeta”, Annelida) based on 18S rDNA and COI sequences. Journal of Zoological Systematics and Evolutionary Research 42: 270–280. Laumer, C.E., Bekkouche, N., Kerbl, A., Goetz, F., Neves, R.C., Sørensen, M. V., Kristensen, R.M., Hejnol, A., Dunn, C.W., Giribet, G. & Worsaae, K. (2015): Spiralian phylogeny informs the evolution of microscopic lineages. Current Biology 25: 2000–2006. Pizl, V. & Chalupsky, J. (1984). Hrabeiella periglandulata gen. et sp. n. (Annelida)—a courious worm from Czechoslovakia. Vest. cs. Spolec. Zool. 48: 291–295. Purschke, G. (1999): Terrestrial polychaetes—models for the evolution of the Clitellata (Annelida)? Hydrobiologia 406: 87–99. Purschke, G. (2000): Sense organs and central nervous system in an enigmatic terrestrial polychaete, Hrabeiella periglandulata (Annelida)—implications for annelid evolution. Invertebrate Biology 119: 329–341. Purschke, G. (2003): Is Hrabeiella periglandulata (Annelida, “Polychaeta”) the sister group of Clitellata? Evidence from an ultrastructural analysis of the dorsal pharynx in H. periglandulata and Enchytraeus minutus (Annelida, Clitellata). Zoomorphology 122: 55–66. Purschke, G. (2006): Problematic annelid groups. In Rouse, G., Pleijel, F. (eds.) Reproductive Biology and Phylogeny of Annelida. Science Publishers, Enfield: 639–667.

Purschke, G. (2016): Annelida: Basal groups and Pleistoannelida. In Schmidt-Rhaesa, A., Harzsch, & S., Purschke, G. (eds.) Structure and Evolution of Invertebrate Nervous Systems. Oxford University Press, Oxford: 254–312. Rota, E. (1998). Morphology and adaptations of Parergodrilus Reisinger and Hrabeiella Pizl & Chalupsky, two enigmatic soil-dwelling animals. Italian Journal of Zoology 65: 75–84. Rota, E. & DeJong, Y. (2015): Fauna Europaea: Annelida—terrestrial Oligochaeta (Enchytraeidae and Megadrili), Aphanoneura and Polychaeta. Biodiversity Data Journal 3: 1–47. Rota, E. & Lupetti, P. (1996): An ultrastructural investigation of Hrabeiella Pizl & Chalupský, 1984 (Annelida): I. Chaetae and body wall organization. Hydrobiologia 334: 229–239. Rota, E. & Lupetti, P. (1997): An ultrastructural investigation of Hrabeiella Pizl & Chalupský, 1984 (Annelida): II. The spermatozoon. Tissue and Cell 29: 603–609. Rota, E., Martin, P. & Erseus, C. (2001): Soil-dwelling polychaetes: Enigmatic as ever? Some hints on their phylogenetic relationships as suggested by maximum parsimony analysis of 18S rRNA gene sequences. Contributions to Zoology 70: 127–138. Rouse, G.W. & Pleijel, F. (2001): Polychaetes. Oxford University Press, New York: 1–354. Rousset, V., Pleijel F., Rouse, G.W., Erséus, C. & Siddall, M.E. (2007): A molecular phylogeny of annelids. Cladistics 23: 41–63. Schlaghamerský, J. & Sídova, A. (2007): On a species-poor enchytraeid community of peculiar composition. Folia Facultatis Scientiarium Naturalium Universitatis Masarykianae Brunnensis Biology 110: 183–192. Schlaghamerský, J. & Sídova, A. (2009): Dynamics and vertical distribution of a Hrabeiella periglandulata (Annelida) population in South Moravia, Czech Republic. Pesquisa Agropecuária Brasileira 44: 917–921. Struck, T.H. (2012): Phylogeny of Annelida. In Schmidt-Rhaesa, A., (ed.) Zoology Online. DeGruyter, Berlin: 1–23. Struck, T.H., Hessling, R. & Purschke, G. (2002): The phylogenetic position of Aeolosomatidae and Parergodrilidae, two enigmatic oligochaete-like taxa of “Polychaeta”. Journal of Zoological Systematics and Evolutionary Research 40: 155–163. Struck, T.H., Paul, C., Hill, N., Hartmann, S., Hoesel, C., Kube, M., Lieb, B., Meyer, A., Tiedemann, R., Purschke, G. & Bleidorn, C. (2011): Phylogenomic analyses unravel annelid evolution. Nature 471: 95–98. Struck, T.H., Golombek, A., Weigert, A., Franke, F.A., Westheide, W., Purschke, G., Bleidorn, C. & Halanych, K.M. (2015): The evolution of annelids reveals two adaptive routes to the interstitial realm. Current Biology 25: 1993–1999. Tzetlin, A. & Purschke, G. (2005). Pharynx and intestine. In Bartolomaeus, T., Purschke, G. (eds.) Morphology, molecules, evolution and phylogeny in Polychaeta and related taxa. Hydrobiologia 353/536: 199–225. Weigert, A., Helm, C., Meyer, M., Nickel, B., Arendt, D., Hausdorf, B., Santos, S.R., Halanych, K.M., Purschke, G., Bleidorn, C. & Struck, T.H. (2014): Illuminating the base of the annelid tree using transcriptomics. Molecular Biology and Evolution 31: 1391–1401. Weigert, A. & Bleidorn, C. (2016): Current status of annelid phylogeny. Organisms, Diversity and Evolution 16: 345–362. Zrzavý, J., Říha, P., Piálek, L. & Janouškovec, J. (2009): Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evolutionary Biology 9: 189: 1–14.



James A. Blake and Nancy J. Maciolek

7.6 Opheliida/Capitellida 7.6.1 Opheliidae Malmgren, 1867 Introduction Opheliidae is one of the best known and most familiar polychaete families in marine habitats from the intertidal to the deep sea. They are burrowing, infaunal, deposit-feeding polychaetes that occur in a wide variety of sedimentary habitats. Opheliids are typically elongate, slender worms with pointed prostomia that are adapted for rapid burrowing. Their bodies are usually cylindrical and often very sleek in appearance. Opheliids have a variety of sensory adaptations including lateral segmental eyespots, sensory pits, nuchal organs, and papillae. Parapodia are biramous and are provided with simple capillary chaetae. Dorsal cirri are absent; ventral cirri may be present. Branchiae, if present, are sometimes branched or pectinate. The pygidium is often elongate and tubular with species-specific arrangements of papillae and cirri. Based on recent phylogenetic analyses, the subfamily Travisiinae Hartmann-Schröder, 1971, which includes a single genus Travisia Johnston, 1840, is hereby removed from Opheliidae and established as a separate family: Travisiidae Hartmann-Schröder, 1971. Unlike opheliids, which generally have elongate, sleek bodies with lateral and ventral grooves and that are often capable of rapid burrowing, species of Travisia have relatively short bodies that are thick and grublike and have a papillated integument that bears some superficial similarity to the areolated cuticle of Scalibregmatidae, a family with which travisiids are sometimes compared. Travisiids and scalibregmatids seem to be sister families according the most recent molecular results (Paul et al. 2010, Law et al. 2013a). However, although superficially similar in appearance, species of the two families differ significantly when details of soft morphology and chaetae are considered. This chapter on Opheliidae therefore includes only those opheliid genera and species that are included within the subfamilies Opheliinae (Ophelia Savigny in Lamarck, 1818 and Thoracophelia Ehlers, 1897) and Ophelininae (Armandia Filippi, 1861, Ophelina Örsted, 1843, and Polyophthalmus Quatrefages, 1850).

Morphology A general account of opheliid morphology was provided by Blake (2000). Opheliids range in length from a few

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millimeters to more than 100 mm. The number of body segments ranges from 30 to 60; with some species having a fixed number of body segments. The body is cylindrical in cross-section and similar in appearance throughout. Body regions may be absent as in Ophelina, weakly defined by a swollen anterior end and tapering posterior end as in Ophelia, or organized into three regions with a prominent anterior constriction as in Thoracophelia. The cuticle is generally smooth in appearance and intersegmental constrictions or grooves are poorly developed. The body may be expanded anteriorly and narrow posteriorly with a deep midventral groove as in Ophelia, or uniformly slender throughout, with midventral and lateral grooves along the body as in Ophelina, Armandia, and Polyophthalmus; the ventral groove is formed between two ridges of longitudinal ventral muscles. Lateral grooves, within which the parapodia and branchiae are protected, sometimes form above these ridges. The prostomium is a tapered cone, often pointed, sometimes with a terminal palpode, but never with lateral antennae; nuchal organs are ciliated pits often eversible; subdermal eyes are present or absent. The mouth is a transverse slit. The proboscis is an eversible axial structure that is used for feeding; it is ciliated and nonmuscular (Tzetlin and Zhadan 2009). The peristomium is reduced to lips surrounding the mouth. The parapodia are biramous and bear small, inconspicuous tori bearing thin fascicles of simple capillary chaetae. Dorsal cirri are absent; ventral cirri are present or absent. Branchiae are present or absent; when present, they are inserted dorsal and just posterior to the notopodia. Branchiae may occur throughout the body or may be confined to middle segments as in Ophelia; they are sometimes branched or pectinate as in Thoracophelia, but are never dendritically branched. Lateral segmental eyespots are present in Armandia and Polyophthalmus; interramal sensory pits and interramal papillae are reported for Ophelina and Ophelia. The posteriormost segments may be achaetous, narrow, and retractile. The pygidium contains a terminal anus and is often prolonged into a tubular funnel-like structure that may bear two stout ventral lobes and a circle of lateral papillae as in Ophelia, or a ring of papillae and long, internal cirri as in Ophelina. The first detailed account of opheliid anatomy was by Brown (1938) for Ophelia rathkei (as O. cluthensis). McConnaughey and Fox (1949) provided data on the internal anatomy of Thoracophelia mucronata. Hartmann-Schröder (1958) provided a comprehensive review of the structure of the integument, musculature, chaetal origins, nervous system, sensory organs, digestive system, circulatory system, nephridia, and reproductive organs for most of the opheliid genera. Detailed works on the ultrastructure of

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opheliids include Hermans and Cloney (1966) on the prostomial eyes of Armandia; Hermans (1969) on the segmental eyes of Armandia; Hermans (1970) on collagen fibrils; West (1978) on the nuchal organs of Ophelia; Harris (1991) on the rectal organs of Ophelia; Bartolomaeus (1993) on the eyes of juveniles; Purschke et al. (1995) on the segmental eyes of Polyophthalmus; and Belova and Zhadan (2014) on the respiratory system. Details of the proboscis morphology of opheliids were provided by Tzetlin and Zhadan (2009). The proboscis of these polychaetes is a large eversible glandular sac that may have several lobes or folds. In the genera Ophelia and Thoracophelia (subfamily Opheliinae), the proboscis is bubble-like, symmetrical, and ciliated (Tzetlin and Zhadan 2009). In contrast, the proboscis of species of Armandia, Ophelina, and Polyophthalmus (subfamily Ophelininae) is dorsoventrally asymmetrical and lobate with at least one species, Armandia maculata, reported to have separate oral tentacles rather than a single tonguelike structure. There is some variability in the morphology of the intestine. Penry and Jumars (1990) found that two species of Armandia had tubular guts, whereas Ophelina acuminata had three separate compartments in the gut; in addition, a dorsoventral partition divides the midgut into left and right halves (Jumars et al. 2015). Harris (1991) described a ciliated rectal organ in Ophelia bicornis that served to increase the rate of defecation of spent sand from the gut. The anatomy of T. mucronata provided by McConnaughey and Fox (1949) reflects the life history of this species, which occurs in dense populations on tidal sand flats in southern California. For example, the authors determined that internal septa were limited to between setigers 2 to 3 and 3 to 4, with the first being more muscular than the second. The two septa extend back over the esophagus forming a large sac they called the “injector organ”. This sac alternately fills with coelomic fluid causing the anterior body of the worm to swell into a bulbous shape and then to shrink back when the sac empties. The lack of septa was postulated as allowing coelomic fluid to flow freely with each movement of the worm and, together with the function of the sac, facilitating movements associated with burrowing and feeding. McConnaughey and Fox (1949) determined that the circulatory system of T. mucronata is closed, with the blood consisting of extracellular hemoglobin (Fox et al. 1948). Groups of cells termed blood cells have been reported from the branchiae of T. arcticus and Ophelia limacina and Ophelina acuminata by Belova and Zhadan (2014) but their function is unknown. Recent photographs of T. mucronata and two related species published by Law et al. (2013b) show the branchiae filled with bright red

blood. McConnaughey and Fox (1949) further described how the blood is distributed to the branchiae and other parts of the body. The excretory system of T. mucronata was determined to be protonephridial with rosettes of solenocytes projecting into the coelom and located mainly on branchiae-­ bearing segments (McConnaughey and Fox 1949). These observations differed from those of Brown (1938) on O.  rathkei (as O. cluthensis), in which nephridia were limited to segments 13 to 15 and consisted of a nephridial canal with an open nephrostome. Thoracophelia mucronata is a deposit feeder that ingests and turns over large amounts sediment as part of its feeding behavior (see next section for details). The digestive system consists of a foregut, stomach, and intestine (McConnaughey and Fox 1949). The foregut consists of the mouth, pharynx, and esophagus; the stomach is the largest part in circumference and is infolded ventrally to form a large typhlosole; the intestine is a relatively simple, thin-walled tube surrounded by a dorsal blood sinus. The pharynx is eversible and bears three ciliated lobes that gather sand and carry it into the digestive system. Studies on the ultrastructure of sensory organs in opheliids have focused on eyes and nuchal organs. Species of Armandia have both prostomial and segmental eyes. Prostomial eyes of Armandia brevis were investigated by Hermans and Cloney (1966) and segmental eyes by Hermans (1969); Purschke et al. (1995) examined the segmental eyes of Polyophthalmus qingdaoensis and Polyophthalmus pictus. A. brevis has 11 pairs of lateral ocelli or pigmented eye cups arranged segmentally from segments 7 to 17 (Hermans 1969), whereas P. qingdaoensis has 12 pairs from segments 7 to 18 (Purschke et al. 1995). For the prostomial eyes, Hermans (1969) determined that there are three prostomial ocelli imbedded in the tissue of the brain; each is composed of two cells. The pigment cell surrounds a photoreceptor and forms a pigmented cup and a transparent unpigmented diaphragm. In contrast, the segmental eyes (ocelli) of each segment consist of a single photoreceptor cell with approximately 15 sensory processes. The photoreceptor is enclosed within a pigment cup consisting of approximately 30 cuboidal cells filled with brown pigment. According to Purschke et al. (1995), the basic structure of the segmental eyes is similar in both A. brevis and P. qingdaoensis. The cellular ultrastructure of opheliid nuchal organs, including details of the sensory cells, supporting cells, and protective structures was investigated by Purschke (1997) as part of a larger study of polychaete nuchal organs in general. Typically, nuchal organs in polychaetes and most opheliids are paired; however, Polyophthalmus species



7.6.1 Opheliidae Malmgren, 1867 

 287

Fig. 7.6.1.1: A, nuchal organs in Opheliidae: Ophelina bowitzi, anterior end, lateral view (A); details of nuchal organ (B); Ophelina helgolandica, anterior end, lateral view (C); details of nuchal organ (D); Ophelina basicirra, details of nuchal organ (E); Ophelina abranchiata, details of nuchal organ (F). All after Parapar et al. (2011). Abbreviation: nuO, nuchal organ. Scale bars: A, C, 1 mm; B, 90 µm; D, E, 100 µm; F, 10 µm.

and Armandia polyophthalma are reported to possess two pairs (Purschke et al. 1995). Recent taxonomic studies of opheliids using SEM revealed considerable superficial variability in the nuchal organs of several species of Ophelina (Fig. 7.6.1.1). The size and external appearance of nuchal organs may prove useful in further distinguishing among species (Parapar et al. 2011). Electron microscopy also revealed details of the lateral organs. Purschke and Hausen (2007) provided observations on the ultrastructure of lateral organs, also called interparapodial ciliated sensory pits in O. rathkei and P.  pictus. In O. rathkei, the lateral organs occur between the noto- and neuropodia; these are small and located in pits containing three rows of cilia. In anterior and middle segments, the cilia are short and few in number, whereas in posterior segments, the cilia are more numerous and longer. Lateral organs are also small in P. pictus and are located in shallow pits. Parapar et al. (2011) described the lateral organs of several species of Ophelina and, for the first time, demonstrated the use of these organs as taxonomic characters. For example, Ophelina basicirra has ciliated pits arranged in a transverse row (Fig. 7.6.1.2 A),

whereas Ophelina abranchiata has pits that are grouped in an oval mound (Fig. 7.6.1.2 B) (Parapar et al. 2011). The same authors also reported details of ventral transverse ciliated bands in the ventral groove of O. basicirra (Fig.  7.6.1.2  C,  D), but the role of these cilia is as yet unknown. The morphology and ultrastructure of the branchiae (gills) and respiratory system of opheliids was recently described by Belova and Zhadan (2014). These authors interpret the branchiae of these taxa as protrusions from the body wall that connect to the coelom and contain blood vessels that are connected to interepithelial blood sinuses. Because the thickness of the cuticle of branchiae in opheliids is only 1.5 to 3.0 µm thick, this arrangement allows effective gas exchange. Among the species of Ophelia, Ophelina, and Thoracophelia (as Euzonus) studied were several important differences in branchial morphology with Travisia, which supports removing this genus from the Opheliidae: (1) branchiae of the opheliids bear cilia, which are absent in Travisia; (2) the cuticle of opheliid branchiae is thin, whereas in Travisia the branchiae are covered with a protocuticle similar to that

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 7.6 Opheliida/Capitellida

Fig. 7.6.1.2: Sensory organs in Opheliidae: Ophelina basicirra, lateral organ (A); Ophelina abranchiata, lateral organ (B); O. basicirra, posterior end, ventral view with ventral groove and transverse ciliary bands (C); same, details of ciliary bands (D). All after Parapar et al. (2011). Scale bars: A, B, 5 µm; C, 200 µm; D, 50 µm.

found in polychaete larvae; (3) the branchial epithelium of the opheliids has multiple gland cells, whereas Travisia has none; (4) epidermal cells are connected by dense junctions and/or adhesive belts in the opheliids, whereas in Travisia they are connected by desmosomes; and (5) blood cells are present in the branchiae of opheliids whereas they are absent in Travisia. Law et al. (2013a) published an account of opheliid musculature in relation to burrowing using the opheliids A. brevis and T. mucronata, which have different burrowing behaviors. Armandia exhibits undulatory burrowing; it has prominent bilateral longitudinal muscle bands and oblique muscles that, along with the longitudinal muscles, serve to bend the body during undulation. In contrast, Thoracophelia burrows by peristalsis using circular muscles that branch away from the body wall and form oblique muscles. Helical fibers in the cuticle facilitate radial expansion during peristalsis.

Biology and ecology A summary of the biology of opheliids was provided by Blake (2000). Opheliids are burrowers, capable of rapid movement downward into sand or mud using peristaltic or undulatory movement (Law et al. 2013a). Some species have streamlined bodies and a pointed prostomium that facilitates burrowing. Some species leave the sediment

and swim through the water by retrograde sinusoidal movements typical of smooth-bodied animals (Clark and Hermans 1976). The lateral grooves present in many species provide an avenue for respiratory currents that are generated by the branchiae. Opheliids are deposit feeders that engulf sediment with a saclike proboscis. The rectal organ of Ophelia bicornis described by Harris (1991) was believed to increase the rate of defecation of spent sand from the gut. He suggested that the rectal organ was an adaptation that facilitated the movement of large amounts of nutrient-poor sand through the gut. Fauchald and Jumars (1979) noted that opheliids are considered to be nonselective deposit feeders that ingest sediment for its associated organic matter; however, an updated assessment by Jumars et al. (2015) suggests that some species do exhibit selectivity for different kinds of mineral grains. Furthermore, Jumars et al. (2015) reported that some opheliids studied from various habitats exhibit high stable nitrogen (δ15N) values, suggesting selectivity. Guerin (1971) found that Polyophthalmus pictus ingests dead copepods and organic debris, again suggesting some selectivity. Similarly, McConnaughey and Fox (1949) found that Thoracophelia mucronata feeds on organic matter on the sand grains it ingests, including bacteria, protozoans, and other small organisms. These authors found that at high tide, the worms burrowed down to a depth of 30 cm, but with exposure of the sand at low tide, they came up



to within 2.5 to 5 cm of the surface or the depth where the sand was saturated by water (McConnaughey and Fox 1949). At this depth, they become prey to a variety of longbilled shore birds. The surface of the sand where these worms reside exhibits thousands of minute pits denoting the location of their burrows. McConnaughey and Fox (1949) also calculated sediment turnover rates of approximately 84 g of sand per worm per year on tidal flats. In a later study of T. mucronata (as Euzonus) feeding, Kemp (1986, 1988) determined that detrital carbon degraded by bacteria was directly taken up by the worms from sand grains as well as refractory carbon from algae. Opheliids may at times be among the dominant taxa in benthic communities. As part of the long-term monitoring of a deep-sea–dredged material disposal site offshore San Francisco, California, Ophelina abranchiata was 30th in overall abundance out of more than 800 species of benthic invertebrates collected over 10 years of monitoring in water depths of 2200 to 3200 m. Another undescribed species, Ophelina sp. 1 was locally abundant in sediments within or on the boundary of the disposal site, suggesting that it might be opportunistic in sediments that receive dredged material (Blake et al. 2009). Hermans (1969) described phototactic behavior of Armandia brevis in the laboratory. Atokous worms were found to respond negatively to light. When suddenly exposed to light, worms that were against the aquarium glass responded by retreating into the sediment. Hermans (1969) believed this response was due to light perception by the segmental eyes. Epitokous specimens, on the other hand, swarm in the plankton and are attracted to light. Literature on the reproduction and larval development of opheliids is extensive. Opheliids are known to have a full range of life history patterns including species with long-lived planktotrophic larvae with wide dispersal patterns and species with lecithotrophic larvae with short planktic lives and limited distributions. Direct development has been reported only for species of Travisia, now here removed from the Opheliidae to a separate family. A typical opheliid species with a life history representing planktotrophic development is Armandia brevis described by Hermans (1978). Sexually mature specimens swim to the surface and spawn at night during summer months. These epitokes shed their gametes, sink to the bottom, and die. Upon fertilization, the eggs are approximately 50 µm in diameter. Swimming blastulae develop after 12 h and planktotrophic trochophores within 48 h. Trochophores of A. brevis have a classic appearance with a well-developed apical tuft, prototroch, neurotroch, stomodeum, stomach, and intestine (Hermans 1978). During subsequent development, segments are added sequentially one at a time from the pygidial growth zone. Hermans

7.6.1 Opheliidae Malmgren, 1867 

 289

(1978) described a linear relationship between the number of segments and body length. A metatrochal ciliary band is added posterior to the prototroch. With development, the prototroch forms the upper lip of the mouth and the metatroch forms the lower lip. Late-stage nectochaetes are elongate, slender larvae. Larvae are competent to settle by the time 20 segments have developed and they do so without any apparent substrate specificity. The larvae that Hermans (1978) cultured achieved this stage of development in 3 to 4 weeks. After settlement, the juveniles develop rapidly and after 6 weeks are capable of becoming sexually mature and producing additional gametes. Hermans (1978) suggested that Armandia brevis could produce as many as six generations during a single reproductive season and therefore has a polytelic life history. Miner et al. (1999) used planktic larvae of Armandia brevis to assess evolutionary implications of opposed ciliary bands in invertebrate larval forms. The species was found to have more than one method of feeding. Two opposing bands of cilia, the prototroch and metatroch, serve as an efficient food gathering device. However, latestage larvae of A. brevis are also able to ingest large particles directly. The larval development of a related species, Armandia cirrhosa, was described by Guérin (1972) from the Mediterranean coast of France. Unlike A. brevis, A. cirrhosa develops only five setigers before metamorphosis and has only a brief planktic period before settlement. A similar pattern was described by Guérin (1971) for Polyophthalmus pictus. The development of Thoracophelia species represents another planktotrophic pattern, in which the development in the plankton is of short duration and in which the larvae develop only a few setigers before settlement. The larval development of T. mucronata from southern California sandy beaches was described by Dales (1952). Parke (1973) described the development of Thoracophelia williamsi, T. dillonensis, and T. mucronata (as Euzonus) from Dillon Beach in northern California. Ripe gametes for fertilization were obtained by slitting open the adults and mixing eggs and sperm. Eggs are generally small, 85 to 90 µm when mature. Dales (1952) believed that natural spawning took place in or on the surface of the sand. Development is rapid in the species of Thoracophelia described by these authors. Parke’s (1973) tabulation of the developmental rate for T. williamsi at 15°C included pretrochophores developing in 24 to 36 h, full trochophores in 36 to 48 h, two-chaetiger larvae in 6 to 10 days, and three-chaetiger larvae in 9 to 14 days. No further chaetigers were developed until after settlement in 12 to 20 days. The life cycle of Ophelia bicornis in England was described by Wilson (1948a) and represents a species

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 7.6 Opheliida/Capitellida

having lecithotrophic development and a short planktic larval life (Fig. 7.6.1.3). Unfertilized eggs are flattened discs measuring approximately 150 × 130 µm. After fertilization, the eggs round up and measure 95 µm in diameter. Wilson was able to strip gametes from sexually mature worms and successfully reared the larvae from laboratory fertilizations. Early trochophores developed after 24 h and three-chaetiger swimming larvae after 6 to 8 days. Unlike Armandia brevis, the larvae of O. bicornis never develop more than three chaetigers until after metamorphosis, but they do have a sediment preference, which can delay their metamorphosis. The lecithotrophic trochophores of O. bicornis have a well-developed prototroch, but the neurotroch, apical tuft, and telotroch are not as prominent as in their planktotrophic congeners. This is likely due to the short time these larvae spend in the plankton and the fact that they live on intrinsic yolk reserves until settlement. Riser (1987) described the development of Ophelia verrilli, a New England species that develops similarly to O. bicornis.

Wilson (1948b, 1952, 1953a,b, 1954, 1955) followed his article on Ophelia bicornis larval development with a classic series of experiments intended to determine the factors that promote settlement and metamorphosis of larvae. These studies led to the establishment of an entire field of study to assess attractive factors in larval settlement. Wilson’s initial experiments suggested that particle size and shape were important factors; his later studies demonstrated that bacterial films on the particles were the actual attractive factor. Hartmann-Schröder (1956) described the morphology of late-stage larvae and newly settled juveniles of several species of Ophelia and Armandia. Field studies of opheliid recruitment and population ecology, however, are few. Tamaki (1985a) worked with Armandia sp. recruitment on an intertidal flat in Japan and found that the larvae settled into two distinct zones on the tidal flats. Subsequently, after growth, the juveniles migrated in a seaward direction to establish the final population. He also found that

Fig. 7.6.1.3: Larval development of Ophelia bicornis: A, unfertilized egg; B, same, in side view; C, fertilized egg; D, trochophore, 1 day; E, trochophore, 2 days; F, trochophore, 3 days; G, 4-day-old larva, side view; H, I, 4- to 5-day-old larva, ventral and side views; J, 5-dayold two-chaetiger larva, dorsal view; K, L, 7-day-old two-chaetiger nectochaetes, ventral and side views; M, 11-day-old, three-chaetiger nectochaete, ventral view; N, 10-day-old, four-chaetiger postlarval juvenile; O, winged chaeta. All after Wilson (1948a).



populations of other polychaetes tended to inhibit Armandia settlement (Tamaki 1985b). Parke (1973) studied the morphology, reproduction, larval development, and general ecology of three sympatric species of Thoracophelia at Dillon Beach, California, based on field and laboratory experiments. He found that the species with the greatest degree of pinnule development on the branchiae and with the largest respiratory surface, T. dillonensis, occurred highest in the intertidal zone where exposure and oxygen stress was greatest. Likewise, T. mucronata, with no pinnule development, occurred lower in the intertidal where there was less exposure and oxygen stress at low tide. T. williamsi was observed to be intermediate both in branchial morphology and position in the intertidal and exhibited the most variability in pinnule development. Cross-breeding experiments by Parke (1973) revealed that each species × species combination resulted in successful hybridization, albeit with a low degree of compatibility for some crosses. In most crosses, larvae were successfully reared to the settlement stage. The development of pinnules on the branchiae is therefore a species-level adaptation to habitat and important only as a species-level character and cannot be used to support subgenera as had been proposed earlier by Hartman (1938). The validity of these three species was validated with molecular analysis by Law et al. (2013b).

Phylogeny and taxonomy Taxonomic history Opheliids have been known since the early 19th century when Ophelia bicornis was first described from the Mediterranean by Savigny (1822). The family was first recognized by Grube (1850) and named by Malmgren (1867). Støp-Bowitz (1945, 1948) described all of the opheliids found in Norwegian and Arctic waters and included complete synonymies; he also established the priority of Ophelina over Ammotrypane. Tebble (1952, 1953) provided an important review of the genus Ophelia and established a segmental and branchial formula for distinguishing among species and species groups. Bellan and his colleagues in France contributed to the systematics of Ophelia by describing new species (Bellan and Picard 1965, Bellan 1975) and developing a phylogeny (Bellan-Santini et al. 1992). Riser (1987) described a new species of Ophelia from New England and reviewed species from the western North Atlantic. Important faunal accounts of opheliids include Fauvel (1925, 1927: France), Day (1967: South Africa), Hartmann-Schröder (1971, 1996: Northern Europe), and

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Hartman (1969: California). The opheliids of the eastern Pacific and California are well known through a series of articles by Moore (1906a,b, 1923), Hartman (1938, 1969), McConnaughey and Fox (1949), Berkeley and Berkeley (1952), Hobson (1976), and Blake (2000). Recently, numerous additional species have been described from deep-water in the North Atlantic by Parapar et al. (2011) and Kongsrud et al. (2011); the South Atlantic by Elías and Bremec (2003) and Elías et al. (2003), and the Southern Ocean and Antarctica by Maciolek and Blake (2006) and Schüller (2008). Phylogeny Morphological studies. Hartmann-Schröder (1971) established three subfamilies for the Opheliidae: Opheliinae (Ophelia and Euzonus), Ophelininae (Armandia, Ophelina, Polyophthalmus), and Travisiinae (Travisia). This arrangement was supported as part of the first cladistic analyses to be performed on the Opheliidae together with intrageneric phylogenetic and taxonomic summaries of Ophelia and Travisia (Bellan et al. 1990, Bellan and Dauvin 1991, Bellan-Santini et al. 1992, Dauvin and Bellan 1994). Dauvin and Bellan (1994) also reduced the Travisiinae to a single genus with the synonymy of Dindymenides and Kesun with Travisia. A more extensive cladistic analysis using morphological characters was performed by Sene Silva (2007), who found that, among the three subfamilies, only the Travisiinae was monophyletic. Although these subfamilies were found by Bellan et al. (1990) to correspond to clades in their phylogenetic analysis and Travisia was determined to be plesiomorphic, these authors used a hypothetical ancestor as an outgroup rather than an actual taxon. The cladistic analysis of polychaetes by Rouse and Fauchald (1997) placed Opheliidae in a clade close to Capitellidae and Scalibregmatidae. The recent cladistic analysis by Sene-Silva (2007) confirms the results of Bellan et al. (1990) and supports a close relationship of Travisia to Scalibregmatidae. Several authors have postulated or suggested a close relationship between Travisia and the family Scalibregmatidae (Ashworth 1901, Blake 2000, Rouse and Pleijel 2001). However, apart from the grublike appearance of their bodies, there is little other morphological similarity between these two groups. The rough body of Travisia is due to papillae embedded into the cuticle, whereas, in scalibregmatids, the areolated body surface lacks papillae. Molecular studies. The earliest molecular analyses suggested a scalibregmatid origin for Travisia (Bleidorn et al. 2003, Hall et al. 2004). However, the 18S rDNA sequence in GenBank for Travisia forbesii used by these authors was discovered by one of the authors (C. Bleidorn, according to

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 7.6 Opheliida/Capitellida

Paul et al. 2010) in 2004 to actually belong to the scalibregmatid Polyphysia crassa. Persson and Pleijel (2005) used a new Travisia sequence with a species identified as T. brevis collected from Brittany, France. These authors found a scalibregmatid sister-group relationship for Travisia. However, T. brevis is an eastern Pacific species and the identity of their Travisia species needs to be confirmed. Another set of 18S rDNA sequence data for T. forbesii was used by Rousset et al. (2007), who found Travisia was grouped with opheliids. There are obvious problems with the earlier molecular sequence data developed for T. forbesii. If possible, voucher specimens need to be examined by an independent expert and correct species identifications applied to these sequences before any further use; otherwise, they should be deleted from GenBank. More recently, Paul et al. (2010) developed and used sequence data for T. brevis and T. pupa, both species collected from the Northeast Pacific coast of North America from four genes: 18S, 28S, 16S, and histone. These two species were used in an analysis with 26 other polychaetes including 12 opheliids, 7 scalibregmatids, and representatives of 7 other families. Results from parsimony, maximum likelihood, and Bayesian analyses were largely consistent and demonstrated that Opheliidae was monophyletic without Travisia with the two subfamilies Opheliinae and Ophelininae being sister groups to one another. Travisia and the scalibregmatids were sister groups to one another. The Opheliinae clade included two genera: Ophelina and Thoracophelia (as Euzonus and Lobochesis); and five species: O. bicornis, O. neglecta, O. rathkei, T. ezoensis, and T. bibranchia. Species within each of the two genera were in sister clades to one another. For the Ophelininae, three genera and six species were included: Ophelina (O.  acuminata and O. cylindricaudata), Polyophthalmus (P. pictus), and Armandia (A. cf. maculata, A. bilobata, and A. brevis). Further discussion on the phylogenetic relationship of Opheliidae, Travisia, and Scalibregmatidae are found in separate chapters of this handbook. Genera diagnoses Opheliidae Malmgren, 1867 Type genus: Ophelia Savigny in Lamarck 1818 Diagnosis: Body elongate, with smooth, sleek cuticle, typically with a defined number of segments; with ventral groove and with or without lateral elongate grooves; body of some species anteriorly inflated, posteriorly cylindrical and narrow; with or without distinct body regions. Prostomium elongate, conical, without appendages, often with terminal palpode. Parapodia biramous or uniramous, with small buttonlike parapodial lobes;

branchiae present or absent, when present simple, bifurcate, or rarely pectinate. Pygidium simple or with long anal tube. Chaetae all capillaries, usually smooth or weakly serrated. Remarks: This revised definition of the family is limited to taxa having elongate, relatively sleek bodies with or without distinct body regions; taxa with grublike bodies (genus Travisia) are removed to a separate family. The two subfamilies established by Hartmann-Schröder (1971) are retained. A synapomorphy for Opheliidae might be the presence of a ventral groove in all taxa (Sene Silva 2007). Opheliinae Hartmann-Schröder, 1971 Type genus: Ophelia Savigny in Lamarck 1818 Diagnosis: Body divided into two to three distinct regions; ventral grooves limited to posterior region; prostomial eyes present or absent; segmental eyes absent; branchiae single, paired, or with multiple branches, limited to posterior part of body; pygidium, short, with or without cirri. Remarks: These opheliids are readily distinguished by their distinct body regions instead of the elongate, sleek form of the Ophelininae. Two genera, Ophelia and Thoracophelia, currently with more than 50 species, comprise this subfamily. Ophelia Savigny in Lamarck, 1818 Type species: Ophelia bicornis Savigny in Lamarck, 1822, by monotypy Synonyms: Cassandane Kinberg, 1866. Type species: C. formosa Kinberg, 1866. Neomeris A. Costa, 1844. Type species: Neomeris urophylla Costa, 1844. Nitetis Kinberg, 1866. Type species: N. praetiosa Kinberg, 1866. Diagnosis: Body fusiform, divided externally into two regions: (1) cylindrical anterior region and (2) tapered posterior region bearing one deep ventral and two lateral grooves. Segments annulated. Prostomium small pointed cone. Cirriform branchiae present, rarely absent; branchiae normally with single filaments, rarely doubled; branchiae from setigers 8 to 14 to all but the last one to three terminal segments. Noto- and neuropodia with small fascicles of capillary chaetae; sometimes with pair of low rounded lobes. Sensory papilla (lateral organ) present between rami of each parapodium. Pygidium with stout ventral lobes and several dorsal papillae (Fig. 7.6.1.4). Remarks: The most important article on the systematics of Ophelia is by Tebble (1953), who established important characters, including certain branchial formulas, and provided keys to the then-known species. At present,



the genus includes 36 valid species, 14 of which were described subsequent to Tebble’s revisionary work. List of species, synonyms, and distributions (from the World Register of Marine Species (WoRMS), World Polychaeta Database, and recent publications); synonyms in brackets. 1. Ophelia africana Tebble, 1953. South Africa 2. Ophelia agulhana Day, 1961. South Africa 3. Ophelia algida Maciolek and Blake, 2006. Southern Ocean, near Macquarie Island 4. Ophelia amoureuxi Bellan and Costa, 1987. Mediterranean Sea 5. Ophelia anomala Day, 1961. South Africa 6. Ophelia ashworthi Fauvel, 1917. South Australia, Gulf of St Vincent and Spencer 7. Ophelia assimilis Tebble, 1953. California, intertidal and shallow subtidal 8. Ophelia bicornis Savigny in Lamarck, 1818. Widespread in the Northwest Atlantic, European waters; United Kingdom; Mediterranean; Northeast United States, Maine to Cape Cod 9. Ophelia bipartita Monro, 1936. Off Western Chile, 35 m 10. Ophelia borealis Quatrefages, 1866. Greenland; widespread in European waters

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 293

11. Ophelia bulbibranchiata Hartmann-Schröder and Parker, 1995. South Australia 12. Ophelia capensis Kirkegaard, 1959. South Africa 13. Ophelia celtica Amoureux and Dauvin, 1981. European waters 14. Ophelia dannevigi Benham, 1916. South Australia 15. Ophelia denticulata Verrill, 1875. Northwest Atlantic; Gulf of Mexico 16. Ophelia elongata Hutchings and Murray, 1984. Australia, New South Wales 17. Ophelia formosa (Kinberg, 1866). Argentina, La Plata 18. Ophelia glabra Stimpson, 1854. Northwest Atlantic, eastern Canada 19. Ophelia kirkegaardi Intes and Le Loeuff, 1977. West Africa 20. Ophelia koloana Gibbs, 1971. Central Pacific, Solomon Islands 21. Ophelia laubieri Bellan and Costa, 1987. European waters 22. Ophelia limacina (Rathke, 1843). Widespread in European waters; Canadian Arctic to Gulf of St. Lawrence a. [Ophelia eruciformis Johnston, 1865] b. [Ophelia taurica Bobretzky, 1881]

Fig. 7.6.1.4: Ophelia species: O. assimilis, anterior end, left lateral view (A); posterior end, right lateral view (B); O. pulchella, anterior end, left lateral view (C); posterior end, left lateral view (D); O. algida, posterior end, dorsal view (E); entire animal in left lateral view (F). A–C, after Hartman (1969); D, E, after Blake (2000); F, after Maciolek and Blake (2006).

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 7.6 Opheliida/Capitellida

23. Ophelia magna (Treadwell 1914). California 24. Ophelia multibranchia Hutchings and Murray, 1984. Australia, New South Wales 25. Ophelia neglecta Schneider, 1892. European waters 26. Ophelia peresi Bellan and Picard, 1965. East Africa, Madagascar 27. Ophelia praetiosa (Kinberg 1866). Patagonia, Cape Virgin 28. Ophelia profunda Hartman, 1965. Northwest Atlantic, off New England, deep water 29. Ophelia pulchella Tebble, 1953. California, shallow water 30. Ophelia radiata (Delle Chiaje 1828). Western Europe; Mediterranean a. [Ophelia coarctata Milne Edwards, 1849] b. [Ophelia contractata Milne Edwards in Quatrefages, 1866] c. [Ophelia neapolitana Quatrefages, 1866] 31. Ophelia rathkei McIntosh, 1908. European waters a. [Ophelia cluthensis McGuire, 1935] b. [Ophelia remanei Augener, 1939] 32. Ophelia roscoffensis Augener, 1910. European waters 33. Ophelia rullieri Bellan, 1975. Eastern Canada 34. Ophelia simplex Leidy, 1855. Northeast United States 35. Ophelia translucens (Katzmann 1973). European waters 36. Ophelia verrilli Riser, 1987. Eastern Canada to New England Thoracophelia Ehlers, 1897 Type species: Thoracophelia furcifera Ehlers, 1897 Synonyms: Euzonus Grube, 1866. Type species: E.  arcticus Grube, 1866 (Polychaeta: Opheliidae); junior homonym of Euzonus Menge, 1854 Type species: E. collulum Menge, 1854 (Arthropoda, Diplopoda), fide Brewer et al. 2011. Lobochesis Hutchings and Murray, 1984. Type species: L. bibrancha Hutchings and Murray, 1984. Pectinophelia Hartman, 1938. Type species: P. dillonensis Hartman, 1938. Diagnosis: Body elongate, divided into three distinct regions; cephalic region formed by the prostomium and one to two setigers; an anterior swollen region with up to eight segments separated from the narrow posterior region by the swollen and modified setiger 10; chaetiger 10 with lateral modification either as a flap arising from the body wall or with rows or patches of papillae; posterior body region with ventral groove. Prostomium small, conical; eyes present. Branchiae present, limited to posterior region, single, paired, or pectinate. Segmental eyes absent. Parapodia reduced, bearing fascicles of capillaries; chaetae of setigers 1 to 2 longer, more conspicuous than those on rest of body; ventral cirri absent. Pygidium with ventral plate and several long cirri (Fig. 7.6.1.5).

Remarks: Blake (2011) referred species of Euzonus to the genus Thoracophelia after Brewer et al. (2011) demonstrated that Euzonus was preoccupied in the ­Diplopoda. Readers are referred to Blake (2011) for a complete review of the taxonomic history of this group of opheliids. Blake (2011) also commented on the presence of three s­ ympatric California, species of Thoracophelia at Dillon Beach, ­ originally reported by Hartman (1938, 1944) and subsequently part of biological studies by Parke (1973). The validity of all three species was recently confirmed by Law et al. (2013b) as part of a molecular analysis. Species of Thoracophelia are unusual among the Opheliidae in having the body divided into three distinct regions: (1) an anterior cephalic region formed by the prostomium and the first two chaetigers; (2) a swollen thoracic region, usually through chaetigers 2 to 10; and (3) a long narrow posterior region with a distinct ventral groove; sometimes, the posterior pygidial region is enlarged or modified. Branchiae are limited to the posterior region, but are typically absent from the posteriormost segments. The three species at Dillon Beach have simple bifurcate branchiae (T. mucronata), bifurcated branchiae with pinnules (T. williamsi), and pectinate branchiae (T. dillonensis). Santos et al. (2004) also noted that all species of Thoracophelia have a lateral modification of setiger 10, either a flap arising from the body wall or rows or patches of papillae. List of species and distribution (after Blake 2011) 1. Thoracophelia arctica (Grube 1866). Arctic Ocean 2. Thoracophelia bibrancha (Hutchings and Murray 1984). Merimbula, New South Wales, Australia 3. Thoracophelia dillonensis (Hartman 1938). Dillon Beach, California 4. Thoracophelia ezoensis Okuda, 1934. Northern Japan 5. Thoracophelia flabellifera Zeigelmeier, 1955. North Sea 6. Thoracophelia furcifera Ehlers, 1897. Patagonia 7. Thoracophelia heterocirra (Rozbaczylo and Zamorano 1970). Eltabo, Chile 8. Thoracophelia japonica (Misaka and Sato 2003). Oura Bay, Shimoda, Izu Peninsula, Japan 9. Thoracophelia longiseta (Hutchings and Murray 1984). Ocean Beach, New South Wales, Australia 10. Thoracophelia mammallata (Santos et al. 2004). North and northeast Brazil, intertidal 11. Thoracophelia mucronata Treadwell, 1914. Southern California 12. Thoracophelia otagoensis (Probert, 1976). Otago Peninsula, New Zealand 13. Thoracophelia papillata (Santos et al. 2004). Southeast Brazil, shelf depths 14. Thoracophelia profunda (Hartman 1967). Off Cape Horn, South America, 4008 m



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 295

Fig. 7.6.1.5: Thoracophelia species: T. mucronata, entire animal, right lateral view (A); anterior end, dorsal view (B); branchia (C); T. williamsi, branchia (D); T. dillonensis, branchia (E); T. mucronata, posterior end (F); T. papillatus, entire animal, right lateral view, sand grains in gut visible (G); posterior end, left lateral view (H); chaetae from posterior chaetigers, showing subterminal knob (I); T. mammillatus, entire animal in right lateral view (J); lateral papillae and branchiae on chaetiger 10 (K); posterior end, dorsal view (L); posterior end, ventral view (M). A–F, after McConnaughey and Fox (1949); G‒M, after Santos et al. (2004).

15. Thoracophelia williamsi (Hartman 1938). Dillon Beach, California 16. Thoracophelia yasudai Okuda, 1936. Northern Japan. Referred to Euzonus arcticus by Annenkova (1935) and Imajima and Hartman (1964); treated as a distinct species by Uschakov (1955) and Hartman (1959) 17. Thoracophelia zeidleri (Hartmann-Schröder and Parker 1995). Haystack Beach, Reevesby Island, South Australia

Ophelininae Hartmann-Schröder, 1971 Diagnosis: Body elongate, sleek in appearance, not divided into distinct regions; ventral and lateral grooves continuous along body; prostomial eyes present or absent; segmental eyes present or absent; branchiae absent or present; if present, single without branches, occurring along entire body or limited to certain part of body; pygidium short or with long anal tube and cirri.

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 7.6 Opheliida/Capitellida

Remarks: Ophelininae currently include approximately 70 species in three genera: Armandia, Ophelina, and Polyophthalmus. Three obscure genera, Ammotrypanella, Tachytrypane, and Antiobactrum are here referred to synonymy with Ophelina. These genera are largely defined on the presence/absence or distribution of branchiae along the body, a character that, if used for other groups of species, would justify additional genera (see below for additional comments). Armandia Filippi, 1861 Type species: Armandia cirrhosa Filippi, 1861, by monotypy Diagnosis: Body elongate, not divided into distinct regions; with deep ventral groove and two lateral grooves along the entire length of the body; segments annulated. Prostomium conical, sometimes with terminal palpode; eyes present. Branchiae from setiger 2, continuing to posterior end; branchiae single, cirriform. Segmental lateral eyes present between parapodia from anterior setigers to posterior end. Noto- and neuropodia with small fascicles of capillaries; small ventral cirrus present. Pygidium with anal funnel surrounding anus bearing numerous short or long cirri (Fig. 7.6.1.6 B), or cirri absent, ventral papillae present or absent Remarks: To date, 25 species of Armandia are considered valid, known; however, most species are poorly known. A. brevis is common along the eastern Pacific in intertidal and shallow subtidal muddy sediments and has been the subject of several biological investigations. A. ­cirrhosa, a widespread European species, has also been well studied. List of species, synonyms, and distributions (from the WoRMS, World Polychaeta Database, and recent publications); synonyms in brackets. 1. Armandia agilis (Andrews 1891). Southeastern United States; Gulf of Mexico; Caribbean Sea 2. Armandia amakusaensis Saito, Tamaki and Imajima, 2000. Japan 3. Armandia andamana Eibye-Jacobsen, 2002. Thailand, Andaman Sea 4. Armandia bilobata Hartmann-Schröder, 1986. Australia, southern coast 5. Armandia bipapillata Hartmann-Schröder, 1974. Mozambique, east coast 6. Armandia brevis (Moore 1906). Alaska to Southern California, intertidal to shallow subtidal a. [Armandia bioculata Hartman, 1938] 7. Armandia broomensis Hartmann-Schröder, 1979. Australia, Broome, Western Australia

8. Armandia cirrhosa Filippi, 1861. Widespread in European waters a. [Armandia dollfusi Saint-Joseph, 1894] b. [Armandia flagellifera Southern, 1914] c. [Armandia oligops Marenzeller, 1874] 9. Armandia exigua Kükenthal, 1887. China 10. Armandia hossfeldi Hartmann-Schröder, 1956. Southwest Atlantic, Brazil to Argentina; shallow water 11. Armandia ilhabelae Hartmann-Schröder, 1956. Southwest Atlantic, Santos, Brazil 12. Armandia intermedia Fauvel, 1902. Senegal, West Africa (type locality); also reported from South Africa; Mauritania; Red Sea; Caribbean Sea, Trinidad and Tobago 13. Armandia lanceolata Willey, 1905. Indian Ocean, Mannar Island, India 14. Armandia leptocirris (Grube 1878). Indian Ocean, East Africa, Kenya to Mozambique; Red Sea; Philippines 15. Armandia loboi Elias and Bremec, 2003. Southwest Atlantic, Argentina 16. Armandia longicaudata (Caullery 1944). East Africa, Madagascar and Mozambique 17. Armandia maculata (Webster 1884). Bermuda (type locality); Gulf of Mexico; Caribbean Sea: Aruba, Bonaire, Curaçao; Trinidad and Tobago; Brazil 18. Armandia melanura Gravier, 1905. Red Sea 19. Armandia nonpapillata Jones, 1962. Caribbean Sea, Jamaica 20. Armandia polyophthalma Kükenthal, 1887. Widespread in European waters 21. Armandia salvadoriana Hartmann-Schröder, 1956. Eastern Pacific, El Salvador 22. Armandia secundariopapillata Hartmann-Schröder, 1984. Australia, southern coast 23. Armandia simodaensis Takahashi, 1938. Shimoda, Japan 24. Armandia sinaitica Amoureux, 1983. Red Sea, Sinai 25. Armandia weissenbornii Kükenthal, 1887. Red Sea, Perim Ophelina Örsted, 1843 Type species: Ophelina acuminata Örsted, 1843 Synonyms: Ammotrypane Rathke, 1843. Type species: Ammotrypane aulogaster Rathke, 1843 Ammotrypanella McIntosh, 1879. Type species: Ammotrypanella arctica McIntosh, 1879. Antiobactrum Chamberlin, 1919. Type species: Ophelina brasiliensis Hansen, 1882, new synonymy Ladice Kinberg, 1866. Type species: Ladice adamantea Kinberg, 1866.



7.6.1 Opheliidae Malmgren, 1867 

 297

Fig. 7.6.1.6: Ophelina and Armandia species. A. brevis, anterior end, right lateral view (A); posterior end, dorsal view (B); O. abranchiata, entire animal, right lateral view (C); O. acuminata, entire animal, right lateral view (D); posterior end, ventral view (E). A–C, after Blake (2000); D, after Støp-Bowitz (1945); E, after Berkeley and Berkeley (1952).

Omaria Grube, 1869. Type species: Omaria aulopygos Grube, 1869. Tachytrypane McIntosh, 1879. Type species: Tachytrypane jeffereysii McIntosh, 1879, new synonymy. Terpsichore Kinberg, 1866. Type species: Terpsichore delapidans Kinberg, 1866. Diagnosis: Body elongate, not divided into distinct regions; with deep ventral groove and two lateral grooves along entire length of body; segments annulated. ­Prostomium conical, sometimes with terminal palpode; prostomial eyes present or absent. Branchiae present or absent; when present, from chaetiger 2 continuing to posterior end, or sometimes absent from far posterior

chaetigers and rarely from anterior and or middle segments; branchiae single, cirriform. Segmental lateral eyes absent. Noto- and neuropodia with small fascicles of capillaries; small ventral cirrus present or absent. Pygidium with an anal funnel bearing long, unpaired ventral cirrus and sometimes additional lateral cirri. (Fig. 7.6.1.6 C–E). Remarks: Despite variability in branchial distribution, Ophelina is an easily recognizable genus within the Opheliidae. The recent effort by Schüller (2008) to resurrect Ammotrypanella from synonymy was largely based on the absence of branchiae from anterior and middle segments. However, if one were to consider this

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 7.6 Opheliida/Capitellida

as a generic-level character, then other branchial patterns would have to be considered as well. The presence of branchiae in only posterior segments should be considered a species-level character that is no more significant than the absence of branchiae in anterior, middle, or posterior segments, or their absence entirely. Schüller (2008) also described additional species of Ammotrypanella on the basis of the presence or absence of an anal tube or anal cirrus. However, the anal tube easily detaches from the body during sample processing and unless a large collection is available, this character is highly unreliable. Tachytrypane McIntosh, a monotypic genus that has a ventral groove along the entire body, an anal tube, and lacks branchiae, also falls into the definition of Ophelina. These characters also agree with O. abranchiata Støp-Bowitz, 1948 and O. nematoides (Ehlers 1900) and a separate genus is not warranted. As part of a morphological phylogenetic analysis by Sene Silva (2007), both Ammotrypanella and Tachytrypane were nested within clades containing species of Ophelina. Likewise, the genus Antiobactrum established by Chamberlin (1919) for O. brasiliensis Hansen, 1882 is well within the definition of the genus Ophelina as originally proposed by Hansen (1882). All three of these genera are thus referred to synonymy with Ophelina. List of species, synonyms, and distributions of Ophelina species (from the WoRMS, World Polychaeta Database, and recent publications); synonyms in brackets. 1. Ophelina abranchiata Støp-Bowitz, 1948. East Greenland (type locality); eastern and western North Atlantic; Eastern Pacific in shelf and slope depths a. [Ophelina farallonensis Blake, 2000]. Fide Sene Silva, 2007; Blake et al. 2009; Parapar et al. 2011 2. Ophelina acuminata Örsted, 1843. A widespread northern hemisphere Arctic-boreal species, shelf and slope depths 3. Ophelina adamantea (Kinberg 1866). Southeast Atlantic, Brazil 4. Ophelina alata Elias, Bremec, Lana and Orensanz, 2003. Southeast Brazil 5. Ophelina ammotrypanella Schüller, 2008. Antarctica, Weddell Sea, deep water 6. Ophelina arctica (McIntosh 1879). Davis Strait, Greenland deep water (type locality); western North Atlantic; Antarctica, Scotia Sea, Weddell Sea, abyssal depths; off New Zealand, abyssal depths 7. Ophelina aulogaster (Rathke 1843). Widespread in European waters; Northeast United States 8. Ophelina aulogastrella (Hartman and Fauchald 1971). Western North Atlantic, slope and abyssal depths

9. Ophelina basicirra Parapar, Moreira and Helgason, 2011. Off Iceland, shelf and upper slope depths, 20 to 2298 m 10. Ophelina bowitzi Parapar, Moreira and Helgason, 2011. Off Iceland in deep water, 1897 to 2709 m 11. Ophelina brattegardi Kongsrud and Bakken. Off East Greenland, 1600 m 12. Ophelina brasiliensis Hansen, 1882. Brazil 13. Ophelina breviata (Ehlers 1913). Widespread in Antarctic seas in shelf depths 14. Ophelina cirrosa (Schüller 2008). New combination. Antarctica, Weddell Sea, abyssal depths 15. Ophelina cylindricaudata (Hansen 1878). Arctic and subarctic records from Atlantic and Pacific; questionable Antarctic records 16. Ophelina delapidans (Kinberg 1866). Chile 17. Ophelina gaucha Elias, Bremec, Lana and Orensanz, 2003. Brazil to Patagonia 18. Ophelina groenlandica Stop-Bøwitz, 1948. East Greenland a. [Ammotrypane breviata sensu Pettibone, 1954]. Not Ehlers (1913) 19. Ophelina gymnopyge (Ehlers 1908). Off Argentina; Antarctic and sub-Antarctic locations 20. Ophelina hachaensis Augener, 1934. Colombia 21. Ophelina helgolandica Augener, 1912. Arctic, subarctic species; northern Europe; Iceland a. [Ophelina helgolandiae Augener, 1912] Variant spelling 22. Ophelina jeffreysi (McIntosh 1879), new combination. Davis Strait, deep-water. As Tachytrypane 23. Ophelina kinbergi Hansen, 1882. Brazil 24. Ophelina longicaudata Caullery, 1944. East Indies 25. Ophelina longicephala Hartmann-Schröder, 1977. Off Portugal, 72 m a. [Ophelina delapidans longicephala HartmannSchröder, 1977]. Originally as a subspecies 26. Ophelina longicirrata Hartmann-Schröder and Parker, 1995. South Australia 27. Ophelina margaleffi Sarda, Gil, Taboada and Gili, 2009. Northwest Mediterranean submarine canyons 28. Ophelina mcintoshi (Schüller 2008), new combination. South African Basin, abyssal depths (type locality); Southern Atlantic Ocean, abyssal depths 29. Ophelina minima Hartmann-Schröder, 1974. Northern Europe, Norway; Skagerrak a. [Ophelina cylindricaudata minima HartmannSchröder, 1974] originally as a subspecies 30. Ophelina modesta Støp-Bowitz, 1958. Norwegian waters

7.6.1 Opheliidae Malmgren, 1867 



31. Ophelina nematoides (Ehlers 1900). Antarctica, shelf and slope depths 32. Ophelina norvegica Støp-Bowitz, 1945. Eastern Norway, in fiords 33. Ophelina nybelini Eliason, 1951. Azores 34. Ophelina opisthobranchiata Wirén, 1901. Nordic seas, deep water 35. Ophelina princessa (Schüller 2008), new combination. Weddell Sea, abyssal depths. As Ammotrypanella 36. Ophelina robusta Schüller, 2008. Antarctica, Weddell Sea in deep water 37. Ophelina scaphigera (Ehlers 1900). Antarctica, shelf and slope depths 38. Ophelina setigera (Hartman 1978). Antarctica: Ross Sea; Weddell Sea; deep water 39. Ophelina syringopyge (Ehlers 1901). Off Argentina; Straits of Magellan; South Georgia; Antarctic Peninsula Polyophthalmus Quatrefages, 1850 Type species: Nais picta Dujardin, 1839 Diagnosis: Body elongate, not divided into distinct regions; ventral groove present along entire length of body; lateral grooves present; segmental annulations poorly defined, body appearing nematode-like. Prostomium short, conical, but usually rounded on anterior margin; eyes present, subdermal; nuchal organs well developed as paired ciliated projections or recessed into convex grooves. Branchiae absent. Segmental lateral eyes present. Noto- and neuropodia reduced closely spaced, with fascicles of capillaries; dorsal and ventral cirri absent. Pygidium with anal funnel and small papillae. Remarks: Out of 20 named species of Polyophthalmus, 17 have been referred to synonymy with P. pictus (see below), with this species having a wide distribution. However, comparative morphological and molecular studies have not been conducted and it is likely that cryptic species are present given the global distribution of these records. Two species, P. pictus (Dujardin 1839) and P. translucsens Hartman, 1960, are recorded from California. The latter species is distinguished from the former by the absence of an anal funnel, a structure that is often lost or damaged with rough handling during collection and preservation (but see Hartman, 1969). Purschke et al. (1995) separated their P. qingdaoensis from China on the basis of consistent size and ultrastructural differences between the segmental eyes of the Chinese specimens and those of P.  pictus from Italy. The authors noted that the two species were otherwise identical. Purschke et al. (1995) noted that P. striatus previously described by Kükenthal (1887) from

 299

Hong Kong, China and currently considered a synonym of P. pictus differed from the new species in several details. P. striatus was considered valid by Hartman (1959), but is currently listed as a synonym of P. pictus in WoRMS. List of species, synonyms, and distribution (from the WoRMS, World Polychaeta Database, and recent publications); synonyms in brackets. 1. Polyophthalmus pictus (Dujardin, 1839). France a. [Armandia robertianae McIntosh, 1908]. Great Britain b. [Polyophthalmus agilis Quatrefages, 1850]. Bay of Biscay c. [Polyophthalmus australis Grube, 1869]. Cape York, Australia d. [Polyophthalmus ceylonensis Kükenthal, 1887]. Sri Lanka e. [Polyophthalmus collaris Michaelsen, 1892]. Sri Lanka f. [Polyophthalmus dubius Quatrefages, 1850]. France g. [Polyophthalmus ehrenbergi Quatrefages, 1850]. Sicily h. [Polyophthalmus floridanus Augener, 1922]. Tortugas, Florida i. [Polyophthalmus incertus Treadwell, 1936]. Bermuda j. [Polyophthalmus longisetosus Michaelsen, 1892]. Sri Lanka k. [Polyophthalmus pallidus Claparède, 1869]. Italy l. [Polyophthalmus papillatus Treadwell, 1943]. Lobito, Angola, West Africa m. [Polyophthalmus pictus pontica Czerniavsky, 1881]. Sevastopol, Black Sea n. [Polyophthalmus striatus Kükenthal, 1887]. China 2. Polyophthalmus qingdaoensis Purschke, Ding and Müller, 1995. China 3. Polyophthalmus translucens Hartman, 1960. California References Annenkova, N.P. (1935): Über Dysponetus pygmaeus Levinsen und Euzonus arcticus Grube. Compte Rendus Exploration Mers U.R.S.S. 8(23): 233–236. Ashworth, J.H. (1901): The anatomy of Scalibregma inflatum Rathke. Quarterly Journal of Microscopical Science 45: 237–309, plates 13–15. Bartolomaeus, T. (1993): Different photoreceptors in juvenile Ophelia rathkei (Annelida, Opheliidae). Microfauna Marina 8: 99–114. Bellan, G. (1975): Ophelia rullieri n.sp., Opheliidae (Annélide Polychète sédentaire) des côtes gaspésiennes (Canada). Bulletin de la Société Zoologique de France 100: 421–425. Bellan, G., Bellan-Santini, D. & Dauvin, J.C. (1990): Phénétique et phylogénie des Opheliidae (Annélides Polychètes). Compte

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Rendus de l’Académie des Sciences, III Sciences de la Vie 310: 175–181. Bellan, G. & Dauvin, J.C. (1991): Phenetic and biogeographic relationships in Ophelia (Polychaeta, Opheliidae). Bulletin of Marine Science 48: 544–558. Bellan, G. & Picard, J. (1965): Contributions a l’étude des Polychètes de la région Tuléar (République Malagache). I. Ophelia peresi n.sp. Bulletin de la Société Zoologique de France 90: 295–298. Bellan-Santini, D., Dauvin, J.C. & Bellan, G. (1992): Approche phenetique et phylogenetique des Ophelia (Annélides Polychètes) de Mediterranee occidentale. Bulletin de l’Institute Oceanographique Monaco special number 9: 67–81. Belova, P.A. & Zhadan, A.E. (2014): Comparative morphology and ultrastructure of the respiratory system in four species of the Opheliidae family. Biology Bulletin 41: 752–772. Berkeley, E. & Berkeley, C. (1952): Annelida. Polychaeta Sedentaria. Canadian Pacific Fauna No. 9b: 1–139. Blake, J.A. (2000): Chapter 7. Family Opheliidae Malmgren, 1867. In: Blake, J.A., Hilbig, B. & Scott, P.V. (eds.). Taxonomic Atlas of the Santa Maria Basin and Western Santa Barbara Channel. Vol. 7. Annelida Part 4. Polychaeta: Flabelligeridae to Sternaspidae. Santa Barbara Museum of Natural History, Santa Barbara: 145–168. Blake, J.A. (2011): Revalidation of the genus Thoracophelia Ehlers, 1897, replacing Euzonus Grube, 1866 (Polychaeta: Opheliidae), junior homonym of Euzonus Menge, 1854 (Arthropoda: Diplopoda), together with a literature summary and updated listing of Thoracophelia species. Zootaxa 2807: 65–68. Blake, J.A., Maciolek, N.J., Ota, A.Y. & Williams, I.P. (2009): Long-term benthic infaunal monitoring at a deep-ocean dredged material disposal site off Northern California. Deep-Sea Research II 56: 1775–1803. Bleidorn, C., Vogt, L. & Bartolomaeus, T. (2003): New insights into polychaete phylogeny (Annelida) inferred from 18S rDNA sequences. Molecular Phylogenetics and Evolution 29: 279–288. Brewer, M.S., Sierwald, P. & Bond, J.E. (2011): A generic homonym concerning chordeumatid millipedes (Arthropoda: Diplopoda) and ophellid [sic] worms (Annelida: Polycheata [sic]). Zootaxa 2744: 65–68. Brown, R.S. (1938): The anatomy of the polychaete Ophelia cluthensis McGuire 1935. Proceedings of the Royal Society of Edinburgh 58, Part II (10): 135–160. Chamberlin, R.V. (1919): The Annelida Polychaeta. Memoirs of the Museum of Comparative Zoology at Harvard College 48: 1–514. Clark, R.B. & Hermans, C.O. (1976): Kinetics of swimming in some smooth-bodied polychaetes. Journal of Zoology, London 178: 147–159. Dales, R.P. (1952): The larval development and ecology of Thoracophelia mucronata (Treadwell). Biological Bulletin 102: 232–252. Dauvin, J.C. & Bellan, G. (1994): Systematics, ecology and biogeographic relationships in the sub-family Travisiinae (Polychaeta, Opheliidae). Mémoires du Muséum National d’Histoire Naturelle 162:169–184. Day, J.H. (1967): A Monograph on the Polychaeta of Southern Africa. British Museum of Natural History, Publication No. 656: 1–878. Dujardin, F. (1839): Observations sur quelques Annélides marins. Annales des Sciences Naturelles, Paris ser. 2, 11: 287–294, 1 plate.

Ehlers, E. (1913): Die Polychaeten-Sammlungen der deutschen Südpolar-Expedition 1901–1903. Deutschen SüdpolarExpedition 13(4): 397–598, plates 26–46. Elías, R. & Bremec, C.S. (2003): First record of the genus Armandia (Opheliidae, Polychaeta) in Argentine waters, with the description of Armandia loboi sp. n. Bulletin of Marine Science 72: 181–186. Elías, R., Bremec, C.S., da Cunha Lana, P. & Orensanz, J.M. (2003): Opheliidae (Polychaeta) from the southwestern Atlantic Ocean, with description of Travisia amadoi n. sp., Ophelina gaucha n. sp., and Ophelina alata n. sp. Hydrobiologia 496: 75–85. Fauchald, K. & Jumars, P.A. (1979): The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology. An Annual Review 17:193–284. Fauvel, P. (1925): Sur les Ophéliens des côtes de France. Bulletin de la Société Zoologique de France 50: 77–88. Fauvel, P. (1927): Polychètes sédentaires. Addenda aux Errantes, Archiannélides, Myzostomaires. Faune de France 16: 1–494. Fox, D.L., Crane, S.C. & McConnaughey, B.H. (1948): A biochemical study of the marine annelid worm Thoracophelia mucronata, food, biochromes, and carotenoid metabolism. Journal of Marine Research 7: 567–585. Guérin, J-P. (1971): Modalités d’élevage et description des stades larvaires de Polyophthalmus pictus Dujardin (Annélide Polychète). Vie et Milieu 22A: 143–152. Guérin, J-P. (1972): Le développement larvaire d’Armandia cirrhosa Filippi (Annélide Polychète). Tethys 4: 969–974. Grube, A.E. (1850): Die Familien der Anneliden. Archiv für Naturgeschichte 16: 249–364. Hall, K.A., Hutchings, P.A. & Colgan, D.J. (2004): Further phylogenetic studies of the Polychaeta using 18S rDNA sequence data. Journal of the Marine Biological Association of the United Kingdom 84: 949–960. Hansen, G.A. (1882): Annelida. Den Norske Norhavs-Expedition 1876–1878. Zoologi. Oslo 3: 1–54, 7 plates, map. Harris, T. (1991): The rectal organ of Ophelia bicornis Savigny (Polychaeta): a device for efficient defecation. Zoological Journal of the Linnaean Society 103: 197–206. Hartman, O. (1938): Descriptions of new species and new generic records of polychaetous annelids from California of the families Glyceridae, Eunicidae, Stauronereidae, and Opheliidae. University of California Publications in Zoology 43: 693–111. Hartman, O. (1944): Polychaetous annelids from California, including the descriptions of two new genera and nine new species. Allan Hancock Pacific Expeditions 10: 239–307, plates 19–26. Hartman, O. (1959): Catalogue of the polychaetous annelids of the world. Allan Hancock Foundation Publications Occasional Paper 23 (2): 355–628. Hartman, O. (1960): Systematic account of some marine invertebrate animals from the deep basins of Southern California. Allan Hancock Pacific Expeditions 22: 69–215, 19 plates. Hartman, O. (1969): Atlas of the Sedentariate Polychaetous Annelids from California. Allan Hancock Foundation, University of Southern California, Los Angeles: 1–812. Hartmann-Schröder, G. (1956): Polychaeten-Studien II. Zur Larvalentwicklung der Opheliiden (Polychaeta). Zoologischer Anzeiger 157: 92–101.



Hartmann-Schröder, G. (1958): Zur Morphologie der Opheliiden (Polychaeta Sedentaria). Zeitschrift für wissenschaftliche Zoologie 161: 84–143. Hartmann-Schröder, G. (1971): Annelida, Borstenwürmer, Polychaeta. Die Tierwelt Deutschlands 58:1–594. Hartmann-Schröder, G. (1996): Annelida, Borstenwürmer, Polychaeta. Second Edition. Die Tierwelt Deutschlands 58: 1–648. Hermans, C.O. (1969): Fine structure of the segmental ocelli of Armandia brevis (Polychaeta: Opheliidae). Zeitschrift für Zellforschung 96: 361–371. Hermans, C.O. (1970): The periodicity of collagen in the brain sheath of a polychaete. Journal of Ultrastructure Research 30: 255–261. Hermans, C.O. (1978): Metamorphosis in the opheliid polychaete Armandia brevis. In: Chia, F. & Rice, M.E. (eds.). Settlement and Metamorphosis of Marine Invertebrate Larvae. Elsevier, New York: 113–126. Hermans, C.O. & Cloney, R.A. (1966): Fine structure of the prostomial eyes of Armandia brevis (Polychaeta: Opheliidae). Zeitschrift für Zellforschung 72: 583–596. Hobson, K.D. (1976): Notes on benthic sedentariate Polychaeta (Annelida) from British Columbia and Washington. Syesis 9: 135–142. Jumars, P.A., Dorgan, K.M. & Lindsey, S.M. (2015): Diet of worms emended: an update of polychaete feeding guilds. Annual Review of Marine Science 7: 497–520 + Supplemental Appendix. Kemp, P.F. (1986): Direct uptake of detrital carbon by the deposit feeding polychaete Euzonus mucronata (Treadwell). Journal of Experimental Marine Biology and Ecology 99: 49–61. Kemp, P.F. (1988): Production and life history of a deposit feeding polychaete in an atypical environment. Estuarine & Coastal Shelf Science 26: 437–446. Kongsrud, J.A., Bakken, T. & Oug, E. (2011): Deep-water species of the genus Ophelina (Annelida, Opheliidae) in the Nordic Seas, with the description of Ophelina brattegardi sp. nov. Italian Journal of Zoology 78(S1): 95–111. Kükenthal, W. (1887): Die Opheliaceen der Expedition der Vettore Pisani. Jenaische Zeitschrift für Naturwissenschaft 21: 361–373, plate 21. Law, C.J., Dorgan, K.M. & Rouse, G.W. (2013a): Relating divergence in polychaete musculature to different burrowing behaviors: A study using Opheliidae. Journal of Morphology 275(5): 548–571. Law, C.J., Dorgan, K.M. & Rouse, G.W. (2013b): Validation of three sympatric Thoracophelia species (Annelida: Opheliidae) from Dillon Beach, California using mitochondrial and nuclear DNA sequence data. Zootaxa 3608: 67–74. McConnaughey, B.H. & Fox, D.L. (1949): The anatomy and biology of the marine polychaete Thoracophelia mucronata (Treadwell), Opheliidae. University of California Publications in Zoology 47: 319–340, plates. 26–30. Maciolek, N.J. & Blake, J.A. (2006): Opheliidae (Polychaeta) collected by the R/V Hero and the USNS Eltanin cruises from the Southern Ocean and South America. Scientia Marina 70S3: 101–113. Malmgren, A.J. (1867): Annulata Polychaeta Spetsbergiae, Groenlandiae, Islandiae et Scandinaviae hactenus cognita. Öfversight af Kungliga Vetenskaps-Akademiens Förhandlingar, Stockholm 24: 127–235. Miner, B.G., Sanford, E., Strathmann, R.R., Pernet, B. & Emlet, R.B. (1999): Functional and evolutionary implications of opposed

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bands, big mouths, and extensive oral ciliation in larval opheliids and echiurids (Annelida). Biological Bulletin 197: 14–25. Moore, J.P. (1906a): Additional new species of Polychaeta from the North Pacific. Proceedings of the Academy of Natural Sciences, Philadelphia 58: 217–260, plates 10–12. Moore, J.P. (1906b): Descriptions of two new Polychaeta from Alaska. Proceedings of the Academy of Natural Sciences, Philadelphia 58: 352–355. Moore, J.P. (1923): The polychaetous annelids dredged by the U.S.S. ‘Albatross’ off the coast of southern California in 1904. IV. Spionidae to Sabellariidae. Proceedings of the Academy of Natural Sciences, Philadelphia 75: 179–259, plates 17–18. Paul, C., Halanych, K.M., Tiedemann, R. & Bleidorn, C. (2010): Molecules reject an opheliid affinity for Travisia. Systematics and Biodiversity 8(4): 507–512. Parapar, J., Moreira, J. & Helgasson, G. (2011): Distribution and diversity of Opheliidae (Annelida, Polychaeta) on the continental shelf and slope of Iceland, with a review of the genus Ophelina in northeast Atlantic waters and description of two new species. Organisms, Diversity and Evolution 11: 83–105. Parke, S.R. (1973): Biological aspects of speciation in three sympatric Euzonus species at Dillon Beach, California (Polychaeta: Opheliidae). Master of Science Thesis, University of the Pacific: 1–69. Penry, D.L. & Jumars, P.A. (1990): Gut architecture, digestive constraints and feeding ecology of deposit-feeding and carnivorous polychaetes. Oecologia 82: 1–11. Persson, J. & Pleijel, F. (2005): On the phylogenetic relationships of Axiokebuita, Travisia and Scalibregmatidae. Zootaxa 998: 1–14. Pettibone, M.H. (1954): Marine polychaete worms from Point Barrow, Alaska, with additional records from the North Atlantic and North Pacific. Proceedings of the United States National Museum 103: 203–356. Purschke, G. (1997): Ultrastructure of nuchal organs in polychaetes (Annelida)—new results and review. Acta Zoologica 78(2): 123–143. Purschke, G., Ding, Z. & Müller, M.C. (1995): Ultrastructural differences as a taxonomic marker: the segmental ocelli of Polyophthalmus pictus and Polyophthalmus qingdaoensis sp.n. (Polychaeta, Opheliidae). Zoomorphology 115: 229–241. Purschke, G. & Hausen, H. (2007): Lateral organs in sedentary polychaetes (Annelida)—ultrastructure and phylogenetic significance of an insufficiently known sense organ. Acta Zoologica 88: 23–39. Riser, N.W. (1987): Observations on the genus Ophelia (Polychaeta: Opheliidae) with the description of a new species. Ophelia 28: 111–129. Rouse, G.W. & Fauchald, K. (1997): Cladistics and polychaetes. Zoologica Scripta 26: 139–204. Rouse, G.W. & Pleijel, F. (2001): Polychaetes. Oxford University, London: 1–354. Rousset, V., Pleijel, F., Rouse, G.W., Erséus, C. & Siddall, M. (2007): A molecular phylogeny of annelids. Cladistics 23: 41–63. Santos, C.S.G., Nonato, E.F. & Petersen, M.E. (2004): Two new species of Opheliidae (Annelida: Polychaeta): Euzonus papillatus sp. n. from northeastern Brazilian sandy beach and Euzonus mammillatus sp. n. from the continental shelf of south-eastern Brazil. Zootaxa 478: 1–12.

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Savigny, J-C. (1822): Système des annélides, principalement de celles des côtes de l’Égypte et de la Syrie, offrant les caractères tand distinctifs que naturels des Ordres, Familles et Genres, avec la Description des Espèces. Description de l’Egypte Historie Naturelle, Paris 1: 1–128. Schüller, M. (2008): New polychaete species collected during the expeditions ANDEEP I, II, and III to the deep Atlantic sector of the Southern Ocean in the austral summers 2002 and 2005— Ampharetidae, Opheliidae, and Scalibregmatidae. Zootaxa 1705: 51–68. Sene Silva, G. (2007): Filogenia de Opheliidae (Annelida: Polychaeta). Unpublished Thesis presented for the degree, Doctor of Sciences, in Zoology, Universidade Federal do Paraná, Curitiba: i–xii, + 1–95. (http://dspace.c3sl.ufpr.br/ dspace/handle/1884/12922) Støp-Bowitz, C. (1945): Les opheliens Norvegiens Meddelelser fra det Zoologiske Museum, Oslo. Meddelelser fra det Zoologiske Museum, Oslo 52: 21–61. Støp-Bowitz, C. (1948): Sur les polychètes arctiques des familles des Glycériens des Ophéliens, des Scalibregmiens et des Flabelligériens. Tromsø Museums Årshefter 66: 21–58. Tamaki, A. (1985a): Zonation by size in the Armandia sp. (Polychaeta: Opheliidae) population on an intertidal sand flat. Marine Ecology Progress Series 27: 123–133. Tamaki, A. (1985b): Inhibition of larval recruitment of Armandia sp. (Polychaeta: Opheliidae) by established adults of Pseudopolydora paucibranchiata (Okuda) (Polychaeta: Spionidae) on an intertidal sand flat. Journal of Experimental Marine Biology and Ecology 87: 167–182. Tebble, N. (1952): On three species of the genus Ophelia (Polychaeta) from British and adjacent waters. Annals & Magazine of Natural History, series 12 5: 553–571. Tebble, N. (1953): A review of the genus Ophelia (Polychaeta) with descriptions of new species from South African and Californian waters. Annals & Magazine of Natural History, series 12 6: 361–368. Tzetlin, A. & Zhadan, A. (2009): Morphological variation of axial non-muscular proboscis types in the Polychaeta. Zoosymposia 2: 415–427. Uschakov, P.V. (1955 [1965]): Polychaeta of the Far Eastern seas of the USSR. Akademiya Nauk SSSR, Opredeliteli po faune SSSR 56: i–xxvi + 1–445. [In Russian, translated 1965 by the Israel program for scientific translation, Jerusalem, 419 pp.] West, D.L. (1978): Comparative ultrastructure of juvenile and adult nuchal organs of an annelid (Polychaeta, Opheliidae). Tissue and Cell 10: 243–257. Wilson, D.P. (1948a): The larval development of Ophelia bicornis Savigny. Journal of the Marine Biological Association of the United Kingdom 27: 540–553. Wilson, D.P. (1948b): The relation of the substratum to the metamorphosis of Ophelia larvae. Journal of the Marine Biological Association of the United Kingdom 27: 723–760. Wilson, D.P. (1952): The influence of the nature of the substratum on the metamorphosis of the larvae of marine animals, especially the larvae of Ophelia bicornis Savigny. Annales de l’Institute Océanographique 27(2), 49–156. Wilson, D.P. (1953a): The settlement of Ophelia bicornis Savigny larvae. The 1951 experiments. Journal of the Marine Biological Association of the United Kingdom 31: 413–438.

Wilson, D.P. (1953b): The settlement of Ophelia bicornis Savigny larvae. The 1952 experiments. Journal of the Marine Biological Association of the United Kingdom 32: 209–233. Wilson, D.P. (1954): The attractive factor in the settlement of Ophelia bicornis Savigny. Journal of the Marine Biological Association of the United Kingdom 33: 361–380. Wilson, D.P. (1955): The role of micro-organisms in the settlement of Ophelia bicornis Savigny. Journal of the Marine Biological Association of the United Kingdom 34(3): 531–543.

James A. Blake and Nancy J. Maciolek

7.6.2 Travisiidae Hartmann-Schröder, 1971, new family status Introduction In 1971, Hartmann-Schröder established the subfamily Travisiinae to include the opheliid genera Dindymenides, Kesun, and Travisia. Later, Dauvin and Bellan (1994) synonymized Dindymenides and Kesun with Travisia, leaving a single genus in the subfamily. Unlike opheliids, which generally have elongate, sleek bodies with lateral and ventral grooves that are often capable of rapid burrowing, most species of Travisia have relatively short bodies that are thick and grublike with a papillated integument that bears a superficial similarity to that of the Scalibregmatidae. However, species of the two families differ significantly when details of soft morphology and chaetae are considered. Based on morphological comparisons and recent molecular phylogenetic results, it is evident that Travisia should be removed from the Opheliidae. However, Travisia does not belong in the Scalibregmatidae as is now accepted by several authors (Martinez et al. 2012, 2013, Law et al. 2013); at best, the two families seem to be sister groups. Rather than squeeze Travisia into the Scalibregmatidae and develop a very complex family-level definition, we prefer to treat these taxa as separate families. Therefore, we here reject the inclusion of Travisia in either Opheliidae or Scalibregmatidae and establish Hartmann-Schröder’s (1971) opheliid subfamily Travisiinae as a separate polychaete family.

Morphology External morphology Species of Travisia have relatively short bodies that are thick, fusiform, grublike, and taper at both ends (Fig. 7.6.2.1 A, B). The number of body segments is fixed in



7.6.2 Travisiidae Hartmann-Schröder, 1971, new family status 

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Fig. 7.6.2.1: A, Travisia chiloensis, entire animal in lateral view; B, Travisia palmeri, entire animal in lateral view with insets of a parapodium, posterior end showing anal cirri, and detail of pygidium; C, Travisia pupa, anterior end, dorsal view; D, same, ventral view; E, same, chaetigers 10 to 11 in lateral view; F, Travisia tincta, detail of pygidial lobes. A, after Kükenthal (1887); B, F, after Maciolek and Blake (2006); C–E, after Imajima (2009). Abbreviations: br, branchia; chaet, chaetiger; IntP, interramal papilla; mo, mouth; nuO, nuchal organ; per, peristomium; pr, prostomium.

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Fig. 7.6.2.2: A, Travisia forbesii. A, SEM of anterior end, ventral view; B, midventral view showing rows of papillae; C, epidermal papillae showing surficial pores; D, TEM thin section of epidermis showing morphology of epidermal papillae, basal peduncle circular muscles. All after Vodopyanov et al. (2014). Abbreviations: ep, epidermal papillae; cm, circular muscles; lo, lateral organ; lep, lower epidermal layer of cells; mo, mouth; npc, neurochaetae; ntc, notochaetae; ocu, outer cuticle; ped, peduncle of papillae; po, pores, pr, prostomium.

adults of some species but apparently variable in others (Dauvin and Bellan 1994, Maciolek and Blake 2006). The effect of development on the final number of segments in adults is not well understood and some variability may be size related. The body is cylindrical in cross-section, without prominent lateral or ventral grooves, or if present, grooves are very reduced and restricted in their extent. The integument is formed into extra external furrows or transverse ridges that encompass each body segment (Fig.  7.6.2.1  C,  D); body segments have one to three annulations. The nature of these transverse ridges has sometimes been compared with those of scalibregmatids. However, the nature of the rows and ridges is different in scalibregmatids in that those of scalibregmatids are more numerous and often again subdivided into areolations with padlike elevations that form distinct patterns in different parts of the body; sometimes having taxonomic importance (Blake 2015). In addition to the transverse ridges, the epidermis of Travisia is typically covered with numerous small papillae and sometimes larger pustules (Figs. 7.6.2.1 C–E and 7.6.2. A, B), especially in posterior segments; similar papillae are absent in scalibregmatids. The annulated nature of posterior segments typically becomes modified, forming folds with lappets (lobes), dorsal and ventral to the parapodia; these lappets are low, rounded, large, and leaflike or pointed and triangular. The posterior end narrows to a relatively simple pygidium, sometimes with several

lobes and often bearing short papillae (Fig. 7.6.2.1 B, F). In one species, Travisia palmeri, the pygidial segments are shifted laterally (Maciolek and Blake 2006). The prostomium is small, smooth, and either rounded, conical, pointed, or truncate (Fig. 7.6.2.1 A–D); prostomial horns or processes are entirely absent; prostomial (and segmental) eyes are absent; nuchal organs are present as simple slits. The mouth of travisiids is an oval opening surrounded by upper and lower lips derived from elongated annulations of chaetiger 1 for the upper lip and chaetiger 2 for the lower lip (Figs. 7.6.2.1 D and 7.6.2.2 A). Parapodia are biramous and reduced to low mounds or entirely absent; when present, parapodial lappets or lobes occur along most of the body, or are limited to middle and posterior segments. Interramal sensory organs or pores are present (Fig. 7.6.2.1 B–E). Branchiae are present or absent; when present, they first occur on chaetiger 2 or 3 and continue along most of the body and are typically single, simple cirriform structures that are short or elongate (Fig. 7.6.2.1 E), sometimes annulated. The distribution of short or elongate branchiae along the body is of taxonomic importance. Two species with numerous filaments arising from one side of a single branchia are known (León-González 1998); only one species is reported to have two to three branchial branches, all others have only a single branch. Chaetae are all simple capillaries, with some species having fine serrations along one border (Hartman 1969).



7.6.2 Travisiidae Hartmann-Schröder, 1971, new family status 

Anatomy There are few studies of the internal and external anatomy for species of Travisia. Hartmann-Schröder (1958) provided observations on Travisia forbesii using standard histological methods. She described epidermal papillae imbedded in a thickened cuticle and made a limited number of observations on the intestine, musculature, and nervous systems. The fine structure of the epidermal papillae of T.  forbesii was recently reported by Vodopyanov et al. (2014). The superficial appearance of these papillae is relatively smooth, but each is perforated with numerous fine pores (Fig. 7.6.2.2 C). These authors described the epidermis of Travisia as a highly modified variant of the normal one-layer epithelium found in most polychaetes. The Travisia epidermis consists of basal epidermal cells and an external layer of papillae (Fig. 7.6.2.2 D). The papillae are embedded in a thick cuticle consisting of glandular supporting epidermal cells and intercellular spaces. Each papilla has a single-celled peduncle that penetrates to the basal epidermal cells. The epidermal cells are interconnected such that the epidermis is continuous and uninterrupted over the body. Vodopyanov et al. (2014) go on to suggest that the unique nature of the epidermal papillae of T. forbesii represents a synapomorphy for the genus Travisia that is entirely different from the epithelium of Scalibregma described by Ashworth (1901), thus supporting a sister group relationship between the two taxa rather than the inclusion of Travisia in the Scalibregmatidae. Belova and Zhadan (2014) also determined that the epidermis of Ophelia, Ophelina, and Thoracophelia species have numerous gland cells, whereas there are none in Travisia forbesii. In addition, these authors found that the epidermal cells of T. forbesii were lower and wider than the other species of Opheliidae studied. Ultrastructure of cell contacts revealed that the epidermal cells of T. forbesii were connected by desmosomes whereas the species of Ophelia, Ophelina, and Thoracophelia had additional tight junctions and adhesive bands (Belova and Zhadan 2014). These authors suggested that the anatomical and ultrastructural differences between Travisia and the other three opheliids they studied provided support for the exclusion of Travisia from Opheliidae. An excellent account of the morphology and ultrastructure of the branchiae (gills) and respiratory system of Travisia and several opheliid genera was recently published by Belova and Zhadan (2014). These authors interpret the branchiae of these taxa as protrusions from the body wall that connect to the coelom and contain blood vessels that are connected to interepithelial blood

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sinuses. Several differences among the opheliid species studied differed significantly from Travisia, lending further support for including the latter in a separate family. Some examples are as follows: (1) branchiae of the Travisia lack cilia, whereas they are present in opheliids; (2) the cuticle of branchiae in the opheliids is thin and resembles the cuticle in other parts of the body whereas in Travisia the branchiae are covered with a protocuticle similar to that found in polychaete larvae; (3) the branchial epithelium of Travisia lacks glandular cells, whereas the opheliids have multiple gland cells (two types in Ophelina and one type in Ophelia and Thoracophelia); (4) epidermal cells of Travisia are connected by desmosomes whereas they are connected by dense junctions and/or adhesive belts in the opheliids; and (5) groups of blood cells are present in the branchiae of opheliids whereas they are absent in Travisia. Belova and Zhadan (2014) were unable to classify the branchiae of Travisia with any existing branchial types established by Storch and Alberti (1978). The pharyngeal morphology of Travisia and other deposit-feeding species was described by Tzetlin and Zhadan (2009). Travisia, orbiniids, and scalibregmatids were described as having a terminal mouth opening with a folded symmetrical axial proboscis with well-­developed ciliated lobes that, when everted, often form a ­complicated-looking structure. When everted, the proboscis of Travisia is in the center. In contrast, the proboscis of the opheliid genera Ophelia and Thoracophelia (as Euzonus) was found to be bubble-like, symmetrical, ciliated, and similar to those of Paraonidae, Capitellidae, and some maldanids. The digestive system of Travisia species was investigated by Penry (1988) and Penry and Jumars (1990) relative to feeding ecology. Travisia species were found to belong to a group of deposit-feeding polychaetes having the gut divided into four compartments. Details of the four sections of the intestine of Travisia foetida were described by Penry (1988). Two sections anterior to the cecal attachment were termed the foregut and anterior midgut. The two sections posterior to the cecal attachment were termed the posterior midgut and hind gut. The foregut was found to be elaborated into a number of thick-walled, involuted sacs and likely corresponds to the structure described by Tzetlin and Zhadan (2009) as the pharynx. Penry (1988) described a narrow tube that passes from the elaborate foregut past several septa into the anterior thin-walled midgut. The posterior midgut is described as a large saclike structure; the hindgut is thin-walled and fills most of the body cavity (Penry 1988).

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Reproduction and development There is little known concerning the reproduction and development of Travisia species. The direct development of T. forbesii from the Atlantic coast of France was described by Retière (1971), who observed spawning from November to February. Mature eggs were 280 to 300 µm in diameter. Eggs and larvae were nonpelagic; egg masses were deposited on the seabed where they underwent direct development in capsules. Development of chaetae occurred after the juveniles had hatched and crawled into the sediment. There is no evidence that any species of Travisia produces planktic larvae. The sperm ultrastructure of Travisia japonica was described by Ochi et al. (1977) and was considered by Jamieson and Rouse (1989) to be ­ect-­aquasperm. Postlarvae and juvenile forms of Travisia were collected by one of us (JAB) as part of a survey to the Antarctic Larsen Ice Shelf A in May 2000 and to the Weddell Sea as part of the ANDEEP program in February 2002. Live postlarvae and juveniles were extracted from sediment samples using a meiofaunal elutriation device. The organisms were kept fresh in a refrigerator and observed in a hanging-drop preparation on a microscope equipped with a cooling stage. These methods provided a means to observe living postlarvae and juveniles in the laboratory for an extended period. An eight-chaetiger postlarval form taken from a megacore in a nearshore basin (733 m) in the Larsen Ice Shelf area is shown in Fig. 7.6.2.3 A, B. This is likely Travisia kerguelensis McIntosh, 1885, a relatively common nearshore species in Antarctic seas. At this relatively early benthic stage of development, the body is short and fusiform, the prostomium is triangular and tapers to a pointed anterior end; parapodia are relatively well developed and bear fascicles of stiff capillary chaetae; the pygidium is bilobed and bears approximately five short anal cirri. Figure 7.6.2.3 C–E depicts later stages of benthic juveniles of another species, probably Travisia abyssora (Monro 1930), collected from multicores (Weddell Sea in deep water). This was the only species of Travisia identified from benthic samples as part of the survey (Blake and Narayanaswamy 2005). Figure 7.6.2.3 C shows an entire specimen with 15 chaetigerous segments; the entire body, apart from a short inflated section, is long and narrow, with a triangular prostomium that tapers to an acutely pointed tip. Parapodia are well developed; the pygidium is rounded, but divided into two lobes. The thick fusiform or grub shape typical of Travisia species was not apparent for this species; however, all basic chaetal and soft

morphology except branchiae was developed in these 15- to 18-chaetiger specimens, consistent with T. abyssora, which is an abranchiate species. Further development would include an additional 10 or more segments and a thickening of the body.

Biology and ecology The majority of Travisia species occur in shelf, slope, and abyssal depths: out of the 35 known species, at least 20 species occur in depths exceeding 200 m; the other 15 occur from the intertidal to approximately 200 m; a few species have been reported over great depth ranges.

Fig. 7.6.2.3: Photomicrographs of juveniles of ­Travisia species from Antarctica, from live specimens. A, B, ­Travisia kerguelensis, eightchaetiger benthic postlarvae; C–E, ­Travisia abyssora, 15-, 17-, and 18-chaetiger juveniles. ­Originals.



7.6.2 Travisiidae Hartmann-Schröder, 1971, new family status 

Approximately two-thirds of the 35 species occur in the Pacific Basin; the others occur in the Atlantic, Arctic, or Southern Oceans. Because of their bathymetric distribution, few species are available in sufficient numbers for the study of their biology. Travisia species are burrowing deposit feeders that do not form permanent tubes or burrows. According to Fauchald and Jumars (1971) and Dauvin and Bellan (1994), Travisia species are nonselective deposit feeders. However, Jumars et al. (2015) noted that some species, such as Travisia hobsonae in Florida studied by Dauer (1980), selectively chose large sand grains. Travisia species are known to be deep burrowers. Blake (1994) found that 70% of Travisia gravieri on the slope off Cape Hatteras, North Carolina, were found 2 to 5 cm below the surface. Travisia species have only been recorded from soft sediments; deep-sea species occur in fine sediments. The common North Atlantic species, T. forbesii, has been recorded from fine to coarse sands and has been found in the offshore parts of the North Sea in 15 to 30 m depth (Wolff 1973). Santos (1977) recorded T. hobsonae in clean medium-tofine sands in shallow waters of the Gulf Coast of Florida. A population of T. forbesii at Dinard on the Brittany coast of France was followed for 1 year by Retière (1972). Over a 13-month period, three size classes, corresponding to three generations, were found at any one time. Recruitment of a new generation occurred between November and February. Individual age classes seem to live for at least 2 years. Species of Travisia are known to emit a distinctive iodoform and fetid odor when collected (Santos 1977); indeed, the specific name of T. foetida, a species from western North America, is based on that characteristic (Hartman 1969). Penry and Jumars (1990) speculated that microbial fermentation might be part of the digestive strategy of Travisia species and could account for the characteristic odor.

Phylogeny and taxonomy Phylogeny There have been numerous efforts to analyze and understand the phylogenetic and systematic relationships among the genera of the Opheliidae, which until recently have included Travisia. The first cladistic analyses were based on morphology that, together with intrageneric phylogenetic and taxonomic summaries of Ophelia and Travisia, supported the inclusion of the Travisiinae with the Opheliidae (Bellan et al. 1990, Bellan and Dauvin 1991,

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Bellan-Santini et al. 1992, Dauvin and Bellan 1994). A more extensive cladistic analysis using morphological characters was performed by Sene Silva (2007), who found that of the three subfamilies, only the Travisiinae was monophyletic. Sene Silva (2007) identified the absence of distinct parapodia as a synapomorphy for Travisia together with the nature of the thick cuticle. This latter character is more likely a synapomorphy given the recent work of Vodopyanov et al. (2014), who described the unusual epithelium with an external layer of papillae that are embedded in a thick cuticle consisting of glandular supporting epidermal cells and intercellular spaces (see earlier discussion in the Morphology section). Several authors have postulated or suggested a close relationship between Travisia and the family Scalibregmatidae (Ashworth 1901, Blake 2000, Rouse and Pleijel 2001). Indeed, the earliest molecular analyses suggested a scalibregmatid origin for Travisia (Bleidorn et al. 2003, Hall et  al. 2004). However, the 18S rDNA sequence in GenBank used by these authors for T. forbesii was later discovered to actually belong not to Travisia but to the scalibregmatid Polyphysia crassa (Paul et al. 2010). A new sequence for T. brevis was therefore developed and used by Persson and Pleijel (2005), who identified Travisia and scalibregmatids as sister clades. Subsequently, yet another set of 18S rDNA sequence data for T. forbesii was used by Rousset et al. (2007), who found that Travisia grouped with opheliids. In an effort to resolve these seemingly contradictory results, which were most likely caused by misidentification of the material used in the molecular analyses, Paul et al. (2010) developed new sequence data for four genes: 18S, 28S, 16S, and histone 3 from Travisia brevis and T. pupa, both species from the northeast Pacific coast of North America. These two species were used in an analysis with 26 other polychaetes including 12 opheliids, 7 scalibregmatids, and representatives of 7 other families. Parsimony, maximum likelihood, and Bayesian analyses were largely consistent, supporting monophyly of the Opheliidae without Travisia: the two opheliid subfamilies Opheliinae and Ophelininae were clearly sister groups to one another whereas Travisia and the scalibregmatids were sister groups to one another. However, the results presented by Paul et al. (2010) have recently come under scrutiny because several of the GenBank sequence identifications in the published article were shown to be erroneous (G.R. Reid, posted to the Annelid List on 10 December, 2014); this error was confirmed by C. Bleidorn, one of the authors, in a subsequent post (11 December, 2014), but he stated that the sequences actually used in

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the phylogenetic analyses were correct even though the published sequences were not. Nevertheless, the lack of careful quality control of the data presented in Paul et al. (2010) yet again calls into question the results of molecular analyses involving species of Opheliidae and the genus Travisia. However, an analysis by Law et al. (2013) achieved the same results as Paul et al. (2010), and except for Neolipobranchius sp., their list of GenBank species identifications and DNA sequences seems to be correct, thus suggesting at least that Travisia does not belong with the Opheliidae. Neolipobranchius, a genus originally described as a scalibregmatid by Hartman and Fauchald (1971), nested with the Travisia species in the Persson and Pleijel (2005), Paul et al. (2010), and Law et al. (2013) analyses. The material was collected from the Gulf of Maine, but no information was provided in either publication as to who identified the specimen(s) as Neolipobranchius sp. or what characters were used as the basis for that identification. The same genetic results were used by Martínez et al. (2012, 2013), in which Neolipobranchius and Travisia were a sister clade to scalibregmatids. Neolipobranchius is an obscure and somewhat enigmatic genus with only two described species. The type species, Neolipobranchius glabrus, was described from abyssal depths of 4436 m off New England based on small specimens that were only 2.5 to 3.0 mm in length (Hartman and Fauchald 1971); the description is largely based on negative characters, including the lack of any typical scalibregmatid morphology such as a bifurcated prostomium, segmental annulae, lyrate chaetae, branchiae, or pygidial cirri. Its inclusion in the Scalibregmatidae was not justified by the original authors. As part of a recent study of postlarvae and juveniles of two species of Antarctic scalibregmatids (Blake 2015), recent observations on juveniles of other scalibregmatids from deep-­water (Blake unpublished), and observations on the holotype of N. glabrus, it is clear that the original description of N. glabrus was based on postlarvae that cannot be identified with any known scalibregmatid genus or species. The genus and species were therefore declared incertae sedis by Blake (2015). Similarly, the second species of Neolipobranchius, N. blakei Kudenov, 1985, was also considered to be a juvenile (Blake 2015), but with several characters typical of a scalibregmatid. The species was declared incertae sedis until a growth sequence can be established to determine its generic and specific identification (Blake 2015). Because the specimens identified as Neolipobranchius sp. formed a clade with Travisia in the

DNA analyses, those sequences may actually represent a species of Travisia. Based on morphology alone, there is little to support the inclusion of Travisia in the Scalibregmatidae. The surficial morphology of the epithelium described for Travisia in the Morphology section of this chapter is entirely different from that of scalibregmatids, which have a rugose and tessellated epithelium. Instead of epidermal papillae, Scalibregma has tall club-shaped glandular cells that are grouped into annulated rows of surficial blocky or rounded padlike elevations that are separated from one another by grooves formed of epidermal cells (Ashworth 1901). These elevations form species-specific annulated patterns. There is no thick cuticle or peduncled papillae as in Travisia. Thus, despite a superficially rough epidermal surface to the body, the morphology of the epidermis is entirely different between the two taxa. Additional differences may be seen with the origin of the upper and lower lips of the mouth, chaetae, prostomium, branchiae, and parapodia. Travisia and scalibregmatids both have lobes forming the upper and lower lips of the mouth, in Travisia, these originate from chaetigers 1 and 2, whereas in scalibregmatids, the lobes surrounding the mouth originate from the peristomium (Blake 2015). Travisiids have capillary chaetae, but in addition, scalibregmatids have lyrate chaetae and a wide diversity of spinous and acicular chaetae on anterior segments. The prostomium of Travisia is typically conical and either pointed to rounded, frontal appendages are absent; scalibregmatids, on the other hand, have a bifurcate prostomium and lateral or frontal horns often forming a T-shape. Eyes are absent in Travisia and present or absent in scalibregmatids. The branchiae of Travisia, when present, are usually single, rarely with a few branches and occur from anterior to posterior segments along the body; the branchiae of scalibregmatids, when present, are limited to a few anterior segments and are always dendritically or pectinately branched forming distinct clusters. Parapodia are reduced in both taxa, but several scalibregmatid genera have well-developed noto- and neuropodial lobes in posterior segments, sometimes with dorsal and ventral cirri or additional postchaetal lamellae. The parapodial lappets, when present in Travisia, occur from anterior or middle segments to the posterior end; these are not found in scalibregmatids. Based on morphological and anatomical comparisons reported in the Morphology section of this chapter and recent phylogenetic results, it is evident that Travisia should be removed from Opheliidae. However, Travisia



7.6.2 Travisiidae Hartmann-Schröder, 1971, new family status 

does not belong in the Scalibregmatidae as currently suggested by several authors (Martínez et al. 2012, 2013, Law et al. 2013). At best, molecular and morphological phylogenetic results support a sister-group relationship with Scalibregmatidae. We therefore propose that the opheliid subfamily Travisiinae Hartmann-Schröder, 1971 be elevated to full family status. Taxonomy Travisiidae Hartmann-Schröder, 1971, new family status Type genus: Travisia Johnson, 1840 Diagnosis: Body stout, fusiform, and grublike. Segments annulated, with posterior segments telescoped, forming folds that end in lappets dorsal and ventral to the parapodial rami; these lappets low and rounded, large and leaflike, or pointed and triangular. Prostomium small, conical, often pointed; eyes absent; nuchal organs present as ciliated slits. Parapodia reduced, with small fascicles of capillary chaetae; no other types of chaetae reported; lateral sensory organs present between rami. Cirriform branchiae present or absent, if present, from setiger 2 continuing along the body. Pygidium with ring of stout, unequal papillae. Travisia Johnson, 1840 Type species: Travisia forbesii Johnston, 1840 Synonyms: Dindymene Kinberg, 1866; type species: Dindymene concinna Kinberg, 1866 Dindymenides Chamberlin, 1919, replacement name for Dindymene Kinberg Kesun Chamberlin, 1919; type species: Kesun fuscus Chamberlin, 1919 Diagnosis: Same as for the family (see above). Remarks: The most comprehensive review of Travisia was by Dauvin and Bellan (1994) for the Opheliidae subfamily Travisiinae that had been established by HartmannSchroder (1971). Dauvin and Bellan (1994) reviewed the taxonomic status including synonymies, ecology, and biogeographic distribution of the then-known species of Travisia. They recognized 27 valid species and three subspecies, based largely on examination of types of 21 ­species. A key to these species was provided despite some being poorly known. They also synonymized Dindymenides and Kesun with Travisia, which had included species without branchiae. Additional species have been added by Hartmann-Schroder and Parker (1995), Leon-Gonzales (1998), Elías et al. (2003), and Maciolek and Blake (2006), which together with subspecies now recognized as valid species in the World Polychaete Database brings the total

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of currently known species of Travisia to 36 (see list below). Of these, 20 species occur in depths exceeding 250 m down to the Abyssal Plain; the other 16 occur from the intertidal to shelf depths of approximately 200 m. The definition of Travisia presented above also applies to the newly established family Travisiidae. Synapomorphies for travisiids were discussed in the Phylogeny section. List of species, synonyms, and distributions (from the World Polychaeta Database, Dauvin and Bellan (1994), and recent publications); synonyms in brackets. 1. Travisia abyssora (Monro 1930) Antarctic Ocean, off South Shetland Islands, 1080 m; Weddell Sea, 2942 to 6319 m. [Here removed from synonymy with T. glandulosa, a northern hemisphere species] 2. Travisia amadoi Elias, Bremec, Lana and Orensanz, 2003. Argentina. Intertidal to low water 3. Travisia antarctica Hartman, 1967. Antarctic Ocean, South Georgia, 730 to 6010 m. See Maciolek and Blake, 2006 4. Travisia arborifera Fauvel, 1932. Indian Ocean, 7 to 100 m; Andaman Sea, Gulf of Bengal; off Burma, 35 m 5. Travisia brevis Moore, 1923. Alaska to Southern ­California, shelf, and slope depths; Bering Sea; Sea of Okhotsk 6. Travisia carnea Verrill, 1873. Eastern Canada to New England, shallow water, 5 to 35 m [Travisia parva Day, 1973. Beaufort, North Carolina]. Fide Dauvin and Bellan (1994) 7. Travisia chiloensis Kükenthal, 1887. Southeast Pacific, Chile 8. Travisia chinensis Grube, 1869. China 9. Travisia concinna (Kinberg 1866). Akgoa Bay, South Africa, 5 to 20 m 10. Travisia doellojuradoi Rioja, 1944. Southwest Atlantic, Argentina, 115 m 11. Travisia elongata Grube, 1866. Southeast Pacific Ocean, Peru 12. Travisia filamentosa Leon-Gonzalez, 1998. North Pacific, Mexico, Baja California Sur 13. Travisia foetida Hartman, 1969. Northeast Pacific Ocean, off southern California, 250 to 3100 m 14. Travisia forbesii Johnston, 1840. Circumpolar, Davis Straits, Spitsbergen, Greenland, Iceland, northeast United States; widespread, offshore European waters; low water to 3000 m [Ammotrypane oestroides Rathke, 1843] [Ophelia mamillata Örsted, 1842] [Ophelia mamillata crassa Örsted, 1843]

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15. Travisia forbesii intermedia Annenkova, 1937. Northern Sea of Japan. Northwest Pacific, Japan, 30 m to deep water [Travisia kerguelensis intermedia Annenkova, 1937]. Fide Dauvin and Bellan (1994) 16. Travisia fusiformis Kudenov, 1975. Mexico, Gulf of ­California, intertidal 17. Travisia fuscus (Chamberlin 1919). Pacific Ocean, 3000 to 7580 m 18. Travisia gigas Hartman, 1938. California. Northeast Pacific, California, low water to 180 m 19. Travisia glandulosa McIntosh, 1879. Northwest Atlantic, 3300 m 20. Travisia granulata Moore, 1923. Northeast Pacific, Southern, and Central California, 45 to 105 m 21. Travisia gravieri (McIntosh 1908). Atlantic Ocean, 539 to 7800 m 22. Travisia hobsonae Santos, 1977. Gulf of Mexico, Tampa Bay, 10 to 110 m 23. Travisia horsti Caullery, 1944. Pacific Ocean, Java Sea, 959 m 24. Travisia japonica Fujiwara, 1933. Japan, 10 to 100 m. See Dauvin and Bellan (1994) 25. Travisia kerguelensis McIntosh, 1885. Kerguelen, 50  m. Kerguelen Island; Southern Ocean, Antarctic, low water to 1837 m 26. Travisia lithophila Kinberg, 1866. Port Jackson, ­Australia, 20 to 180 m 27. Travisia monroi Maciolek and Blake, 2006. Antarctic Peninsula, 220 to 315 m [Travisia kerguelensis gravieri Monro, 1930. ­Antarctica, Palmer Archipelago]. Homonym of T. gravieri (­McIntosh, 1908) renamed T. monroi by Maciolek and Blake (2006) 28. Travisia nigrocincta (Ehlers 1913). South Pacific; ­Antarctic seas, 2725 m 29. Travisia oksae Hartmann-Schröder and Parker, 1995. Spencer Gulf, South Australia; Port Phillip Bay and Western Port, Victoria, Australia 30. Travisia olens Ehlers, 1897. Straits of Magellan; ­Southwest Atlantic; Southeast Pacific; Antarctic seas; New Zealand; low water to 1120 m 31. Travisia oregonensis Fauchald and Hancock, 1984. Offshore Oregon, 1600 to 1800 m 32. Travisia palmeri Maciolek and Blake, 2006. Antarctic Peninsula, 650 m 33. Travisia profundi Chamberlin, 1919. Atlantic; Pacific off Peru, 4300 m; Antarctic seas; 975 to 7290 m

34. Travisia pupa Moore, 1906. Northeast Pacific, 35 to 3000 m 35. Travisia tincta Maciolek and Blake, 2006. Off Lima, Peru, 1000 m References Ashworth, JH. (1901): The anatomy of Scalibregma inflatum Rathke. Quarterly Journal of Microscopical Science 45: 237–309, plates 13–15. Bellan, G., Bellan-Santini, D. & Dauvin, J.C. (1990): Phénétique et phylogénie des Opheliidae (Annélides Polychètes). Comptes Rendus de l’Académie des Sciences. Série III, Sciences de la vie 310: 175–181. Bellan, G. & Dauvin, J.C. (1991): Phenetic and biogeographic relationships in Ophelia (Polychaeta, Opheliidae). Bulletin of Marine Science 48: 544–558. Bellan-Santini, D., Dauvin, J.C. & Bellan, G. (1992): Approche phenetique et phylogenetique des Ophelia (Annélides Polychètes) de Mediterranee occidentale. Bulletin de l’Institut Océanographique de Monaco 9: 67–81. Belova, P.A. & Zhadan, A.E. (2014): Comparative morphology and ultrastructure of the respiratory system in four species of the Opheliidae family. Biology Bulletin 41: 752–772. Blake, J.A. (1994): Vertical distribution of benthic infauna in continental slope sediments off Cape Lookout, North Carolina. Deep-Sea Research II 41: 919–927. Blake, J.A. (2000): Chapter 7. Family Opheliidae Malmgren, 1867. In: Blake, J.A., Hilbig, B., & Scott, P.V. (eds.). Taxonomic Atlas of the Santa Maria Basin and Western Santa Barbara Channel. Vol. 7. Annelida Part 4. Polychaeta: Flabelligeridae to Sternaspidae. Santa Barbara Museum of Natural History, Santa Barbara, 145–168. Blake, J.A. (2015): New species of Scalibregmatidae (Annelida, Polychaeta) from the east Antarctic Peninsula including the description of the ecology and post-larval development of new species of Scalibregma and Oligobregma. Zootaxa 4033(1): 57–93. Blake, J.A. & Narayanaswamy, B. (2005): Benthic infaunal communities across the Weddell Sea Basin and the South Sandwich Slope, Antarctica. Deep-Sea Research II 51: 1797–1815. Bleidorn, C., Vogt, L. & Bartolomaeus, T. (2003): New insights into polychaete phylogeny (Annelida) inferred from 18S rDNA sequences. Molecular Phylogenetics and Evolution 29: 279–288. Dauer, D.M. (1980): Population dynamics of the polychaetous annelids of an intertidal habitat of upper old Tampa Bay, Florida. Internationale Revue der gesamten Hydrobiologie und Hydrographie 65: 461–487. Dauvin, J.C. & Bellan, G. (1994): Systematics, ecology and biogeographic relationships in the sub-family Travisiinae (Polychaeta, Opheliidae). Mémoires du Muséum National d’Histoire Naturelle 162:169–184. Elías, R., Bremec, C.S., da Cunha Lana, P. & Orensanz, J.M. (2003): Opheliidae (Polychaeta) from the southwestern Atlantic Ocean, with description of Travisia amadoi n. sp., Ophelina



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gaucha n. sp., and Ophelina alata n. sp. Hydrobiologia 496: 75–85. Fauchald, K. & Jumars, P.A. (1979): The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology. An Annual Review 17:193–284. Hall, K.A., Hutchings, P.A. & Colgan, D.J. (2004): Further phylogenetic studies of the Polychaeta using 18S rDNA sequence data. Journal of the Marine Biological Association of the United Kingdom 84: 949–960. Hartman, O. (1969): Atlas of the Sedentariate Polychaetous Annelids from California. Allan Hancock Foundation, University of Southern California, Los Angeles: 1–812. Hartman, O. & Fauchald, K. (1971): Deep-water benthic polychaetous annelids off New England to Bermuda and other North Atlantic areas: Part II. Allan Hancock Monographs in Marine Biology 6: 1–326. Hartmann-Schröder, G. (1958): Zur Morphologie der Opheliiden (Polychaeta Sedentaria). Zeitschrift für wissenschaftliche Zoologie 161: 84–143. Hartmann-Schröder, G. (1971): Annelida, Borstenwürmer, Polychaeta. Die Tierwelt Deutschlands 58:1–594. Hartmann-Schröder, G. & Parker, S.A. (1995): Four new species of the family Opheliidae (Polychaeta) from southern Australia. Records of the South Australia Museum 28: 1–12. Imajima, M. (2009): Deep-sea polychaetes off Pacific coast of the northern Honshu, Japan. In: Fugita, T. (ed.), Deep-sea Fauna and Pollutants off Pacific Coast of Northern Japan. National Museum of Nature and Science Monographs 39: 39–192. Jamieson, B.G.M. & Rouse, G.W. (1989): The spermatozoa of the Polychaeta (Annelida): an ultrastructural review. Biological Reviews 64: 93–157. Jumars, P.A., Dorgan, K.M. & Lindsey, S.M. (2015): Diet of worms emended: an update of polychaete feeding guilds. Annual Review of Marine Science, 7: 497–520, + Supplemental Appendix. Kudenov, J.D. (1985): Four new species of Scalibregmatidae (Polychaeta) from the Gulf of Mexico, with comments on the familial placement of Mucibregma Fauchald and Hancock, 1981. Proceedings of the Biological Society of Washington 98: 332–340. Kükenthal, W. (1887): Die Opheliaceen der Expedition der Vettore Pisani. Jenaische Zeitschrift für Naturwissenschaft 21: 361–373, plate 21. Law, C.J., Dorgan, K.M. & Rouse, G.W. (2013): Relating divergence in polychaete musculature to different burrowing behaviors: a study using Opheliidae. Journal of Morphology 275(5): 548–571. Leon-Gonzalez, J.A. de. (1998): Spionidae and Opheliidae (Annelida: Polychaeta) from the western coast of Baja California, Mexico. Bulletin of Marine Science 62: 7–16. McIntosh, W.C.A. (1885): Report on the Annelida Polychaeta collected by H.M.S. Challenger during the years 1873–76. Challenger Reports 12: 1–554, plates 1–55 and 1a–39a. Maciolek, N.J. & Blake, J.A. (2006): Opheliidae (Polychaeta) collected by the R/V Hero and the USNS Eltanin cruises from the Southern Ocean and South America. Scientia Marina 70S3: 101–113.

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Martínez, A., Di Domenico, M., & Worsaae, K. (2013): Evolution of cave Axiokebuita and Speleobregma (Scalibregmatidae, Annelida). Zoologica Scripta 42(6): 623–636. http:// doi:10.1111/zsc.12024. Martínez, A., Di Domenico, M., & Worsaae, K. (2014): Gain of palps within a lineage of ancestrally burrowing annelids (Scalibregmatidae). Acta Zoologica 95(4): 421–429. http:// doi:10.1111/azo.12039. Monro, C.C.A. (1930): Polychaete worms. Discovery Reports 2: 1–222. Ochi, O., Kubo, M. & Sawada, N. (1977): Electron microscope study on sperm differentiation in Travisia japonica (Polychaeta). Annotationes Zoologicae Japonensis 50: 87–98. Paul, C., Halanych, K.M., Tiedemann, R. & Bleidorn, C. (2010): Molecules reject an opheliid affinity for Travisia. Systematics and Biodiversity 8(4): 507–512. Penry, D.L. (1988): Digestion theory and applications to deposit feeders. Ph.D. Dissertation, University of Washington, Seattle. Penry, D.L. & Jumars, P.A. (1990): Gut architecture, digestive constraints and feeding ecology of deposit-feeding and carnivorous polychaetes. Oecologia 82: 1–11. Persson, J. & Pleijel, F. (2005): On the phylogenetic relationships of Axiokebuita, Travisia and Scalibregmatidae. Zootaxa 998: 1–14. Retière, C. (1971): Données sur l’ecologie de la polychète Travisia forbesii Johnston 1840 (Opheliidae) dans la region de Dinard: mise en évidence du cycle biologique. Comptes Rendus de l’Académie des Sciences, Paris 272: 3075–3078. Retière, C. (1972): Structure et dynamique d’une population de Travisia forbesii Johnson 1840 (Ophelidae) dans la region de Dinard. Comptes Rendus de l’Académie des Sciences, Paris 275: 1543–1546. Rouse, G.W. & Pleijel, F. (2001): Polychaetes. Oxford University, London: 1–354. Rousset, V., Pleijel, F., Rouse, G.W., Erséus, C. & Siddall, M. (2007): A molecular phylogeny of annelids. Cladistics 23: 41–63. Santos, S.L. (1977): A new species of Travisia (Polychaeta, Opheliidae) from Tampa Bay, Florida. Proceedings of the Biological Society of Washington 89: 559–564. Sene Silva, G. (2007): Filogenia de Opheliidae (Annelida: Polychaeta). Unpublished Thesis presented for the degree, Doctor of Sciences, in Zoology, Universidade Federal do Paraná, Curitiba: i–xii, + 1–95. (http://dspace.c3sl.ufpr.br/ dspace/handle/1884/12922) Storch, V. & Alberti, G. (1978): Ultrastructural observations on the gills of Polychaeta. Helgoländer Wissenschaftliche Meeresuntersuchungen 31: 169–179. Tzetlin, A. & Zhadan, A. (2009): Morphological variation of axial non-muscular proboscis types in the Polychaeta. Zoosymposia 2: 415–427. Vodopyanov, S., Tzetlin, A. & Zhadan, A. (2014): The fine structure of epidermal papillae of Travisia forbesii (Annelida). Zoomorphology 133(1): 7–19. Wolff, W.J. (1973): The estuary as a habitat an analysis of data on the soft bottom macrofauna of the estuarine area of the rivers Rhine, Meuse, and Scheldt. Zoologische Verhandelingen 126: 1–242.

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 7.6 Opheliida/Capitellida

James A. Blake

7.6.3 Scalibregmatidae Malmgren, 1867 Introduction Scalibregmatids are burrowing infaunal deposit-­feeding worms that are widely distributed but not commonly collected. Superficially, the bodies of most scalibregmatids have an areolated appearance due to the presence of one to six annulated rows per segment. Each annulation is composed of elevated pads of varying size. Their bodies are typically either elongate with an expanded anterior end and narrow abdominal region (arenicoliform) or short, thick, and without an expanded anterior end (maggot shaped); a few species have long, linear bodies. Scalibregmatids typically have a bifid or T-shaped prostomium with frontal or lateral horns suggested to be homologous to palps (Orrhage 1966, 1993). Parapodia are biramous with simple podial lobes; dorsal and ventral cirri occur in posterior parapodia of some genera. Branchiae, when present, are limited to a few anterior segments and have numerous branches. Chaetae are all simple and include capillaries, lyrate chaetae, and sometimes large recurved acicular spines. Apart from several early studies using standard histological techniques, there has been little effort to analyze the internal anatomy of scalibregmatids. There have been no studies of ultrastructure of any organ system. Scalibregmatids occur globally and range from the intertidal to the deep sea, but most species occur deeper than 100 m. Little is known about their biology except that they are considered subsurface, burrowing, deposit feeders (Jumars et  al. 2015). Random observations of swimming scalibregmatids and the presence of long natatory-like chaetae (Clark 1954) and the presence of sperm of the ect-aquasperm type (Blake 2015) suggest that spawning takes place in the water column. However, spawning and early embryonic development are not known. Recent observations on postlarvae and juveniles provide important data on the developmental timing of morphology (Blake 2015). Scalibregmatids include approximately 70 species distributed in 15 genera identified largely by a suite of overlapping characters. Because so many species (and genera) occur in deep water or are otherwise in habitats that are difficult to sample, there have been few species for which molecular sequences have been obtained. To date, there have been no phylogenetic analyses, morphological or molecular, that would serve to support a taxonomic revision of the family.

The present review of Scalibregmatidae includes as much information on morphology, biology, and taxonomy as possible given the lack of modern studies of internal anatomy and phylogenetic analysis. Information gaps are discussed where relevant. Current taxonomic status of genera and species is derived in part from the World Register of Marine Species (WoRMS) and in part from recent contributions (Bakken et al. 2014, Blake 2015).

Morphology External morphology Body shape and form. Scalibregmatid polychaetes are usually categorized as having bodies that are either long and arenicoliform with an expanded anterior region (Fig. 7.6.3.1 A) or short and stout (maggotlike) (Fig. 7.6.3.1 B). However, in some instances, this body shape categorization may be more an artifact of preservation rather than a significant morphological difference. For example, Elder (1973) who studied the burrowing of Polyphysia crassa, a species usually classified as having a maggotlike shape, depicts a worm that is capable of considerable elongation during its burrowing activity; however, the expanded region typical of species with the arenicoliform shape is not present in P. crassa. Furthermore, juvenile specimens of species with arenicoliform bodies seem to transition from a fusiform or maggotlike shape to a more elongate form with growth (Blake 2015); the expanded middle region develops later in ontogeny. Some species of Axiokebuita and Speleobregma have bodies that are more-or-less long and linear (Fig. 7.6.3.1 C), departing from more typical scalibregmatids. There are usually no more than 60 segments for any one species, and most species have fewer. The body segments are secondarily annulated with up to six annulations per segment, each of which is subdivided into elevated pads producing an areolated appearance similar to that of arenicolids (Figs. 7.6.3.1 B and 7.6.3.2 D, F). Prostomium. The prostomium of scalibregmatids is typically bifid or T-shaped on the anterior margin with distinct frontal or lateral horns (Fig.  7.6.3.2 A–F). These horns are especially long in the genera Axiokebuita and Speleobregma and have extensive cilia (Fig. 7.6.3.2 B) that probably assist in feeding and are thus analogous and possibly homologous to palps found in other polychaete families (Orrhage 1966, 1993, Orrhage and Müller 2005). Blake (2015) has shown that the postlarvae and juveniles of Scalibregma and Oligobregma pass through a developmental sequence in which an initial oval or round prostomium thickens and broadens along the anterior margin.



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Fig. 7.6.3.1: Three general body forms of scalibregmatids. A, Scalibregma inflatum, arenicoliform body shape with expanded anterior region; B, Polyphysia crassa, a maggot-shaped body with no expansion of body regions; C, Axiokebuita sp. with a narrow, elongate body and no expanded regions. A, after McIntosh (1915); B, after Støp-Bowitz (1945); C, after Persson and Pleijel (2005).

Fig. 7.6.3.2: Prostomia and peristomia of Scalibregmatidae, all in dorsal view. A, Scalibregma australis; B, Axiokebuita minuta; C, Sclerobregma branchiata; D, Pseudoscalibregma sp.; E, Sclerocheilus antarcticus; F, Oligobregma notiale. A, from Blake (2015); B, from Parapar (2011); C, D, originals from deep-water specimens offshore New England; E, F, from Blake (1981). Abbreviations: acS, acicular spines; frH, frontal horn; per, peristomium; pr, prostomium; nuO, nuchal organs.

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Subsequently, the actual horns develop as lateral bulges either directly from the anterior margin or as separate lobes that develop subapically with either a frontal or lateral orientation. The final form of the prostomial horns or lobes is thus defined late in development. Some of the intermediate stages of development have been incorrectly described as the final prostomium for some species, thus presenting taxonomic problems. Eyes are either present or absent; when present, they may be simple ocelli or larger and more complex, likely formed from a merger of numerous ocelli (Fig. 7.6.3.2 E, F). Nuchal organs are present on all scalibregmatids and are either inconspicuous retracted ciliated patches between the prostomium and peristomium (Fig. 7.6.3.2 B, C) or large everted swollen lobes. Peristomium. The peristomium of scalibregmatids typically consist of a single ring dorsally and one to three rings ventrally that merge with and form the upper and lower lips of the mouth (Figs. 7.6.3.2 A and 7.6.3.3 B, C, E). These rings may be simple annuli or consist of lobate pads of various sizes. Blake (2015) noted that the morphology of the upper and lower lips of the mouth differs considerably among three species of Scalibregma: (1) in Scalibregma inflatum, the mouth is surrounded dorsally by a biannulate row of large pads and ventrally by a single narrow row of pads; (2) in Scalibregma californicum, padded rows are not present; instead, there is small rounded upper lip, long lateral lips, and a ventral lip consisting of four to five short lobes; (3) in Scalibregma australis, the upper lip has a curved row of numerous narrow pads, small lobes laterally, and two rows of five to six large pads ventrally. The nature of the peristomial development and elaboration of the upper and lower lips of the mouth is of taxonomic importance, but has rarely been emphasized in species descriptions. The proboscis of scalibregmatids is eversible and anatomically determined to be of the soft axial type and similar to that of orbiniids (Tzetlin and Zhadan 2009). These authors examined four species: Polyphysia crassa, Scalibregma inflatum, Sclerocheilus antarcticus, and Sclerobregma branchiata. The everted proboscis of these species is weakly multilobed, with a boundary between the proximal unciliated and distal ciliated parts. When everted, the opening is in the center of the proboscis (Tzetlin and Zhadan 2009).

Body segmentation, annulation, and ventral groove. The bodies of scalibregmatids have one to six annulated rows of elevated pads on each body segment. The number of these rows varies by body region and the elevated pads may be small and numerous or large and few per row (Figs. 7.6.3.1 B, 7.6.3.2 A, D, F, and 7.6.3.3 A–F). Variation in the annulated rows and the nature of the elevated pads are important taxonomic characters. For example, Scalibregma australis, recently described from the east Antarctic Peninsula (Blake 2015) has the following arrangement of annuli along the body: dorsally, chaetiger  1 biannulate and chaetigers 2 to 3 triannulate, ventrally chaetigers 1 to 3 triannulate; subsequent anterior chaetigers of the expanded thoracic region quadriannulate; narrow posterior segments initially quadriannulate, then becoming first pentannulate and then quadriannulate in far posterior chaetigers. Each annulation is divided into separated elevated pads or blocked partitions, providing a complex areolated appearance to body surface (Fig. 7.6.3.3 B). There are no epidermal papillae such as those that characterize species of Travisia, with which scalibregmatids have been considered close relatives. A prominent ventral groove bearing a ridge line of elevated pads occurs in numerous species (Fig. 7.6.3.3 A, C–F); however, this midventral groove has rarely been emphasized in taxonomic descriptions and is an additional character that deserves further study. The recent articles by Parapar et al. (2011) and Martínez et al. (2013, 2014) on the two closely related genera Axiokebuita and Speleobregma suggest that a ventral groove or ridge line is entirely absent in all species reported. However, examination of Antarctic and North Atlantic specimens of Axiokebuita minuta and Axiokebuita millsi, respectively, suggest that a weakly developed ventral row of pads is present (Blake pers. obs.). Branchiae. Branchiae serve to support the definition of several genera, specifically Scalibregma, Sclerobregma, Cryptosclerocheilus, Parasclerocheilus, and Polyphysia. When present, branchiae occur posterior to the notopodia on four to six or fewer anterior chaetigers. Individual branchiae are typically dichotomously branched forming a complex arborescent structure (Fig.  7.6.3.4  A–C). However, an unusual type of branchia has been observed on Sclerobregma branchiata consisting of one or more large, elongate, pectinate-like structures (Fig. 7.6.3.4 D, E)

▸ Fig. 7.6.3.3: Anterior morphology of Scalibregmatidae, with emphasis on the venter. A, Scalibregma inflatum, entire animal; B, same, anterior end, dorsal view; C, same, anterior end, ventrolateral view; D, same, posterior segments, ventral view; E, S. australis, ventral view; F, Pseudoscalibregma parvum, ventral view. A–D, originals from specimens off Cape Hatteras, North Carolina; E, from Blake (2015); F, after Bakken et al. (2014). Abbreviations: br, branchiae; frH, frontal horn; per, peristomium; pyg, pygidiuim; lL, lower lip of mouth; uL, upper lip of mouth; vC, ventral cirrus; vG, ventral groove.



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in a stacked series in which individual branchial filaments arise from an elongate flattened lamella, with additional, smaller lamellae located under the first (Blake  and Luzak unpublished). These branchiae were erroneously reported by Hartman (1965: 185) as “…­pinnately compound, divided six to eight times into many distal branches.” Pectinate branchiae have also been observed in the opheliid genus Thoracophelia, but are single and smaller when they occur and flaglike in appearance (Blake 2000b, Law et al. 2013a). A recent study of the development of postlarvae and juveniles of Scalibregma australis (Blake 2015) demonstrated that branchiae are one of the last characters to develop and are not recognizable as such until the differentiation of 28 chaetigers and a body length of 3.5 mm is reached. A  similar pattern has been found in Sclerobregma branchiata from the western North Atlantic (Blake and Luzak unpublished). This means that worms of 4.0 mm or less cannot be reliably identified to the generic level unless a growth sequence is available, thus calling into question the taxonomic status and validity of several recently described species. Parapodial morphology. Parapodia are biramous with widely separated rami, but the podia themselves are often poorly developed, especially in anterior segments; in posterior chaetigers the podia may be more elongate but relatively simple in form (Fig.  7.6.3.4 F). Interramal papillae or sensory organs are usually present, but their function is not well understood. Dorsal and ventral cirri, when present, are largely restricted to the middle and posterior segments of the body (Fig. 7.6.3.4 F). In genera and species in which both dorsal and ventral cirri are present, their size and shape are important taxonomic characters. Genera having only ventral cirri but no dorsal cirri are Axiokebuita, Parasclerocheilus, Sclerocheilus, and Speleobregma, with the cirri tending to be elongate narrow structures. Other parapodial structures such as postchaetal lamellae are rare, but sometimes present in posterior segments. At least one species, Asclerocheilus californicum, has long postchaetal lobes arising dorsal and ventral to the noto- and neuropodia along most of the body. In some species with both dorsal and ventral cirri, unique tubular-shaped unicellular glands have been

found within the cirri and may represent an unappreciated taxonomic character that is more widespread than reported (Fig. 7.6.3.4 F–H). Apart from Ashworth (1901) for Scalibregma inflatum, Bakken et al. (2014) for S. hanseni, and Blake (1981) for Pseudoscalibregma usarpium, these glands have rarely been mentioned in the literature or, if mentioned, have not been discussed in detail. Unicellular glands were present in the dorsal and ventral cirri of three new species in three different genera recently described by Blake (2015) from Antarctica. In S. australis, the glands exited along the upper surface of the dorsal cirri and the ventral surface and near the tip of the ventral cirri (Fig. 7.6.3.4 G, H); this is similar to what Ashworth (1901, pl. 13, fig. 10) reported and illustrated for S. inflatum. In Pseudoscalibregma palmeri, these glands are even more numerous and exit along the upper surface and around the entire tip of the dorsal cirri and along the entire ventral surface of the ventral cirri (Blake 2015). In Oligobregma mucronata, the glands in the dorsal and ventral cirri are few in number and exit through the nipplelike tip of each cirrus. Recent scanning electron micrographs (SEM) of the ventral cirri of S. branchiata reveal the presence of minute pores (Fig. 7.6.3.4 I) that are likely the exit points of tubular glands (Fig. 7.6.3.4 F–H; Blake and Luzak unpublished). The tubular and unicellular nature of these glands was described in detail for S. inflatum by Ashworth (1901), but their function remains unknown. In addition to their presence on the dorsal and ventral cirri, similar appearing tubular-shaped glands have been observed on anterior parapodia of some species (­Ashworth 1901, Blake 2015). In Scalibregma australis, a row of these glands occurred across the dorsum of several anterior chaetigers; a few isolated glands were also observed on the neuropodia (Blake 2015). Individual pigmented glands were also observed on anterior noto- and neuropodia of P. palmeri (Blake 2015). Interramal sensory organs or papillae are typically present along the entire body. These occur between the noto- and neuropodia and, based on early investigations by Ashworth (1901) and Dehorne and Dehorne (1913), there seem to be two kinds: (1) a retractile ciliated papilla that is linked to the nervous system and (2) a nonciliated papilla that contains numerous glands. The distinction between these two types of interramal organs has not

▸ Fig. 7.6.3.4: Branchiae, parapodia, and pygidia of Scalibregmatidae. A, Scalibregma australis, lateral view; B, arborescent branchiae of S. australis; C, arborescent branchiae of Scalibregma wireni; D, Sclerobregma branchiata, dorsolateral view; E, same species, parapodium with pectinate branchiae, anterior view; F, Scalibregma australis, posterior parapodium, anterior view; G, H, same, detail of dorsal (G) and ventral (H) cirri showing internal tubular glands; I, Sclerobregma branchiata, detail of ventral cirrus showing minute pits or pores believed to be from tubular glands; J, pygidium of Scalibregma australis, ventral view; K, pygidium of Oligobregma collare; L, pygidium of Hyboscolex pacificus; M, pygidium of Speleobregma lanzaroteum. A, D, I, originals; B, after Knox and Cameron (1998); C, after Furreg (1925); E, after Hartman (1965); F–H, J after Blake (2015); K, after Blake (1981); L, after Imajima (1961); M, after Bertelsen (1986). Abbreviations: aC, anal cirrus; br, branchiae; Ch1, chaetiger 1; dC, dorsal cirrus; pap, papillae; vC, ventral cirrus.



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been investigated and may be of systematic significance. Additional details of these and other sensory organs are discussed in the next section on internal anatomy. Pygidium. The pygidium of scalibregmatids typically bears two or more lobes and five or more anal cirri (Fig.  7.6.3.4 J–L). The number of lobes and cirri and the shape and length of the cirri may be important taxonomic characters. A different kind of pygidium occurs in the genera Axiokebuita and Speleobregma, which have two large rounded lobes that bear numerous small adhesive papillae (Fig. 7.6.3.4 M). Chaetae. Chaetae are simple and include long thin capillaries, long delicate lyrate chaetae, heavy acicular spines in one to four anterior parapodia of some genera, short spinous chaetae on a few anterior chaetigers of many species, and, in Speleobregma, hooked spines in the neuropodia along the entire body (Fig.  7.6.3.5 F, G). When present, the lyrate chaetae have tynes that are of unequal or nearly equal lengths with the ratio between their lengths sometimes useful as a taxonomic character. Lyrate chaetae have delicate bristles or thin plates on the inner surface of each tyne (Fig. 7.6.3.5 K–N). On anterior chaetigers prior to where the lyrate chaetae begin, short spinous chaetae may be present; these are believed to be homologous to the lyrate chaetae that occur on subsequent segments (Mackie 1991, Blake 2000a, 2015, Bakken et  al. 2014). Typically, these short spinous chaetae are inconspicuous and observed only anterior to and at the bases of the long capillaries (Fig.  7.6.3.5 A–E); the spinous chaetae have been reported with blunt or aristate tips, rarely bifid. These short spinous chaetae have now been observed in many species, even in some having large acicular spines (Fig. 7.6.3.5 D, E) (Blake 2015). In contrast to the short, inconspicuous spinous chaetae, the large acicular spines that occur in the genera Asclerocheilus, Oligobregma, Parasclerocheilus, Sclerocheilus, and Sclerobregma are considered to have a separate origin (Mackie 1991). This is supported by the observation that some species with large spines may also have the short spinous chaetae anterior to the large acicular spines (Blake 2015). The large acicular spines typically occur only in the notopodia; 3 of the 12 species of Asclerocheilus, 2 of the 8 species of Oligobregma, and Sclerobregma  branchiata have spines in both noto- and neuropodia (Blake 2000a, 2015). The large acicular spines are typically sickle shaped or curved and are often covered with fibrils that may form a cloak over the tip of a

pointed shaft (Fig. 7.6.3.5 E, H–K); these chaetae are best seen with SEM (Fig. 7.6.3.5 E). Anatomy There have been relatively few detailed accounts of internal scalibregmatid morphology. Four studies of note include Danielssen (1859) and Ashworth (1901) on Scalibregma inflatum, Dehorne and Dehorne (1913) on Sclerocheilus minutus, and Elder (1972) on Polyphysia crassa. McIntosh (1915) provides some discussion of internal anatomy, largely taken from Ashworth (1901). Orrhage (1966) compared the nervous system of S. inflatum with other polychaetes. There are no modern studies in which the ultrastructure of scalibregmatid organs and tissues has been described. Epidermis. Instead of epidermal papillae as recently described for Travisia by Vodopyanov et  al. (2014), scalibregmatids have distinct squared or rounded padlike elevations that are grouped into annulated rows. These elevations form species-specific annulated patterns in many species. Individual pads are formed by elongated columnar cells and club-shaped mucus-forming gland cells (Fig. 7.6.3.6 A) (Ashworth 1901). The large number of elevated pads containing these glands suggests that most of the body surface of scalibregmatids is secretory to some extent. Some specimens of Scalibregma have been observed with a distinctive yellow-orange color over much of the epidermis. Ashworth (1901:258) attributed this to “numerous insoluble yellow granules in the epidermal cells.” The nature and role of this substance has never been analyzed, but it is very evident in specimens collected from the continental slope off Cape Hatteras, North Carolina (Fig.  7.6.3.3 A–D). An initial suspicion was that the substance might be arsenic taken up by the worms during their ingestion of sediment because arsenic and copper have been found to accumulate in tissues of cirratulid polychaetes with no toxic effects (Milanovich et al. 1976, Gibbs et al. 1983). Blake (1996) speculated that the uptake of metals in these cirratulids might account for observations by Yoshiyama and Darling (1982) that a cirratulid they tested was distasteful to intertidal fish. However, arsenic was not among the metals analyzed from the sediment and invertebrate tissue samples taken on benthic surveys at the Cape Hatteras slope site (Blake et al. 1986). This yellow coloration within scalibregmatid epidermal cells deserves further investigation. There is only a small amount of connective tissue between the epidermis and the underlying musculature in Scalibregma inflatum (Ashworth 1901). In contrast,



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Fig. 7.6.3.5: Examples of chaetae of Scalibregmatidae: A, short anterior spinous chaetae from chaetiger 1 of Scalibregma australis (arrows); B, same details of short spinous chaetae; C, Pseudoscalibregma sp., chaetigers 1 to 2 showing capillaries preceded by short spinous chaetae (arrows); D, Sclerobregma branchiata with large acicular spines and short, anterior spinous chaetae (arrow); E, Asclerocheilus tropicus, chaetiger 1 showing large acicular spines and minute spinous chaetae (arrow); F, G, Speleobregma lanzaroteum, hooked neurochaeta; H–L, acicular spinous chaetae of anterior notopodia; H, Sclerobregma branchiata; I, Oligobregma mucronata; J, Asclerocheilus californicus; K, Asclerocheilus beringianus; L–N, lyrate chaetae; L, A. californicus; M, Oligobregma notiale; N, Scalibregma australis. A, B, I, N, from Blake (2015); C, D, H, originals; E, after Nogueira (2002); F, after Bertelsen (1986); G, after Martínez et al. (2013); J, K, L, from Blake (2000a); M, from Blake (1981). Abbreviation: acS, acicular spine.

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Elder (1972) reported that Polyphysia crassa exhibits a well-developed connective tissue layer composed of collagen fibers arranged in honeycombs that exceeds the combined thickness of circular and longitudinal muscles. There are no other reports of epidermal anatomy in scalibregmatids. Sensory organs. There are three kinds of sense organs known for scalibregmatids: (1) ciliated nuchal organs, (2) lateral sense organs or papillae, and (3) eyes, which may be present or absent. Details of these sense organs are contained in the articles by Ashworth (1901) on Scalibregma inflatum and Dehorne and Dehorne (1913) on Sclerocheilus minutus. These earlier works were reviewed by Rullier (1951) who confirmed some observations and added others. There have been no modern studies of scalibregmatid sense organs. Nuchal organs of S. inflatum and other scalibregmatids consist of ciliated cells that are located in a groove between the prostomium and peristomium. These are typically retracted within the groove, but when everted may appear as expanded bulbous vesicles. The nuchal organs are innervated from two lobes that constitute the posterior part of the brain (Ashworth 1901, Dehorne and Dehorne 1913, Rullier 1951). According to Ashworth (1901), a pair of lateral sense organs is present in each parapodium of S. inflatum. They are best developed in the anterior half of the body. Each sense organ is a small mound rising from the base of a shallow depression bordered by prominent folds of epidermis (Fig. 7.6.3.6 F, G). Delicate external sensory cilia arise from internal pyriform or fusiform cells termed ganglia cells by Ashworth (1901). He described these ganglia cells as bipolar with the external sensory hairs connecting to the cell internally and in turn connecting to the ventral nerve cord (Fig. 7.6.3.6 F, G). Ashworth (1901) described the similarity of these sense organs and their innervation to those of Capitella as described by Eisig (1887). In contrast to Ashworth (1901), Dehorne and Dehorne (1913) described the lateral sense organs of Sclerocheilus minutus as papillae consisting of glandular cells (Fig. 7.6.3.6H). Blake (2015) observed the lateral sense organs

of Pseudoscalibregma palmeri as appearing to be a glandular papilla rather than a ciliated structure. It is likely that both types of lateral organs occur but have not been recorded in sufficient detail to categorize further. The “dorsal knob” that occurs ventral to the notochaetae of Axiokebuita (Parapar et al. 2011) is also most likely a lateral sense organ that is displaced from the midpoint between the podial lobes and arises closer to the notochaetae; this seems to be of the glandular type. Externally, however, these sensory organs are often difficult to observe and the cilia, if actually present, tend to be obscured with preservation. Modern histological studies would be of considerable interest to better understand the kinds and distribution of lateral sense organs in scalibregmatids. Eyes, when present, in scalibregmatids are (1) small, single, and inconspicuous or (2) large and composed of numerous ocelli that are conspicuous and form distinct shapes. Dehorne and Dehorne (1913) described the morphology of the large eyes of Sclerocheilus minutus. These eyes are composed of numerous individual ocelli that are epidermal and grouped to form a shape like an arrowhead (Λ) with the point directed anteriorly on the prostomium (Fig.  7.6.3.6 B); the ocelli are further separated into an anterior group and a posterior group. In addition, these authors noted a deeply imbedded pigmented sphere detached from the others; this separate sphere was interpreted as being another type of eye implanted directly on the brain or supraesophageal ganglion. Although there have been no modern descriptions of scalibregmatid eye ultrastructure, the individual ocelli of S. minutus described by Dehorne and Dehorne (1913) using standard histological sections bear some resemblance to the prostomial pigment cup eyes of the opheliid genus Armandia described by Hermans and Cloney (1966). A pigmented cell having a diaphragm and receptor surrounds a clear central area or lens (Fig. 7.6.3.6 C). The individual ocelli of S. minutus also have a heavily pigmented cell that surrounds a clear area containing what Dehorne and Dehorne (1913) called “bâtonnnet” or rodlike cells (Fig. 7.6.3.6 C, D). The authors also identified a set of what they called “retinal” (rétine) cells on both the anterior and posterior sides of the rows

▸ Fig. 7.6.3.6: Some anatomical features of Scalibregmatidae: A, padlike structure from an annular ring of Scalibregma inflatum; B, anterior end of Sclerocheilus minutus showing multiple eyes; C–E, transverse sections of eyes of S. minutus showing details of ocelli and bipolar cells; F, cross section of interramal sense organ of S. inflatum from far posterior segment; G, same from middle body segment; H, cross section of interramal papilla from S. minutus from a middle body segment; I, diagrammatic representation of a metanephridium of S. inflatum; J, section of a nephrostome from segment 13 of S. inflatum with location of associated genital cells indicated. A, F, G, I, J, from Ashworth (1901); B–E, H, from Dehorne and Dehorne (1913). Abbreviations: acS, acicular spines; annNer, annular nerve; coelEp, coelomic epithelium; colCells, columnar cells; circM, circular muscles; epdGl, epidermal glands; frH, frontal horn; intP, interramal papilla; longM, longitudinal muscle; neuroCh, neurochaetae; notoCh, notochaetae.



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of ocelli that presumably serve to collect signals and transmit them to the brain. Details of these cells reported by Dehorne and Dehorne (1913) suggest that the rodlike cells and retinal cells represent a single bipolar cell (Fig. 7.6.3.6E) that carries signals from the “lense” to the nervous system. A modern study of ultrastructure of scalibregmatid eyes would be of considerable interest in understanding the pathway of visual sense and the role such complex eyes composed of numerous ocelli play in the life of the worm. Comparative ultrastructure of scalibregmatid eyes would also allow better comparison with other polychaetes and assist in phylogenetic interpretation. Nervous system. Some aspects of the nervous system of Scalibregma inflatum were reported by Ashworth (1901). The brain or supraesophageal ganglion has an anterior lobe associated with the prostomium and two posterior lobes associated with the nuchal organs. The anterior lobe gives off a pair of nerves to the frontal horns on the prostomium; the esophageal connectives arise from the middle region of the brain; the posterior lobes give off nerves that run along the sensory epithelium of the nuchal organs. Orrhage (1966, 1993) and Orrhage and Müller (2005) identified nerves in the scalibregmatid Polyphysia crassa that correspond to palp innervations in other polychaetes. Out of 12 possible palp nerve roots in annelids identified by these authors, P. crassa had only two: one (No. 6) attached to the ventral nerve and another (No. 9) attached to the dorsal nerve. The only other polychaete family having this arrangement is the Paraonidae. At the time, the frontal horns of scalibregmatids were considered by these authors as being the site where these nerves served. However, the frontal horns of the greater majority of scalibregmatids are short and have been demonstrated to have a role in burrowing and crack propagation rather than feeding, which is the defined role of true palps (see section on burrowing and feeding below). Subsequently, Parapar et al. (2011) termed the elongate lateral horns of Axiokebuita spp. as “palps” because they were long, ciliated, had a shallow groove, and were in a subterminal position relative to the frontal horns of other scalibregmatids. A study of the SEMs in Parapar et al. (2011) reveals that a shallow groove on the “palps” is weakly visible in specimens from the Bellingshausen Sea (Antarctica), but are not evident in specimens from Norway and deep-water Antarctic, nor are they apparent in specimens of my personal collections from Antarctica and the western North Atlantic. Grooves on the “palps” are also not clearly evident in SEMs of Axiokebuita cavernicola and Speleobregma

lanzaroteum (Martínez et  al. 2013). However, these species live in rocky or gravelly habitats in shallow-water marine caves rather than the soft-sediment habitats of other scalibregmatids and the palps were found to have a role in feeding (Martínez et al. 2014). Before confirming the homology of the palps and horns, however, evidence of transformation of a structure used for burrowing to one used for feeding needs to be demonstrated by histological studies and confirmation of similarities or differences with the palp nerve roots identified for P. crassa by Orrhage (1966, 1993) and Orrhage and Müller (2005). In addition, the frontal horns of Scalibregma and other genera have been demonstrated to be lateral or frontal outgrowths of the anterior margin of the prostomium during postlarval development (see below; Blake 2015). The same process needs to be examined for Axiokebuita spp. and Speleobregma. Digestive system (alimentary canal). According to Ashworth (1901), the stomach and intestine of S. inflatum are connected to the midventral body wall by numerous thin strands of muscular tissue, forming a weak ventral mesentery. Ashworth (1901) noted that this arrangement is similar to that of Arenicola reported by Gamble and ­Ashworth (1898). The stomach seems to have a relatively loose attachment and, according to Ashworth (1901), swings back and forth with body movements and with the inversion and retraction of the proboscis. Ashworth speculated that this action provides a mixing of sand and ingested particles. The intestine is in a more fixed position. Penry and Jumars (1990) determined that Scalibregma californicum (as S. inflatum) from Puget Sound and S. inflatum from off North Carolina belong to a group of deposit feeders having three anatomically distinct gut compartments: foregut, midgut, and hindgut. As deep-burrowing deposit feeders, partitioning the gut into distinct compartments likely allows these scalibregmatids to have slower ingestion rates and longer through-times for processing. Coelom. In Scalibregma inflatum, the coelomic cavity is large and spacious, especially in the inflated anterior region (Ashworth 1901). The only conspicuous septa Ashworth observed were associated with the branchial segments (2–5). In the rest of the body, the septa are inconspicuous and represented by a thin strand of tissue running alongside the afferent nephridial vessel. Ashworth (1901) described the coelomic fluid as containing gametes in various stages of growth and various amoeboid cells. The reproductive cells collect principally in the space between the oblique muscles and the ventral body wall, especially in ripe females in which this space is crowded with ova. In S. australis,



Blake (2015) observed different specimens with spheroid masses of spermatids in the coelomic fluid in males and ova in different stages of maturation in ripe females. Musculature. Scalibregma inflatum has a layer of circular muscles immediately under the epidermis; beneath these are longitudinal muscle bands that project into the coelom (Ashworth 1901). The longitudinal muscles are interrupted by oblique muscle insertions and by the ventral nerve cord. Oblique muscles are short, thin, narrow bands that arise lateral to the nerve cord and are inserted into the body wall dorsal to the notopodial chaetal sacs. The parapodial muscles are moderately well developed. Each fascicle of chaetae is moved by five to eight slender protractor muscles attached to the base of the chaetal sac and to the body wall. In addition, a few short strands pass from the base of the notopodial chaetal sac and insert into the base of the neuropodial sac (Ashworth 1901). Two short muscle bands arise from the lateral body wall and are inserted into the inner and lower end of the nuchal organs. On contraction, this muscle serves to retract the nuchal organ. The prostomium is well supplied with muscles including several strong muscle strands that pass from the buccal mass to the neighboring body wall; these serve to retract the proboscis. A ventral mesentery connects the ventral wall of the stomach to the body wall close to the nerve cord (Ashworth 1901). Blood vascular system. The vascular system was first described by Danielsson (1859) and in more detail by Ashworth (1901). All observations were by dissection of large specimens of S. inflatum. The blood vascular system can be divided into dorsal and ventral vessels and their derivatives. The dorsal blood vessel originates near the anus and extends along the entire length of the intestine, dividing into capillaries on the pharynx and connecting via numerous branches with the stomach and intestine. A large extension, termed the blood reservoir by Danielsson (1859), is located near the anterior end of the stomach. Anterior to this reservoir, the dorsal vessel again narrows and continues anteriorly to a conical bulb that both Danielsson (1859) and Ashworth (1901) termed the heart but that may be more correctly termed the heart body. From there, the vessel resumes normal size and gives off branches to the branchiae, and finally branches that supply the pharynx, peristomium, and brain. The ventral blood vessel originates near the mouth from small vessels from the prostomium and peristomium and continues posteriorly to the entire length of the worm dorsal to the nerve cord. Four pairs of vessels from the

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branchiae join the ventral vessel causing it to assume a thickened size that is retained along its length. Along the way, the ventral blood vessel gives off branches to the stomach, nephridia, chaetal sacs, and adjacent tissues. There are also several blood sinuses associated with the stomach. A diagram of the entire blood system is shown in Ashworth (1901: fig. 14). Nephridia and reproductive organs. In Scalibregma inflatum, each metanephridium is a delicate ciliated tube that opens into the coelom by a minute simple nephrostome (Fig. 7.6.3.6 I). The excretory part of the tube is bent once on itself. In S. inflatum, there is a pair of nephridia in each chaetigerous segment except for the first three (Ashworth 1901). Genital cells arise along the tissue associated with the nephrostome (Fig.  7.6.3.6 J). These are the gonads of S. inflatum and are formed by the proliferation of cells covering the septum by which the nephrostome is attached to the body wall (Ashworth 1901). The genital cells are released from the gonad at an early stage and complete their growth and maturation in the coelom, thus following extra-ovarian development, deriving their nutrition from the coelomic fluid (Eckelbarger 2005, 2006). Upon release into the coelom, the ova gradually increase in size with a germinal vesicle and nucleolus becoming apparent at an early stage. Ova are initially flattened and somewhat doughnut shaped, but eventually round up prior to release from the body (Fig.  7.6.3.7 A). In S. australis, the largest ova found were approximately 110 μm in diameter (Blake 2015). Male gonads of S. australis and O. mucronata form sperm platelets bearing spermatids (Fig.  7.6.3.7 B) and mature into ect-aquasperm having a small rounded nucleus, a middle piece consisting of four mitochondria, and a long flagellum or tail (Blake 2015).

Reproduction and development Little is known concerning the reproductive biology of scalibregmatids. Adults of Scalibregma inflatum have been observed swimming in the plankton, a behavior that is likely associated with spawning (Ditlevsen 1911, Clark 1954). Clark (1954) reported Lipobranchius jeffreysii (McIntosh, 1869) swarming in the plankton in February 1953. Fage and Legendre (1927) reported a scalibregmatid swarming in the Mediterranean; Mackie (1991) thought this might have been Scalibregma celticum because eyes were present. In most cases, these swimming scalibregmatids exhibited long, natatory-like chaetae. Blake (1993) provided data on reproductive characteristics and size frequency for S. inflatum off Cape Hatteras,

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North Carolina. No seasonality was apparent in mean egg diameters found in collections from July 1984 (150 µm), May 1985 (160 µm), and September 1985 (130 µm). In addition, there was no indication of seasonality in the size frequency distribution of the number of chaetigers or the sizes of specimens observed during the three seasons studied. However, a shift toward the smaller size classes from May to September suggested possible summer recruitment. The presence of ect-aquasperm and eggs in the 110-µm diameter size range for Scalibregma australis, together with similar sperm observed for Oligobregma mucronata (Blake 2015) and published observations that adults of some species of scalibregmatids develop long natatory-like chaetae and swim in the plankton, suggest that spawning takes place in the water column for at least some species of Scalibregmatidae (Ditlevsen 1911, Clark 1954). Data on the mode and mechanism of spawning, fertilization, and early development in scalibregmatids is lacking. Ashworth (1901) did not consider the posterior nephridial ducts to be functional oviducts. He noted, however, that Danielssen (1859) reported eggs being squeezed out of intersegmental spaces. Clark (1954) suggested that some species might release gametes in mass spawnings into the sea. Development. Although embryology and early development are not known for scalibregmatids, Blake (2015) has described the development of postlarvae and juveniles of Scalibregma australis and Oligobregma mucronata from the East Antarctic Peninsula and notes that similar information is available for Scalibregma inflatum and Sclerobregma branchiatum from the western North Atlantic (Blake and Luzak unpublished). The following summary of postlarval and juvenile growth and differentiation is taken from Blake (2015). In Scalibregma australis, the body shape of postlarvae and juveniles is initially fusiform (Fig.  7.6.3.7 C–F); the characteristic inflated thoracic region and elongate, narrow posterior segments with dorsal and ventral cirri is not evident until approximately 22 chaetigers have developed (Fig.  7.6.3.7  F). Pigmented glands within the dorsal and ventral cirri of posterior segments are evident approximately by the 20-chaetiger stage. The midventral longitudinal groove with paired elevated pads begins to differentiate by the 14-chaetiger stage (Fig. 7.6.3.7 D) with medial pads evident in anterior chaetigers approximately by the 16-chaetiger stage and along the entire body after 20 chaetigers are developed. A 30-chaetiger juvenile has large midventral pads from chaetiger 2 and, with development, these single pads eventually divide into two and then four per segment, and form a prominent ventral ridge line within the ventral groove.

The early prostomium is bulbous and rounded (Fig. 7.6.3.7 G), becoming wider and somewhat triangular, and narrowing anteriorly to a conical tip (Fig. 7.6.3.7 H). With growth, the anterior border of the prostomium becomes thickened (Fig.  7.6.3.7 I) and by approximately 28 chaetigers has extended laterally as two lateral peaks (Fig.  7.6.3.7  J) that transition to short lateral horns (Fig. 7.6.3.7 K); prostomial horns are fully developed and assume adult form by the 30-chaetiger stage (Fig.  7.6.3.7  L).  Oligobregma mucronata follows the same sequence except that instead of ­lateral horns, subapical frontal horns develop. The peristomium of Scalibregma australis consists of a single ring both dorsally and ventrally through the 16-chaetiger stage; whereas the dorsal ring remains single; the ventral side becomes enlarged and begins to form the upper lip of the mouth. By the 28-chaetiger stage, the peristomium encompasses both the upper and lower lips of the mouth; by the 30-chaetiger stage, short narrow pads are present on the upper lip and large pads are present on the ventral lip as in adults. In larger adults, elements from the first chaetiger are also incorporated into the lower lip of the mouth. Dorsal cirri are the first to develop in S. australis; this happens by the 16-chaetiger stage. Ventral cirri do not develop until the 20-chaetiger stage and are initially limited to the last one or two posterior chaetigers. Dorsal cirri are always longer than ventral cirri; both, however, bear pigmented internal glands, with those of the dorsal cirri being more prominent (Figs. 7.6.3.4 F–H and 7.6.3.7 P). In O. mucronata, both cirri develop at the same time. The first branchial anlage of S. australis is a single bulge from the parapodial wall of chaetigers 3 to 4 of a 22-chaetiger juvenile; a single branchial filament was evident on chaetigers 3 to 5 of a 24-chaetiger specimen; a 28-chaetiger juvenile had branchiae on chaetigers 2 to 5, with one, two, three, and four lobes respectively, with branching. Juveniles with 30 chaetigers exhibited branchiae on chaetigers 2 to 5, with branching evident on branchiae of chaetigers 3 to 5. Capillary chaetae are present in both noto- and neuropodia on all chaetigers of all specimens of S. australis having 10 to 30 chaetigers. Lyrate chaetae are entirely absent on postlarvae of 10 to 15 chaetigers. However, short, spinous chaetae are present on chaetigers 1 to 4, anterior to the capillaries in noto- and neuropodia (Fig. 7.6.3.7 M). The first lyrate chaetae appear on chaetigers 3 to 4 of a 16-chaetiger postlarvae and then on chaetigers 2 to 4 of juveniles in the 17- to 20-chaetiger range. Thereafter, lyrate chaetae develop on middle and posterior chaetigers together with many more capillaries. It is noteworthy that through the 24-chaetiger stage, both spines and lyrate



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Fig. 7.6.3.7: Gametes, postlarvae, and juveniles of Scalibregma australis: A, egg ~110 μm removed from ovigerous female; B, sperm packet removed from mature male; C–F, specimens with 10, 16, 15, and 26 chaetigers showing development of body shape, parapodia, pygidium, and branchiae; G–L, development of prostomium by number of chaetigers attained (G, 16; H, 17; I, 20; J, 22; K, 28; L, 30); M, capillaries and short anterior spinous chaetae (arrows) from chaetiger 1 of a 26-chaetiger juvenile; N, same, short spinous chaetae and lyrate chaetae from chaetiger 4; O, pygidium and anal cirri on an 18-chaetiger juvenile; P, a 28-chaetiger juvenile with pygidium with anal cirri and also showing pigmented glands in dorsal cirri (P). All from Blake (2015). Abbreviation: aC, anal cirrus.

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 7.6 Opheliida/Capitellida

chaetae occur together with capillaries on chaetigers 2 to 4 (Fig. 7.6.3.7 N); thereafter, spines are present only on chaetiger 1. This suggests that the short spinous chaetae serve as precursors to the lyrate chaetae. In adults, these spinous chaetae are limited to chaetiger 1, the only chaetigerous segment to lack lyrate chaetae. The pygidium of Scalibregma australis is initially a simple bulbous segment, weakly divided into two lateral halves (Fig.  7.6.3.7 C, D). Four or five short pygidial cirri occur approximately at the 15-chaetiger stage. All five cirri are definitely present at 18 chaetigers (Fig. 7.6.3.7 O). The five cirri are arranged with two dorsolateral, two ventrolateral, and one midventral. With continued development, the pygidial cirri become elongate, cirriform, and rounded on the tips (Fig. 7.6.3.7 P). It is clear from these observations that the sequence and timing of development of key morphological characters varies considerably during ontogeny for the two species reported by Blake (2015) and also for unpublished observations on Scalibregma inflatum and Sclerobregma branchiata from the US Atlantic continental slope (Blake and Luzak unpublished). For example, the anterior margin of the prostomium of all four species progress gradually from a rounded, bulbous shape to the characteristic form of the adults with frontal horns while passing through growth phases in which the prostomium actually has the appearance reported for adults of other scalibregmatids. In S. australis, the dorsal cirri develop earlier than the ventral cirri and branchiae do not develop until approximately 28 chaetigers are present. The development of these and other characters suggests that for a species such as S. ­australis and likely other species, juveniles less than 4.0 mm in length and with 28 to 30 chaetigers may not possess sufficient morphology for accurate referral to a species or genus unless a growth sequence is available. Evidence of gametes or sexual maturity is typically not observed until largersized specimens are available (Blake 2015).

Biology and ecology Little is known about the biology of scalibregmatids because, with few exceptions, they are not readily available in sufficient numbers for either field observations or for experimental research in the laboratory. Most species inhabit muddy sediments and although known from intertidal depths, many species occur in depths greater than 100 m, with many described from continental slope and abyssal depths. Most species are subsurface deposit feeders that utilize the soft, eversible proboscis to ingest fine particles, which often result in the gut being distended (Jumars et al. 2015).

Burrowing and feeding. Dorgan et  al. (2006: 87) defined burrowing as “the act of making the opening in the substratum and moving into it.” Elder (1973) studied the burrowing of Polyphysia crassa, a relatively common scalibregmatid in soft, flocculent subtidal muds in Scottish waters. P. crassa uses its prostomial horns to move the sediment to the sides as it burrows, whereas the rest of body advances by direct peristaltic waves. Elder (1973) found that the body wall musculature and septa of P. crassa were modified to expedite this behavior (see also Elder 1972). Hunter and Elder (1983) used computer image analysis of video and observed that P. crassa used a peristaltic wave to move the body into a cavity of loosened sediment formed by the “head region” of the worm. Dorgan et  al. (2006) found similar behavior with Scalibregma californicum (as S. inflatum) in Puget Sound, where the worms burrowed by using a side-by-side motion of the frontal horns to propagate a leading crack in the sediment that they moved into. Scalibregma inflatum may be a reverse conveyor belt species in the Cape Hatteras sediments and capable of taking surface particles and possibly caching them at depth. This concept was supported by Cahoon et al. (1994) who tracked S. inflatum causing the movement of diatoms from the surface to depths greater than 14 cm and the rapid subduction of labeled material. In addition, Blair et al. (1996) documented rapid in situ uptake of 13C- labeled Chlorella sp. by S. inflatum and rapid subduction of labeled material in the same sediments off Cape Hatteras. However, subsequent labeling experiments with diatoms in the same region where the Chlorella was emplaced did not find rapid uptake, leading the investigators to suggest that S. inflatum took advantage of greater subduction of organic material by maldanids (Levin et al. 1997). The number and depth of other burrowers were positively correlated with maldanid abundance (Levin et al. 1997). Fauchald and Jumars (1979) suggested that S. inflatum could feed either at the surface or deep within the sediment. Jumars et al. (2015) largely corroborated this conclusion. Axiokebuita cavernicola and Speleobregma lanzaroteum are two unusual scalibregmatids that occur in marine and anchialine caves in the Canary Islands (Martínez et al. 2013). Specimens of A. cavernicola occur only in coarse sands and gravel sediments in areas where there is active water movement produced by waves and tides and where the water turbulence precludes particle deposition. Adults are semi-sessile and apparently anchor themselves to coarse sediment by the adhesive papillae of the pygidium. Worms were also observed using undulatory movements to swim for short distances; juveniles are apparently capable of swimming by use of ciliary bands along the body. S. lanzaroteum lives in a



part of the anchialine cave system where only tidal currents carry suspended organic matter. This species swims in the water column using undulatory body movements and slow movement of the parapodia; the species also attaches to the rocky substrate sediment with adhesive papillae on the pygidium. Both species have elongate ciliated lateral horns termed “palps” by Martinez et  al. (2013). It is likely that these palps serve to collect particles from the water column and carry them to the mouth. Thus, Axiokebuita and Speleobregma differ significantly from the greater majority of scalibregmatids that burrow into soft sediments and are deposit feeders. Density and diversity in soft-sediment benthic communities. High densities of species of Scalibregma were documented by Blake (2015). S. australis was one of the five dominant benthic species in mixed sediments on the east side of the Antarctic Peninsula in an area newly open to the sea by the collapse of the Larsen A Ice Shelf. Pockets of high densities of S. californicum were found at shallow subtidal locations in Puget Sound in the State of Washington, USA (R.E. Ruff and M. Dutch personal communications). Off Cape Hatteras, North Carolina, S. inflatum was found as a dominant component of continental slope assemblages between approximately 550 and 1500 m, with densities of up to 27,000 individuals per square meter at some stations (Blake and Hilbig 1994). S. inflatum occurred to a depth of 20 cm or more in the sediment (Blake and Hilbig 1994, Aller et al. 2002). The site is unusual in that a near-coastal sedimentary/nutrient regime is displaced to an otherwise deep-sea oceanic environment by downslope currents that transport both organic and inorganic particulates at a high rate (Rhoads and Hecker 1994). In addition to S. ­inflatum, several of the other dominant polychaetes are species that typically occur in shelf depths.

Phylogeny and taxonomy Taxonomic history The family Scalibregmatidae was established by Malmgren (1867) and originally included only S. inflatum and Eumenia crassa. As currently defined, the Scalibregmatidae now includes approximately 70 known species distributed among 15 genera; additional undescribed species, mainly from the deep sea, are also known (Blake unpublished). The earliest review of the family was by Ashworth (1901), who recognized 6 genera and 10 species. Early works dealing with new species and certain genera were published by Ashworth (1915), Furreg (1925), Fauvel (1928), and Støp-Bowitz (1945). More recently, additional new species and genera were described largely

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from the deep sea by Hartman (1963, 1965, 1966, 1967), Hartman  and Fauchald (1971), and Blake (1972). Day (1967) provided a useful review of the morphology and taxonomic problems of scalibregmatids. Important summaries of species were done by Kudenov and Blake (1978) and Blake (1981) who organized the genera on the basis of the presence or absence of ventral cirri, branchiae, and anterior acicular spines. Additional species were described by Bertelsen and Weston (1980), Kudenov (1984, 1985), Bertelsen (1986), Pocklington and Fournier (1987), Mackie (1991), Hartmann-Schröder (1994), Blake (2000a, 2015), Eibye-Jacobsen (2002), Schüller and Hilbig (2007), Schüller (2008), Imajima (2009), Martínez et  al. (2013), and Bakken et al. (2014). The main taxonomic problems with scalibregmatids seem to be at the generic level because many of the characters used to distinguish one genus from another are shared between some genera. Synapomorphies have not been identified that would resolve the relationships among genera. In the absence of a phylogenetic analysis of the family, the current arrangement of genera and species serves as a practical way to classify and identify species being used in ecological and biodiversity surveys. Phylogeny Morphological studies. Traditionally, Scalibregmatidae has been combined with Opheliidae to form the order Opheliida within Polychaeta (Fauchald 1977, ­HartmannSchröder 1996). The first major effort to develop a cladistic-based family-level phylogeny of polychae­ tes using morphological characters was by Rouse and ­Fauchald (1997). These authors established a phylogenetic hypothesis that arranged the polychaete families into six basic clades. Although they avoided Linnaean categories, the six clades might be called orders because they are the next category above the family level. Scalibregmatidae were grouped with eight other families into a clade termed Scolecida. The four families most closely grouped with scalibregmatids were Arenicolidae, Maldanidae, Capitellidae, and Opheliidae. Other families assigned to Scolecida were Orbiniidae, Paraonidae, Questidae, and Cossuridae. All these families are burrowing deposit-feeders that lack palps. In general, these families are often treated together in monographic or faunal works (e.g., Day 1967, Hartman 1969, Hartmann-Schröder 1996). There have been no efforts to develop a morphological phylogeny of the scalibregmatid genera or species. Sene Silva (2007) developed a phylogeny of the Opheliidae using morphological characters that included nine species of Scalibregmatidae in his cladistic analysis, but because a full suite of scalibregmatid characters was not included, these species remained more or less unresolved.

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There have been no other cladistic analyses of scalibregmatids using morphology. Molecular studies. Most attempts at phylogenetic analysis of scalibregmatids using molecular sequence data have focused on their relationships to other families; in particular, the Opheliidae with which they are often compared. There have been numerous efforts to analyze and understand the phylogenetic and systematic relationships among the genera of the Opheliidae, which until recently has included Travisia. Several authors have postulated a close relationship between the genus Travisia and Scalibregmatidae based on a superficial resemblance (Ashworth 1901, Blake 2000a, Rouse and Pleijel 2001). Initial molecular analyses also suggested a close scalibregmatid and Travisia relationship (Bleidorn et al. 2003, Hall et al. 2004). However, errors in the identification of the species of Travisia used in the 18S rDNA sequence were identified, which negated these early reports (Travisia forbesii was actually a scalibregmatid, Polyphysia crassa). A new Travisia sequence for T. brevis was therefore developed and used by Persson and Pleijel (2005), who found a scalibregmatid sister-group relationship for Travisia. Subsequently, yet another set of 18S rDNA sequence data for T. forbesii was used by Rousset et al. (2007), who found that Travisia grouped with opheliids. Paul et al. (2010) developed new sequence data for four genes: 18S, 28S, 16S, and histone 3 from T. brevis and Travisia pupa, both species from the northeast Pacific coast of North America. These two species were used in an analysis with 26 other polychaetes including 12 opheliids, 7 scalibregmatids, and representatives of 7 other families. Parsimony, maximum likelihood, and Bayesian analyses were largely consistent, supporting the monophyly of Opheliidae without Travisia: the two opheliid subfamilies, Opheliinae and Ophelininae, were sister groups to one another whereas Travisia and the scalibregmatids were sister groups to one another. Details of these and more recent molecular results with opheliids and scalibregmatids were reviewed by Blake and Maciolek (2019a,b) in companion chapters in this handbook. Based on more careful analyses by Paul et al. (2010) and Law et al. (2013b) using gene sequences from different species of Travisia, it is evident that this genus is more closely related to scalibregmatids and should be removed from the Opheliidae. All phylogenies recently published in which opheliids, Travisia, and a limited number of scalibregmatids have been analyzed demonstrate that Travisia is a sister group to scalibregmatids. These studies have been interpreted as assuming that Travisia and scalibregmatids actually represent a single family (Paul et  al. 2010, Law  et  al. 2013b, Martínez et  al. 2013, 2014). However, morphological differences between Travisia and

scalibregmatids are so great that, rather than squeezing the genus into the Scalibregmatidae and attempting to define a family in which one genus has nothing in common morphologically with the rest, Blake and Maciolek (2019b) elected to raise Travisia to full family status resulting in two sister families that are logical and easy to understand. Blake and Maciolek (2019b) based their decision to elevate Travisia to family status on (1) the differences in morphology between Travisia and the scalibregmatids and (2) molecular analyses, which, apart from those earlier studies with misidentified Travisia sequences, have never demonstrated that any Travisia species is nested within the scalibregmatid species tested. The superficial morphology of the epithelium with numerous epidermal papillae described for Travisia by Vodopyanov et al. (2014) is entirely different from that of scalibregmatids, which have a rugose and tessellated epithelium. Instead of epidermal papillae, Scalibregma has tall club-shaped glandular and columnar epithelial cells (Fig. 7.6.3.6 A) that are grouped into annulated rows of surficial blocked or rounded padlike elevations that are separated from one another by grooves formed of epidermal cells (Ashworth 1901). These elevations form species-specific annulated patterns. There is no thick cuticle or peduncled papillae as in Travisia. Thus, despite a superficially rough epidermal surface to the body, the histology of the epidermis is entirely different between the two taxa. Additional differences may be seen with the origin of the upper and lower lips of the mouth, chaetae, prostomium, branchiae, and parapodia. Travisia and scalibregmatids both have lobes forming the upper and lower lips of the mouth, but in Travisia these originate from chaetigers 1 and 2, whereas in scalibregmatids the lobes surrounding the upper lip originate entirely from the peristomium and the lower lip has contributions either all from the peristomium or partially from chaetiger 1 (Blake 2015). Travisiids have capillary chaetae but, in addition, scalibregmatids have lyrate chaetae and a wide diversity of spinous and acicular chaetae on anterior segments. The prostomium of Travisia is typically conical and either pointed to rounded and frontal appendages are absent; scalibregmatids, on the other hand, have a bifurcate prostomium and often lateral or frontal horns forming a T-shape on the anterior end. Eyes are absent in Travisia and present or absent in scalibregmatids. The branchiae of Travisia, when present, are usually single, rarely with a few lateral branches and occur from anterior to posterior segments along the body; the branchiae of scalibregmatids, when present, are limited to a few anterior segments and are always dichotomously or pectinately branched, forming distinct clusters. Parapodia are reduced in both taxa, but several scalibregmatid genera have well-developed noto- and neuropodial lobes in posterior segments, sometimes with dorsal and



ventral cirri or additional postchaetal lamellae. The parapodial lappets when present in Travisia occur from anterior or middle segments to the posterior end; these are not found in scalibregmatids. To date, there have been no phylogenies developed in which the full diversity of the 15 scalibregmatid genera has been examined. Given the distribution of these genera and the fact that so many species occur in deep water, it is unlikely that any comprehensive molecular phylogeny of scalibregmatids will be developed in the near future. Furthermore, given the vagaries of scalibregmatid taxonomy, great care must be taken to ensure that the identity of species selected for DNA sequencing are confirmed by recognized taxonomic experts to avoid errors such as those made with past mistaken identifications of species of Travisia and Neolipobranchius used in molecular sequencing. The situation with Neolipobranchius is unusual. The genus is obscure; a single species was described from a very small specimen found in abyssal depths of 4436 m off the coast of New England by Hartman and Fauchald (1971). Blake (2015) examined the holotype of Neolipobranchius glabrus and compared this specimen to the morphology of postlarvae and juveniles of S. australis from the Antarctic Peninsula and concluded that N.  ­glabrus represented a juvenile with no relevant morphology developed to classify it with any known scalibregmatid genus or even to confirm that it is a scalibregmatid. Blake (2015), therefore, declared the genus and its type species incertae sedis. A second species, Neolipobranchius blakei, described by Kudenov (1985) from a single specimen from shallow water in Florida was also considered to be a juvenile, requiring study of a growth sequence before it could be assigned to a scalibregmatid genus. Specimens identified as Neolipobranchius sp. collected from the Gulf of Maine and their DNA sequences were reported in articles by Paul et al. (2010), Law et al. (2013), and Martínez et al. (2013, 2014). The results were that the Neolipobranchius sp. sequences nested within Travisia sequences, suggesting that the genus Neolipobranchius should be synonymized with Travisia and by implication supporting the concept that Travisia belonged in the Scalibregmatidae. In fact, there was no information provided regarding the morphology of the specimens from the Gulf of Maine, who identified them, or why they were referred to such an obscure and invalid genus in the first place. It is most likely these were simply juvenile specimens of Travisia that were not recognized as such. The genera Axiokebuita and Speleobregma have evoked  considerable interest because species of both genera have been found in a marine cave system in the Canary Islands (Bertelsen and Weston 1980, Martínez et al. 2013, 2014). In molecular analyses, Axiokebuita and Speleobregma sequences suggest that these two genera and

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tested species form a distinct clade that is a sister group to other genera tested: Polyphysia, Scalibregma, Sclerobregma, Asclerocheilus, and Hyboscolex. Morphologically, these two genera lack most of the morphological characters that characterize the other 13 genera of scalibregmatids. Taxonomy Scalibregmatidae Malmgren, 1867 Type genus: Scalibregma Rathke, 1843, by monotypy Diagnosis (emended): Body variably shaped: (1) elongate and narrow throughout, (2) fusiform, (3) thick, maggot-shaped, or (4) elongate arenicoliform with anterior segments greatly expanded; with no more than 30 to 60 chaetigerous segments. Body with one to five annular rings on each segment; each ring composed of elevated pads; distribution of these rings and pads differs among species; venter with midventral groove or ridge formed of elevated pads along body, limited to one part of body or entirely absent. Prostomium either bilobed or T-shaped with two frontal or lateral horns, sometimes long, ciliated, and functioning as palps; eyes present or absent; nuchal slits present. Proboscis eversible, soft, unarmed. Peristomium achaetous; dorsal ring typically single, encompassing prostomium; ventral part with one to three rings forming upper and lower lips of mouth. Branchiae present or absent, when present limited to four to six or fewer anterior chaetigers, always with multiple branches, usually dichotomous. Parapodia biramous, with weakly developed podial lobes; interramal sensory organs or papillae present; dorsal and/or ventral cirri present or absent in middle and posterior segments, when present often with internal tubular glands; postchaetal lamellae rarely present. Chaetae all simple, including capillaries, lyrate chaetae present or absent, acicular chaetae on anterior segments present or absent; short spinous chaetae often present anterior to capillaries on chaetigers anterior to those where lyrate chaetae begin. Pygidium with two or more lobes; anal cirri present or absent. Remarks: This diagnosis encompasses most of the traditional morphology assigned to scalibregmatids and several newly emphasized characteristics (Blake 2015). Scalibregmatids are not commonly collected in routine investigations along the shore, being found mostly offshore in deeper sediments; the majority of species inhabit deepsea sediments and many species remain undescribed. A total of 15 genera are recognized here as valid; three others are referred elsewhere or are considered incertae sedis. Each genus is treated separately. Within the 15 genera, approximately 70 species are currently known, but several are poorly described and an additional 15 to 20 undescribed species, mostly from deep water, are also known (Blake unpublished). In addition, historical global records of S. inflatum continue to be parsed out as newly

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described species (Mackie 1991, Bakken et al. 2014, Blake 2000a, 2015). Asclerocheilus Ashworth, 1901 Type species: Lipobranchius intermedius Saint Joseph, 1894. Designated by Ashworth (1901) Synonym: Kebuita Chamberlin, 1919:390. Type species: Eumenia glabra Ehlers, 1897. Fide Blake 2000a (fifteen species) Diagnosis: Body elongate, arenicoliform. Prostomium T-shaped with frontal horns (Fig.  7.6.3.8 B). Parapodia of posterior segments reduced; dorsal and ventral cirri absent (Fig. 7.6.3.8 E); interramal papillae or cilia present or absent; postchaetal lamellae absent. Branchiae absent. Chaetae include capillaries, lyrate chaetae (Figs. 7.6.3.5 L and 7.6.3.8 D, I), and large, conspicuous curved spines on chaetigers 1 to 4 (Fig.  7.6.3.8 C, H), sometimes accompanied by short spinous chaetae (Fig.  7.6.3.5 E). Pygidium with long anal cirri (Fig. 7.6.3.8 E). Remarks: With 15 species as listed below, Asclerocheilus is presently the largest scalibregmatid genus. Twelve species of Asclerocheilus were reviewed by Blake (2000a). The majority of species are from the Indo-Pacific; to date, only one species is described from the North Atlantic. None of these species are commonly collected. Asclerocheilus beringianus, a deep-sea species reviewed by Blake (2000a), seems to have the widest distribution (Fig.  7.6.3.8 F, G). A. californicus is unusual in having elongate fleshy lobes arising dorsal and ventral to the noto- and neuropodia. Asclerocheilus kudenovi is a common species from offshore California (Fig.  7.6.3.8 B–E). The majority of species (10) have been named since 1980. The following list of valid species is taken from WoRMS (accessed 16 November 2015). 1. Asclerocheilus acirratus (Hartman, 1966), California, shallow subtidal 2. Asclerocheilus ashworthi Blake, 1981, subantarctic, 200 to 400 m; additional records will extend range to deeper Antarctic seas (Blake unpublished) 3. Asclerocheilus beringianus Ushakov, 1955, northeast Pacific Ocean, Bering Sea, Western North Atlantic, slope and abyssal depths 4. Asclerocheilus californicus Hartman, 1963, Southern California in shelf depths 5. Asclerocheilus capensis Day, 1963, South Africa, s­ ubtidal 6. Asclerocheilus elisabethae Eibye-Jacobsen, 2002, Andaman Sea off Thailand, 70 to 80 m 7. Asclerocheilus glabrus (Ehlers, 1887), Caribbean Sea 8. Asclerocheilus intermedius (Saint-Joseph, 1894), eastern North Atlantic, Ireland to Azores 9. Asclerocheilus kudenovi Blake, 2000a, Central California, shelf depths

10. Asclerocheilus mexicanus Kudenov, 1985, Gulf of Mexico, subtidal 11. Asclerocheilus shanei Hartmann-Schröder, 1994, Tasmania, shelf depths 12. Asclerocheilus shanonae Eibye-Jacobsen, 2002, Andaman Sea, shallow subtidal 13. Asclerocheilus tasmanius Kirkegaard, 1996, Tasman Sea, southwest of New Zealand, abyssal depths 14. Asclerocheilus tropicus Blake, 1981, Ecuador, Southern California, Brazil, shallow water 15. Asclerocheilus victoriensis Blake, 2000a, Southeast Australia, shallow subtidal [A. heterochaetous Kudenov and Blake, 1978, was identified as a homonym of Oncoscolex heterochaetous Augener, 1906 and referred to synonymy with Kebuita glabra (Ehlers, 1887) (see Blake (2000a)]. Axiokebuita Pocklington and Fournier, 1987 Type species: Axiokebuita millsi Pocklington and Fournier, 1987, by monotypy (three species) Diagnosis (emended): Body elongate, with segments similar throughout; generally slender throughout body (Fig. 7.6.3.1 A), but with at least one species having a fusiform shape (Fig. 7.6.3.9 B); segments with one to four annulated rings composed of small, inconspicuous elevated pads, best developed on middle and posterior segments; venter with weakly developed median ridge. Prostomium triangular (Figs. 7.6.3.2 B and 7.6.3.9 A, C), truncate on anterior margin with subterminal ciliated lateral horns (Figs.  7.6.3.2 B and 7.6.3.9 A, C, D); eyes absent, nuchal organs in narrow grooves on posterior part (Figs. 7.6.3.2 B and 7.6.3.9 C). Peristomium a single, complete ring, weakly incised dorsally, divided into upper and lower lips of mouth ventrally; formed from large expanded lobes (Fig.  7.6.3.9 A, C); unique paired ciliated “neck organs” present posterior to lower lip of mouth (Fig.  7.6.3.9 D). Parapodia biramous, similar throughout with short, digitate, or papilla-like ventral cirrus (Fig. 7.6.3.9 F); interramal sense organ or papilla present (Fig. 7.6.3.9 F), referred to by authors as “dorsal knob”;  postchaetal lamellae absent. Branchiae absent. Chaetae all capillaries, lyrate and spinous chaetae absent; long, natatory-like chaetae present or absent. Pygidium with two padlike lobes covered with papillae (Figs. 7.6.3.1 C and 7.6.3.9 E). Numerous cilia and ciliary patterns, similar to those of Speleobregma present on lateral horns and prostomium, and interramal papillae; unique paired ciliated patches on ventral side of body. Remarks: Axiokebuita millsi Pocklington and Fournier (1987) was initially described from upper slope depths off Nova Scotia. In the same article, the authors recognized



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Fig. 7.6.3.8: Examples of species of Scalibregma and Asclerocheilus. A, S. australis, anterior end, dorsal view; B–E, A. kudenovi: B, anterior end, dorsal view; C, acicular notochaetae from chaetiger 1; D, lyrate chaeta; E, posterior end, dorsal view; F–I, A. beringianus: F, anterior end, dorsal view; G, anterior end, right lateral view; H, acicular notochaetae from chaetiger 1; I, lyrate chaetae. A, from Blake (2015); B–I, from Blake (2000a). Abbreviations: acS, acicular spine; frH, frontal horn; per, peristomium; pr, prostomium; uL, upper lip of mouth.

Kebuita minuta Hartman (1967) from Antarctica as a species of Axiokebuita and referred it to their new genus. Subsequent reports of Axiokebuita spp. were from the Juan de Fuca Ridge, Northeast Pacific and off New England in slope depths by Blake and Hilbig (1990 as A. millsi), off Norway by Persson and Pleijel (2005 as Axiokebuita sp.), and other areas of the North Atlantic by Parapar et  al. (2011). The latter authors provided a detailed account of specimens of A. minuta from the Bellingshausen Sea, Antarctica and, based on new observations and reviews of older records and accounts, concluded that A. millsi and A. minuta should be synonymized with Hartman’s name taking priority (but see below). Most recently, Martínez et al. (2013) described A. cavernicola from marine caves in the Canary Islands. Several features of Axiokebuita species are characteristic for the genus and differ from most Scalibregmatidae

including (1) long subterminal lateral prostomial horns (termed palps by Parapar et  al. 2011) that are ciliated and likely assist in feeding and burrowing (Figs. 7.6.3.1 C, 7.6.3.2 B, and 7.6.3.9 A, C, D); (2) the presence of paired sensory “neck” organs on the ventral peristomium, separate from prostomial nuchal organs, that are either unique to Axiokebuita or unreported in other scalibregmatids (Fig. 7.6.3.9 D); (3) a unique pygidium with a pair of lobes that are covered with papillae (Fig. 7.6.3.9 E); (4) absence of lyrate and spinous chaetae; (5) the presence of ciliary bands on the prostomial horns and elsewhere on the prostomium and body. The paired sensory peristomial neck organs identified by Parapar (2011) for A. minuta have not been reported for other scalibregmatids, but may have been overlooked because there have been few studies using SEM. They are not reported in the closely related S. lanzaroteum by

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Fig. 7.6.3.9: Examples of species of Axiokebuita and Speleobregma. A, A. cavernicola, entire worm, dorsal view (specimen from marine cave, Canary Islands); B, A. millsi, entire worm, dorsal view (specimen from slope depths off New England); C, Axiokebuita sp., anterior end, dorsal view (specimen from Juan de Fuca Ridge); D, A. minuta, anterior end, ventral view; E, Axiokebuita sp., detail of pygidial pad with adhesive papillae (specimen from Trondheim, Norway); F, Axiokebuita sp. middle parapodium (specimen from the Juan de Fuca Ridge); G, S. lanzaroteum, anterior end, dorsal view. A, after Martínez et al. (2013); B, original; C, F, after Blake and Hilbig (1990); D, from after Parapar et al. (2011); E, after Persson and Plejiel (2005); G, after Bertelesen (1986). Abbreviations: intP, interramal papilla; lL, lower lip of mouth; neuroCh, neurochaetae; notoCh, notochaetae; nuO, nuchal organ; pr, prostomium; prob, proboscis, Seg1, segment 1; uL, upper lip of mouth; vC, ventral cirrus; vR, ventral ridge.



Martínez et al. (2013). The paired papillated pygidial lobes found in Axiokebuita also occur in the closely related genus Speleobregma. The absence of lyrate chaetae has been confirmed in all studies; the one report by Hartman (1967) seems to have been due to the presence of more than one species in the sample. The “dorsal knob” that occurs below the notochaetae is a lateral sense organ or papilla that occurs widely in scalibregmatids. In this case, it is a papilla displaced from the midpoint between the podial lobes closer to the notochaetae (Fig. 7.6.3.9 F). There are two types of lateral sense organs in scalibregmatids, ciliated and glandular, as described in the Morphology section of this chapter. The glandular type seems to be what occurs in Axiokebuita. Because the synonymy of A. millsi and A. minuta by Parapar et al. (2011) implies that A. minuta is a bipolar species, this deserves some comment. By definition, a bipolar species has a range that encompasses many thousands of miles and biogeographic provinces between the two poles. In deep water where both A. millsi and A. minuta are reported, bipolarity is more likely than with noninvasive shallow-water species that need to cross and adapt to numerous temperature and salinity regimes to become bipolar. In the deep sea, there are few barriers to dispersal given sufficient time and there are many deep-water polychaete species that have been reported with wide geographic ranges. However, bipolar species in general are few and with careful study are usually found to consist of closely related sibling species. One perceived bipolar scalibregmatid species is S. inflatum with the type-locality in Greenland and numerous reports from Antarctica. Blake (2015) has recently demonstrated differences between S.  inflatum and the Antarctic populations and established a new species, S. australis. The basis of this work is the use of new characters that have largely been overlooked in previous descriptions. These include the nature of the ventral peristomial rings and morphology of the lips surrounding the mouth, the presence and morphology of a midventral ridge, and details concerning the number and distribution of elevated pads on the annular rings. One obvious difference between the A. millsi and A. minuta specimens examined by the author is with body shape. A. millsi tends to have thicker and more fusiform bodies (see Pocklington and Fournier 1987: Fig.  7.6.3.1 and Fig. 7.6.3.9 B in this chapter, a specimen from off New England), whereas A. minuta tends to have a more slender body (see fig. 5A of Parapar et al. 2012 from Antarctica). Furthermore, specimens of A. millsi have a more distinct midventral ridge line than specimens of A. minuta. Parapar et al. (2011) noted that North Atlantic specimens have longer chaetae than Antarctic specimens. This is confirmed by new observations of North Atlantic material

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from off New England (Blake pers. obs.) in which the specimens have chaetae sufficiently long to be called “natatory-like.” In contrast, the figured specimen of A. minuta from the Weddell Sea has relatively short chaetae (Fig. 7.6.3.9 D and the numerous figures in Parapar et al. 2011). Based on these additional observations, A. millsi and A. minuta should be retained as separate species. Furthermore, there are no taxonomic accounts that actually compare specimens identified as A. millsi from the areas off Nova Scotia and New England with those of the eastern North Atlantic. Given the fusiform bodies of specimens from the Canadian and American locations (Fig. 7.6.3.9 B) and the more slender bodies from the European locations (Fig. 7.6.3.1 A), it is likely that more than one species is involved. The specimen from near hydrothermal vents on the Juan de Fuca Ridge identified as A. millsi by Blake and Hilbig (1990) seems to be an entirely different species based on overall morphology (Fig. 7.6.3.9 C) and the presence of slender spinous chaetae with pointed tips that these authors recorded. In contrast to the known records of A. millsi and A.  minuta in deep-water sediments, A. cavernicola from the Canary Islands is from a marine cave that is accessible by diving (Fig. 7.6.3.9 A). Martínez et al. (2013, 2014) suggest that the worms from the cave inhabit rocky crevices that are similar to crevicular habitats of the deepsea Axiokebuita species, suggesting a distributional or evolutionary pathway for the genus from the deep sea to the shallow-water caves. However, there is little evidence that deep-sea Axiokebuita species inhabit anything other than soft sediments as is typical of nearly every deep-sea ­scalibregmatid known. The genus Speleobregma, based on a single species, S. lanzaroteum, occurs in the same marine caves in the Canary Islands as Axiokebuita cavernicola (Bertelsen 1986, Martínez et al. 2013, 2014). As part of the phylogenetic analysis published by Martínez et al. (2013, 2014), the two cave-dwelling species were more closely related to one another and other Axiokebuita species than to other scalibregmatids. The main morphological difference between the two genera seems to be the presence of hooked neuropodial spines in Speleobregma (Fig. 7.6.3.5 F, G) that are not present in Axiokebuita. The following list of valid species is taken from WoRMS (accessed 16 November 2015) and as updated here: 1. Axiokebuita cavernicola Martínez, Di Domenico and Worsaae, 2013. Shallow marine caves, Canary Islands 2. Axiokebuita millsi Pocklington and Fournier, 1987. Deep-water habitats, Atlantic Ocean; Pacific records questionable 3. Axiokebuita minuta (Hartman, 1967). Deep-water habitats, Antarctica

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Cryptosclerocheilus Blake, 1972 Type species: Cryptosclerocheilus baffinensis Blake, 1972, by monotypy (one species) Diagnosis: Body elongate, arenicoliform; with numerous annulated segments (Fig.  7.6.3.10 A); ventral ridge with prominent pads present along body (Fig.  7.6.3.10 B). Prostomium T-shaped with lateral horns (Fig. 7.6.3.10 A, B); eyes absent; nuchal organs present in groove between prostomium and peristomium. Parapodia without dorsal or ventral cirri (Fig. 7.6.3.10 A); interramal papillae or cilia present; postchaetal lamellae absent. Branchiae present on chaetigers 2 to 5 (Fig. 7.6.3.10 A, B). Chaetae include capillaries, lyrate chaetae, and sometimes few inconspicuous spines, blunt or bifurcated among capillaries of chaetigers 1 to 2, representing homologues of lyrate chaetae found on following chaetigers; large conspicuous spines absent; large conspicuous spines absent. Pygidium with multiple lobes (Fig. 7.6.3.10 A). Remarks: This genus and species was originally misconstrued by Blake (1972) as belonging to scalibregmatids having acicular spines in anterior parapodia. A re-­examination of prepared slides from the type collection of C. baffinensis confirms that these spines on chaetigers 1 to 2 are actually the small spinous chaetae that are now considered homologues of the lyrate chaetae that begin on chaetiger 3 (Blake 2015). This is similar to the findings of Mackie (1991), who noted that the small acicular spines of S. stenocerum Bertelsen and Weston were of the same type as in S. inflatum and transferred that species to Scalibregma. Cryptosclerocheilus baffinensis was erroneously referred to the genus Polyphysia by Jirkov (2001). C.  ­baffinensis, with an elongate and arenicoliform body and an expanded anterior region (Fig. 7.6.3.10 A), differs fundamentally from Polyphysia, which has a short, maggot-shaped body with no expanded anterior region (Fig. 7.6.3.1 B); furthermore, the prostomium of C. baffinensis is T-shaped (Fig. 7.6.3.10 A, B), whereas that of P. crassa bears two short frontal horns that are mostly hidden by the prostomium. C. baffinensis is actually most closely related to species of Scalibregma in overall body shape, the T-shaped prostomium, and presence of branchiae, differing in the absence of dorsal and ventral cirri. A single species is known. 1. Cryptosclerocheilus baffinensis Blake, 1972. Baffin Bay off eastern Canada, in deep-water muds, 1830 m Hyboscolex Schmarda, 1861 Type species: Hyboscolex longiseta Schmarda, 1861, by monotypy (nine species) Diagnosis: Body elongate, arenicoliform. Prostomium with frontal horns (Fig.  7.6.3.10 C, F); eyes present or absent. Parapodia of posterior segments without dorsal

or ventral cirri (Fig. 7.6.3.10 C); interramal papillae or cilia present (Fig.  7.6.3.10 D); postchaetal lamellae absent. Branchiae absent. Chaetae include capillaries, lyrate chaetae, and sometimes few inconspicuous spines, blunt or bifurcated among capillaries of chaetigers 1 to 2, representing homologues of lyrate chaetae found on following chaetigers; large conspicuous spines absent. Pygidium with long anal cirri (Fig. 7.6.3.10 E, G). Remarks: Nine species of Hyboscolex are recorded in the WoRMS database (accessed 16 November 2015); most are from shallow water and based on old records and are poorly known. The best known and most widely distributed species is Hyboscolex pacificus (Moore, 1909) (Fig.  7.6.3.10 C–E). Only three species have been described since 1980. H. equatorialis from western South America is illustrated (Fig.  7.6.3.10 F–H). The following list of valid species is taken from WoRMS (accessed 16 November 2015). 1. Hyboscolex dicranochaetus (Schmarda, 1861). Australia, NSW and Victoria, low water 2. Hyboscolex equatorialis Blake, 1981. Ecuador and Peru, intertidal to shallow subtidal 3. Hyboscolex homochaetus (Schmarda, 1861). New Zealand, in mud 4. Hyboscolex longiseta Schmarda, 1861, South Africa 5. Hyboscolex oculatus (Ehlers, 1901). Southern Chile, intertidal 6. Hyboscolex pacificus (Moore, 1909). Widespread: Northeastern Pacific; Northwestern Pacific, subtidal, in rocks 7. Hyboscolex quadricincta Kudenov, 1985. Florida, northeast Gulf of Mexico, shallow subtidal 8. Hyboscolex reticulatus (McIntosh, 1885). New Zealand, deep water 9. Hyboscolex verrucosa Hartmann-Schröder, 1979, Australia, northwest coast, shallow water Lipobranchius Cunningham and Ramage, 1888 Type species: Lipobranchius jeffreysii (McIntosh, 1869). Designated by Cunningham and Ramage (1888) (one species) Diagnosis: Same as for Polyphysia except branchiae are absent. Remarks: As discussed above, a single species, L. jeffreysii (Fig.  7.6.3.12 A, D) is retained and separated from P. crassa because branchiae are absent. 1. Lipobranchius jeffreysii (McIntosh, 1869). Widespread in northern European waters, shelf depths Oligobregma Kudenov and Blake, 1978 Type species: Pseudoscalibregma aciculata Hartman, 1965. Designated by Kudenov and Blake (1978) (ten species)



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Fig. 7.6.3.10: Examples of species of Cryptosclerocheilus and Hyboscolex. A, B, C. baffinensis: A, entire worm, dorsal view; B, anterior end, ventral view. C–E, H. pacificus: C, anterior end, dorsal view; D, parapodium from middle of body, anterior view; E, posterior end, lateral view. F–H, H. equatorialis: F, anterior end, dorsal view; G, posterior end, dorsolateral view; H, lyrate chaeta. A, B, from Blake (1972); C–E, after Imajima (1961); F–H, from Blake (1981). Abbreviations: aC, anal cirrus; br, branchiae; frH, frontal horn; lL, lower lip of mouth; intP, interramal papilla; per, peristomium; pr, prostomium; Seg 1, segment 1; uL, upper lip of mouth; vG, ventral groove.

Diagnosis: Body elongate and arenicoliform. Prostomium T-shaped with two prominent frontal horns (Fig. 7.6.3.11 A, B, D, E); eyes present or absent; nuchal organs present. Peristomium achaetous, surrounding prostomium dorsally

and forming upper and lower lips of mouth ventrally (Fig.  7.6.3.11 E). Branchiae absent. Parapodia with well-­ developed dorsal and ventral cirri (Fig.  7.6.3.11 F,  G); interramal papilla present (Fig.  7.6.3.11 F) or absent. ­

336 

 7.6 Opheliida/Capitellida



Large acicular spines present on anterior chaetigers (Figs.  7.6.3.5  M and 7.6.3.11 C). Capillaries present in all parapodia; lyrate chaetae present anterior to capillaries of chaetigers 2, 3, or 4; some species with short, slender, blunt, or pointed spinous chaetae anterior to capillaries of chaetigers 1, 2, or 3, representing homologues of lyrate chaetae found on following chaetigers. Pygidium with five or more anal cirri. Remarks: Ten species are known and listed below. Eight species are from the deep sea. Seven species are from Antarctic seas; only two species are known from the northern hemisphere. O. hartmanae Blake, 1981 was transferred to Pseudoscalibregma by Blake (2015). Tubular-shaped glands similar to those now known from species of Scalibregma and Pseudoscalibregma were reported by Blake (2015) from the dorsal and ventral cirri for O. mucronata. In O. mucronata, these glands are few in number and exit via the nipplelike tip of the cirrus. The following list of valid species is taken from WoRMS (accessed 16 November 2015) and as updated based on recent literature: 1. Oligobregma aciculata (Hartman, 1965). Western North Atlantic, in abyssal depths, 4850 m 2. Oligobregma blakei Schuller and Hilbig, 2007. Antarctica, Scotia Sea, 2889 to 2892 m. Juvenile, possibly belongs to a different genus 3. Oligobregma collare (Levenstein, 1975). Antarctic and subantarctic seas, 1622 to 6070 m 4. Oligobregma lonchochaeta Detinova, 1985. North Atlantic, Reykjanes Ridge 5. Oligobregma mucronata Blake, 2015. East Antarctic Peninsula, 323 to 912 m 6. Oligobregma notiale Blake, 1981. Widespread in Antarctica, 18 to 923 m 7. Oligobregma oculata Kudenov and Blake, 1978. South of New Caledonia, 57 m 8. Oligobregma pseudocollare Schüller and Hilbig, 2007. Antarctica, Scotia and Weddell Seas, 753 to 3050 m 9. Oligobregma quadrispinosa Schüller and Hilbig, 2007. Antarctica, Scotia and Weddell Seas, 2258 to 4069 m 10. Oligobregma simplex Kudenov and Blake, 1978. Australia, Western Port Bay, Victoria, 11 m Parasclerocheilus Fauvel, 1928 Type species: Parasclerocheilus branchiatus Fauvel, 1928, by monotypy (two species)

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 337

Diagnosis: Body elongate, arenicoliform. Prostomium T-shaped with frontal lobes; eyes present. Peristomium achaetous. Branchiae from chaetigers 2 to 7. Segments after first few with four annulae. Parapodia biramous, dorsal cirri absent; ventral cirri present; interramal sense organ or papilla present. Acicular notochaetae on first one to four chaetigers. Chaetae include capillaries, curved spinous chaetae, and lyrate chaetae. Remarks: With six pairs of branchiae, the two species of Parasclerocheilus are the only scalibregmatids known to have more than four pairs. Parasclerocheilus is similar to Sclerocheilus in having notopodial acicular spines on a few anterior parapodia and a ventral cirrus in posterior parapodia; a dorsal cirrus is absent. The difference between the two genera is that Parasclerocheilus has branchiae on chaetigers 2 to 7, whereas Sclerocheilus lacks them. There are two species, both from shallow water. The following list of valid species is taken from WoRMS (accessed 16 November 2015). 1. Parasclerocheilus branchiatus Fauvel, 1928. India, Gulf of Mannar, shallow water 2. Parasclerocheilus capensis Day, 1961. South Africa, intertidal on rocky shores Polyphysia Quatrefages, 1865 Type species: Eumenia crassa Örsted, 1843. Fide Furreg (1925) Synonyms: Eumenia Örsted, 1843 (homonym, preoccupied by Eumenia Godard, 1824 in the Lepidoptera) (three species) Diagnosis: Body short, swollen, maggot-shaped, with no more than 35 segments (Fig. 7.6.3.1 B). Prostomium bilobed, but not T-shaped; with two short frontal horns (Fig. 7.6.3.12 B); eyes absent; nuchal organs narrow slits. Peristomium achaetous. Body segments each with three annuli. Parapodia biramous with two cushion-shaped podial lobes; lateral sensory organs present; dorsal and ventral cirri absent. Branchiae present on segments 2 to 5 (Fig. 7.6.3.12 B). Chaetae include capillaries and lyrate chaetae (Fig. 7.6.3.12 C), no acicular spines. Pygidium without anal cirri. Remarks: Støp-Bowitz (1945) synonymized the monotypic genus and species L. jeffreysii with P. crassa because he was convinced that the former was a juvenile of the latter in which branchiae had not yet developed. This proposed synonymy has been both supported and rejected by different authors over the years. Wesenberg-Lund (1950: 37) wrote concerning a specimen 26 mm long that

◂ Fig. 7.6.3.11: Examples of species of Oligobregma. A, O. notiale, dorsal view; B, C, O. aciculata: B, anterior end, dorsal view; C, acicular chaetae; D–G, O. mucronata: D, anterior end, dorsal view; E, same, ventral view; F, posterior parapodium, anterior view; G, detail of dorsal cirrus and internal tubular glands. A, from Blake (1981); B, C, after Hartman (1965); D–G, from Blake (2015). Abbreviations: acS, acicular spines; dC, dorsal cirrus; frH, frontal horn; intP, interramal papilla; lL, lower lip of mouth; per, peristomium; pr, prostomium; uL, upper lip of mouth; vC, ventral cirrus; vG, ventral groove.

338 

 7.6 Opheliida/Capitellida

Fig. 7.6.3.12: Examples of species of Polyphysia and Lipobranchius. A, L. jeffreysii, entire worm in right lateral view, showing overall shape; B, C, P. crassa, B, anterior end, left lateral view; C, lyrate chaeta; D, L. jeffreysii, anterior end frontolateral view. A, after Cunningham and Ramage (1888); B, C, after Hartmann-Schröder (1996); D, after Wesenberg-Lund (1950). Abbreviations: br, branchiae; frH, frontal horns.

lacked branchiae and that she identified as L. jeffreysii: “The present species should in no way be considered a juvenile form of Eumenia crassa; in my opinion, it is a species closely related to—but not synonymous with— the latter.” In contrast, Clark and Dawson (1963: 647) wrote “Clearly the presence or absence of gills cannot be regarded as a character of taxonomic significance in these scalibremids [sic].” Hartmann-Schröder (1971, 1996) kept the two species (and genera) separate. Clearly, the issue is not resolved and it may take DNA sequencing to provide a definitive answer. However, the large 26-mm abranchiate specimen illustrated by Wesenberg-Lund (1950) for L. jeffreysii (Fig. 7.6.3.12 D) is well over the size (ca. 4 mm) for branchial development suggested by Blake (2015) that is needed to distinguish between abranchiate juveniles and branchiate adult specimens of Scalibregma australis. For this chapter, Lipobranchius is kept separate until further assessments of larger collections can be made. It is very apparent that this discussion of two species in two different genera (Polyphysia/Lipobranchius) can also be applied to discussions of other generic pairs that have and lack branchiae: Scalibregma/ Pseudoscalibregma, Parasclerocheilus/Sclerocheilus, and Sclerobregma/Oligobregma. This emphasizes problems associated with the present arrangement of genera. The following list of valid species is taken from WoRMS (accessed 16 November 2015): 1. Polyphysia caulleryi (McIntosh, 1922). Japan, 48 m 2. Polyphysia crassa (Örsted, 1843). Widespread in Arctic and European waters, intertidal to shallow subtidal 3. Polyphysia hystricis, P (McIntosh, 1922). Off England, Porcupine slope, 470 to 1207 m

Pseudoscalibregma Ashworth, 1901 Type species: Scalibregma parvum Hansen, 1879. Designated by Ashworth (1901) (eight species) Diagnosis: Body elongate, arenicoliform (Fig. 7.6.3.13 A). Prostomium T-shaped with frontal horns (Fig. 7.6.3.13 C, F). prostomium Peristomium a single ring, encompassing ­ dorsally (Figs. 7.6.3.2 D and 7.6.3.13 F) and ventrally forming upper lip of mouth (Fig. 7.6.3.3 F); lower lip of mouth formed from elements of peristomium and chaetiger 1. Parapodia of posterior segments with dorsal and ventral cirri (Fig.  7.6.3.13 B, D); interramal papillae present (Fig.  7.6.3.13 B); postchaetal lamellae absent. Branchiae absent. Chaetae include capillaries, lyrate chaetae, and sometimes few inconspicuous spinous chaetae among capillaries of chaetigers 1 to 2 (Fig. 7.6.3.5 C), blunt, pointed, or bifurcated, representing homologues of lyrate chaetae found on following chaetigers (Fig. 7.6.3.13 E); large conspicuous spines absent. Pygidium with long anal cirri. Remarks: Apart from a more diverse morphology of dorsal and ventral cirri, the only character that separates Pseudoscalibregma from Scalibregma is the absence of branchiae. The presence of short spinous chaetae in the first one to two chaetigers as occurs in species of Scalibregma was confirmed by Imajima (2009), Bakken et al. (2014), and Blake (2015) for several species. Pseudoscalibregma currently includes eight species, all from the deep sea in upper slope to abyssal depths. Five species are from Antarctic seas, one from the North Pacific, one from the eastern North Atlantic and Arctic, and another from an abyssal trench in the Pacific. The best known species are P. parvum, redescribed by Bakken et al. (2014) and P. bransfieldium redescribed by



7.6.3 Scalibregmatidae Malmgren, 1867 

 339

Fig. 7.6.3.13: Examples of species of Pseudoscalibregma. A, B, P. parvum: A, entire animal in dorsolateral view; B, posterior parapodium, posterior view. C–E, P. bransfieldium: C, anterior end, dorsal view; D, posterior parapodium, anterior view; E, lyrate chaeta. F, P. palmeri, anterior end, dorsal view. A, after Støp-Bowitz (1945); B, after Bakken et al. (2014); C, E, from Blake (1981); D, from Blake (2015); F, from Blake (2015). Abbreviations: dC, dorsal cirrus; frH, frontal horn; per, peristomium, pr, prostomium; vC, ventral cirrus.

Blake  (1981,  2015). The following list of valid species is taken from WoRMS (accessed 16 November 2015) and as updated with recent literature: 1. Pseudoscalibregma bransfieldium (Hartman, 1967). Antarctica, 332 to 916 m 2. Pseudoscalibregma hartmanae (Blake, 1981). Antarctica, Weddell Sea, shelf and slope depths. Fide Blake (2015) 3. Pseudoscalibregma orientalis Imajima, 2009. Offshore northern Japan, 373 to 1005 m 4. Pseudoscalibregma pallens Levenstein, 1962. Pacific Ocean, Kermadec Trench, 8928 to 9174 m 5. Pseudoscalibregma palmeri Blake, 2015. East Antarctic Peninsula, 385 to 768 m 6. Pseudoscalibregma papilia Schüller, 2008. ­Antarctica, Weddell Sea, Drake Passage, 1970 to 3690 m 7. Pseudoscalibregma parvum (Hansen, 1879). Arctic and subarctic locations, East Greenland, Jan Mayen, Spitsbergen, Norwegian Sea, Kara Sea, 20 to 1715 m 8. Pseudoscalibregma usarpium Blake, 1981. Antarctica, Ross Sea, 2100 m

Scalibregma Rathke, 1843 Type species: Scalibregma inflatum Rathke, 1843, by monotypy Synonyms: Oligobranchus Sars, 1846. Fide Hartman, 1959 (eight species) Diagnosis: Body elongate, arenicoliform, expanded anteriorly (Fig.  7.6.3.3 A). Prostomium T-shaped with lateral horns (Figs. 7.6.3.2 A, 7.6.3.3 B, and 7.6.3.8 A). Parapodia of posterior segments with dorsal and ventral cirri; interramal papillae or cilia present; postchaetal lamellae absent. Branchiae present from chaetiger 2, up to four pairs (Fig.  7.6.3.3 B, 7.6.3.4 A, and 7.6.3.8 A). Chaetae include capillaries, lyrate chaetae (Fig. 7.6.3.5 N), and sometimes few blunt or bifurcated inconspicuous spines among capillaries of chaetigers 1 to 2 (Fig. 7.6.3.5 A, B), representing homologues of lyrate chaetae found on the following chaetigers; large acicular spines absent. Pygidium with long anal cirri (Fig. 7.6.3.4 J). Remarks: Scalibregma inflatum has historically been considered cosmopolitan in distribution and indeed there are numerous records of this species globally.

340 

 7.6 Opheliida/Capitellida

However, Mackie (1991) demonstrated sufficient variability in European populations to define another closely related species. Mackie (1991) discovered that slender spines were present among the capillaries of a few anterior notopodia. Prior to his study, Scalibregma had been defined as lacking acicular chaetae. The chaetae observed by Mackie were not the large, curved spines that have been reported for species of Asclerocheilus, Oligobregma, Parasclerocheilus, Sclerobregma, and Sclerocheilus but were instead inconspicuous companions of the capillaries. For S. inflatum, Mackie (1991) found that some of these chaetae were forked or split on their tips. This observation plus the position of these chaetae in the chaetal fascicles anterior to the capillaries suggested that they were homologous to the lyrate chaetae of the following segments. Mackie further suggested that the larger recurved spines of other genera were homologous with capillaries. Mackie (1991) redescribed S. inflatum based on specimens from the type locality in Norway as well as specimens from Sweden, Scotland, Wales, and Ireland. A second species, S. celticum, was newly described from Scotland, Wales, and France, and differed from S. inflatum in that the small anterior notopodial spines of chaetigers 1 to 2 were blunt-tipped instead of bifurcate, eyes were present instead of absent, an expanded peristomium obscured portions of the prostomium instead of leaving it exposed, smaller epidermal pads were present above the notopodia, and there were differences in the number and arrangement of the pygidial cirri. S. celticum has since been reported from the Mediterranean by Çinar (2005) and Lomiri et al. (2012). Mackie (1991) also re-examined the two known species of Sclerobregma, S. branchiata Hartman and S. stenocerum Bertelsen and Weston, and referred the latter species to Scalibregma because the anterior acicular spines were of the inconspicuous form found in the two species of Scalibregma he had studied. S. branchiata, however, had large, curved spines and was not transferred to Scalibregma. Subsequent to Mackie’s work, additional species of Scalibregma were described by Blake (2000a, 2015) from California and Antarctica, respectively, and by Bakken et al. (2014) from Norwegian waters. It is likely that additional species will be identified as well. The genus Scalibregma currently includes eight recognized species (WoRMS, accessed 16 November 2015). Of these, Scalibregma robustum Zachs (1923, 1925) and Scalibregma wireni Furreg (1925) are two poorly known Arctic–Subarctic species that have rarely been reported since their original descriptions and should be compared using additional characters now in use. However, because the dorsal and ventral cirri of both species are weakly

developed and asymmetrical with a broad basal attachment and are unlike those of other species of the genus (Furreg 1925), they may represent one (or two?) valid species. Wirén (1883) described the polychaetes from the Vega Expedition to the Siberian Arctic and Bering Sea in 1878 to 1879 and identified and named some specimens from the Siberian Arctic and Chukchi Seas as Eumenia crassa forma arctica. These same specimens were examined by Furreg (1925) and described by him as Scalibregma vegae Furreg, a new species with Wirén’s forma or subspecies referred to synonymy. However, in WoRMS (accessed 16 November 2015), Wiren’s forma arctica is erroneously referred to synonymy with S. inflatum, with Furreg (1925) cited as the authority. Annenkova (1937) referred S. vegae to synonymy with S. robustum based on an earlier publication date (May vs. July) by Zachs (1925); the WoRMS database gives Zachs (1923) as the actual date of publication (WoRMS accessed 16 November 2015). However, because Wirén’s forma arctica is of subspecific rank and is a trinomial, it is available as a full species if elevated to that rank. This is expressly stated in Article 45.6.4 of the current International Code of Zoological Nomenclature (ICZN 1999) for such names established prior to 1961. This is justified because both Wirén (1883) and Furreg (1925) examined exactly the same specimens and their two descriptions emphasize the same characters, albeit Furreg’s description is more detailed and well-­ illustrated. Therefore, Wirén’s subspecies or forma name “arctica” is here elevated to full species status with both S. vegae and S. robustum reduced to junior synonyms. The following eight species of Scalibregma are currently considered valid. The most recently described species are S. hanseni by Bakken et al. (2014) and S. ­australis by Blake (2015). Given the numerous widespread records of specimens referred to S. inflatum, the number of species is likely to increase once additional collections are closely examined. 1. Scalibregma arctica (Wirén, 1883) New status, Siberian Arctic, Laptev Sea; Chukchi Sea, shelf depths a. Scalibregma vegae Furreg, 1925, same distribution as S. arctica. New synonymy b. Scalibregma robusta Zachs, 1923, White Sea, Sea of Okhotsk, shelf depths. New synonymy 2. Scalibregma australis Blake, 2015, Antarctica, widespread in shelf depths 3. Scalibregma californicum Blake, 2000a, California, offshore in shelf and slope depths 4. Scalibregma celticum Mackie, 1991, United Kingdom, coast of France, Mediterranean, shallow subtidal 5. Scalibregma hanseni Bakken, Oug and Kongsrud, 2014, Norwegian Sea, shelf and slope depths



6. Scalibregma inflatum Rathke, 1843, widespread in the North Atlantic, shelf depths; reported globally 7. Scalibregma stenocerum (Bertelsen and Weston 1980), southeastern United States in shelf depths 8. Scalibregma wireni Furreg, 1925, East Greenland, Kaiser Franz-Joseph Fjord; 3 to 9 m deep; mud with sand and algae Scalibregmella Hartman and Fauchald, 1971 Type species: Scalibregmella antennata Hartman and Fauchald, 1971, by monotypy (one species) Diagnosis (emended): Body elongate, weakly fusiform; anterior segments smooth in smaller specimens (