The Evolution and Fossil Record of Parasitism: Coevolution and Paleoparasitological Techniques (Topics in Geobiology, 50) 3030522326, 9783030522322

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Topics in Geobiology 50

Kenneth De Baets John Warren Huntley   Editors

The Evolution and Fossil Record of Parasitism Coevolution and Paleoparasitological Techniques

Topics in Geobiology Volume 50

Series Editors Neil H. Landman, Department of Paleontology, American Museum of Natural History, New York, NY, USA Peter J. Harries, Department of Marine, Earth and Atmospheric Sciences, North Carolina State University, Raleigh, NC, USA

The Topics in Geobiology series covers the broad discipline of geobiology that is devoted to documenting life history of the Earth. A critical theme inherent in addressing this issue and one that is at the heart of the series is the interplay between the history of life and the changing environment. The series aims for high quality, scholarly volumes of original research as well as broad reviews. Geobiology remains a vibrant as well as a rapidly advancing and dynamic field. Given this field’s multidiscipline nature, it treats a broad spectrum of geologic, biologic, and geochemical themes all focused on documenting and understanding the fossil record and what it reveals about the evolutionary history of life. The Topics in Geobiology series was initiated to delve into how these numerous facets have influenced and controlled life on Earth. Recent volumes have showcased specific taxonomic groups, major themes in the discipline, as well as approaches to improving our understanding of how life has evolved. Taxonomic volumes focus on the biology and paleobiology of organisms – their ecology and mode of life – and, in addition, the fossil record – their phylogeny and evolutionary patterns – as well as their distribution in time and space. Theme-based volumes, such as predator-prey relationships, biomineralization, paleobiogeography, and approaches to high-resolution stratigraphy, cover specific topics and how important elements are manifested in a wide range of organisms and how those dynamics have changed through the evolutionary history of life. Comments or suggestions for future volumes are welcomed. Neil H.  Landman Department of Paleontology American Museum of Natural History New York, USA E-mail: [email protected] Peter J. Harries Department of Marine, Earth and Atmospheric Sciences North Carolina State University Raleigh, USA E-mail: [email protected] More information about this series at http://www.springer.com/series/6623

Kenneth De Baets  •  John Warren Huntley Editors

The Evolution and Fossil Record of Parasitism Coevolution and Paleoparasitological Techniques

Editors Kenneth De Baets GeoZentrum Nordbayern Friedrich-Alexander University Erlangen-Nürnberg Erlangen, Germany

John Warren Huntley Department of Geological Sciences University of Missouri Columbia, MO, USA

ISSN 0275-0120 Topics in Geobiology ISBN 978-3-030-52232-2    ISBN 978-3-030-52233-9 (eBook) https://doi.org/10.1007/978-3-030-52233-9 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Foreword

The word “parasites” triggers annoyance at best but also strikes deep fear in many. But for their scholars, the intellectual and utilitarian rewards of studying parasites are rich. Every 30–100 years or so, Homo sapiens are struck by a pandemic, usually caused by a viral or bacterial parasite. As I write this, many of us have been working from home and constrained to a much-smaller-than-usual visiting radius for more than a year; and the towns and cities in which we live have gone through several cycles and variants of lockdowns, all to prevent SARS-CoV-2, a viral parasite, from removing too many of us prematurely. The tiny SARS-CoV-2 (to the best of current knowledge its genome is about 30 kB, smallish, even by viral standards) has induced behavioral changes in many human populations, and genetic signatures of our bodies dealing with the virus will surely be detectable at least in some of our populations down the road. And although it has wreaked havoc on our social lives and work routines, it thankfully did not stop colleagues from working on this second volume of The Evolution and Fossil Record of Parasitism. Parasites are ubiquitous, ecologically and phylogenetically. They affect literally every branch of life and are found nearly in any species in which we bother to look for them (and logically so). There are, by some estimates, more parasitic species than non-parasitic ones. Hence, parasites are at once products of and drivers of evolution, just as are predators, competitors, and symbionts. While there is an understandably huge societal investment in investigating the mechanisms of diseases (many caused by parasites) and their treatments and cures in humans and their livestock, understanding the evolutionary history of parasitism of other, diverse organisms is regretfully and disproportionately neglected. This volume ameliorates this neglect by presenting an eclectic collection of intriguing studies of parasitism and their broader phylogenetic, spatial and temporal patterns, mainly from the vantage point of the fossil record. Many questions are begging for answers. Is parasitism as old as life? How do Red Queen dynamics play out between parasites and their hosts over shorter and longer (geological) time scales? How and when do parasites switch hosts and what are the long-term evolutionary consequences of host-switching? What are the v

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Foreword

population consequences of parasitic infestations and do these consequences scale up to macroevolutionary patterns? What happens when multiple parasite species compete for the same host individual or species? How does a changing (paleo)environmental backdrop influence host-parasite coevolution? The answering of these questions adequately will benefit from collaboration between parasitologists, paleontologists, pathologists, epidemiologists, statisticians, evolutionary biologists, ecologists, and surely many other specialists, which this volume demonstrates and inspires. Parasites are usually small and may or may not leave detectable marks on their fossilized victims (think SARS-CoV-2!). Even potentially detectable marks and traces may be masked by taphonomic processes, but windows of exceptional preservation can leave a remarkable amount of information for both fossilized host and parasite. Time can also erase much evidence of parasitism, not just those remaining in fossils but also those left (as genetic signatures or phenotypic signatures) in the host’s and parasite’s living descendants. Yet, with enough comparative knowledge based on related organisms, substantial sample sizes, extant analogues for fossil systems, and a solid understanding of phenotypic variation among “healthy” organisms, much can be inferred by paleontological detectives of parasitism, especially when disparate approaches are embraced. Some things are clear: parasitism is a vitally important biological process and it is understudied in the fossil record. I am sure this superb volume will enthuse many to (continue to) collect data and develop new tools and methods in order to understand the ecology and evolution of parasites and their hosts, both living and long dead. 29 April 2021 Natural History Museum University of Oslo Oslo, Norway

Lee Hsiang Liow

Contents

1 The Fossil Record of Parasitism: Its Extent and Taphonomic Constraints������������������������������������������������������������������������������������������������    1 Kenneth De Baets, John Warren Huntley, Adiël A. Klompmaker, James D. Schiffbauer, and A. D. Muscente 2 Importance of Data on Fossil Symbioses for Parasite–Host Evolution��������������������������������������������������������������������������������������������������   51 Ninon Robin 3 Biodiversity and Host–Parasite (Co)Extinction������������������������������������   75 Jeroen van Dijk and Kenneth De Baets 4 Evolutionary History of Colonial Organisms as Hosts and Parasites��������������������������������������������������������������������������������������������   99 Olev Vinn and Mark A. Wilson 5 Crustaceans as Hosts of Parasites Throughout the Phanerozoic��������  121 A. A. Klompmaker, C. M. Robins, R. W. Portell, and A. De Angeli 6 Trilobites as Hosts for Parasites: From Paleopathologies to Etiologies����������������������������������������������������������������������������������������������  173 Kenneth De Baets, Petr Budil, Oldřich Fatka, and Gerd Geyer 7 Evolutionary History of Cephalopod Pathologies Linked with Parasitism����������������������������������������������������������������������������  203 Kenneth De Baets, René Hoffmann, and Aleksandr Mironenko 8 Bivalve Mollusks as Hosts in the Fossil Record������������������������������������  251 John Warren Huntley, Kenneth De Baets, Daniele Scarponi, Liane Christine Linehan, Y. Ranjeev Epa, Gabriel S. Jacobs, and Jonathan A. Todd

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  9 Parasitism of Paleozoic Crinoids and Related Stalked Echinoderms: Paleopathology, Ichnology, Coevolution, and Evolutionary Paleoecology��������������������������������������������������������������  289 James R. Thomka and Carlton E. Brett 10 Deep Origin of Parasitic Disease in Vertebrates�����������������������������������  317 Valerie Watson and Bruce Rothschild 11 Gastrointestinal Parasites of Ancient Nonhuman Vertebrates: Evidence from Coprolites and Other Materials��������������  359 Karen Chin 12 Blood to Molecules: The Fossil Record of Blood and Its Constituents ��������������������������������������������������������������������������������  377 Dale Greenwalt 13 The Molecular Clock as a Tool for Understanding Host-Parasite Evolution��������������������������������������������������������������������������  417 Rachel C. M. Warnock and Jan Engelstädter 14 Horizontal Transfer of Transposons as Genomic Fossils of Host-Parasite Interactions������������������������������������������������������  451 Alexander Suh Index������������������������������������������������������������������������������������������������������������������  465

Chapter 1

The Fossil Record of Parasitism: Its Extent and Taphonomic Constraints Kenneth De Baets, John Warren Huntley, Adiël A. Klompmaker, James D. Schiffbauer, and A. D. Muscente Abstract  The fossil record of parasites is limited thus far. A survey of the fossil record shows that some modes of preservation show a higher potential for the preservation of parasitic remains or parasite–host associations than generally recognized. A better understanding of the taphonomy of parasites is critical to better predict their preservation potential and, together with new techniques like computed tomography, can open the door for systematic screening of parasite sources in deep time. Phosphatization seems particularly fruitful to characterize anatomical details for microscopic parasites or pathogens. Amber deposits are rich in terrestrial parasitic ecdysozoans and their pathogens, but their extent does not bracket a single mass extinction. For particular parasite–host associations, preservation of direct evidence is unlikely, but traces they leave in skeletons and other host remains can be used to trace them back to the Mesozoic or even the Paleozoic. Vertebrate coprolites

K. De Baets () Fachgruppe PaläoUmwelt, GeoZentrum Nordbayern, Friedrich-Alexander University Erlangen-Nürnberg, Erlangen, Germany e-mail: [email protected] J. W. Huntley Department of Geological Sciences, University of Missouri, Columbia, MO, USA A. A. Klompmaker Department of Museum Research and Collections & Alabama Museum of Natural History, University of Alabama, Tuscaloosa, AL, USA Department of Integrative Biology & Museum of Paleontology, University of California Berkeley, Berkeley, CA, USA J. D. Schiffbauer Department of Geological Sciences, University of Missouri, Columbia, MO, USA X-Ray Microanalysis Core Facility, University of Missouri, Columbia, MO, USA A. D. Muscente Department of Geology, Cornell College, Mount Vernon, IA, USA Department of Geological Sciences, Jackson School of Geoscience, The University of Texas at Austin, Austin, TX, USA

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 K. De Baets, J. W. Huntley (eds.), The Evolution and Fossil Record of Parasitism, Topics in Geobiology 50, https://doi.org/10.1007/978-3-030-52233-9_1

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have yielded remains of endoparasites as far back as the Carboniferous, but a more systematic screening of coprolites is necessary to make them a successful source of parasitic remains as for the Quaternary. Parasites with preservable hard parts and/or characteristic pathologies have the best potential to track changes in marine disease prevalence in high resolution across extinction or environmental perturbations  in deep time, but more studies need to report their sample sizes and prevalences. Keywords  Parasite–host interactions · Evolution · Ecology · Pathogens · Taphonomy

1.1  Introduction Parasitism is a ubiquitous life mode throughout the evolutionary tree (Littlewood 2005; Bass et al. 2015) that has originated at least 200 times within the animal kingdom alone (Weinstein and Kuris 2016). Even so, the role of parasitism as a driving force of evolution and ecological structure has received little attention. Parasites have been implicated in the evolution of sex (Ebert and Hamilton 1996) as well as food web complexity (Dunne et al. 2013). Complex life cycle parasites may stabilize ecosystems (Hudson et  al. 2006; Lafferty et  al. 2008; Mouritsen and Poulin 2005, 2002), with the possible exception during rapid environmental perturbations and/or mass extinctions (Seilacher et al. 2007; Rudolf and Lafferty 2011; Strona and Lafferty 2016; Carlson et al. 2017; Van Dijk and De Baets 2021). Parasitism may also promote evolutionary success in the Metazoa as measured by diversification and species numbers among phyla (Jezkova et al. 2017). Unfortunately, most parasites have no preservable hard parts, which, together with their small size and residence within their hosts, strongly limit their fossilization potential (Littlewood and Donovan 2003). Their evolutionary history has, therefore, often been inferred from their host associations in modern times, which might lead to circular arguments regarding their (co)evolution with their hosts (De Baets and Littlewood 2015; Warnock and Engelstädter 2021). Coevolution has often been assumed and tested based on a direct mirroring of phylogenies of parasites and their hosts (Page 2003; Martínez-Aquino 2016). However, co-phylogeny does not necessarily reflect coevolution (Poisot 2015) and various instances can lead to false congruence or incongruence including host or parasite extinction (e.g., Van Dijk and De Baets 2021), intrahost specification, and failure of a parasite to speciate in response to host speciation (Poulin 2011). Parasites can not only evolve independently of their hosts, but they can also switch hosts. Host switching requires that the organisms occur together and are anatomically, ecologically, and physiologically compatible (Leung 2021). The fossil record contains direct evidence of ancient parasites, their host associations, and disease (Littlewood and Donovan 2003; Leung 2017, 2021; De Baets

1  The Fossil Record of Parasitism: Its Extent and Taphonomic Constraints

3

et al. 2021b). Identifying ancient remains of parasites presents a number of challenges, as the organisms might have possessed traits not found in modern analogues or their free-living relatives (Nagler and Haug 2015; De Baets and Littlewood 2015). In addition, convergent evolution may result in losses of traits that may make ancient taxa appear superficially similar to modern symbionts with similar feeding requirements. Parasite lineages have converged over evolutionary time to share or lose traits and exploit their hosts in similar ways. In some cases, such convergence has led to extreme loss of morphological complexity and genetic makeup (Zarowiecki and Berriman 2015; Sundberg and Pulkkinen 2015; Poulin and Randhawa 2015), particularly in orthonectids and Myxozoa (Giribet 2016; Okamura and Gruhl 2016, 2015, 2021; Mikhailov Kirill et al. 2016), which have historically even been confused with unicellular organisms. Phylogenetic approaches help to disentangle the evolutionary relationships of extant parasites with convergent morphology character sets. Nevertheless, the study of DNA in deep time is limited by its rapid decay (Sidow et al. 1991; Allentoft et al. 2012; Muscente et al. 2017a; Greenwalt 2021). Other compounds like proteins might survive longer (Briggs and Summons 2014). Aside from their DNA, proteins secreted by parasites during life or antibodies produced by the host against the parasite have been convincingly reported from the archeological record (Greenwalt 2021), but not from the deep fossil record (De Baets and Littlewood 2015). Porphyrins could however be used to demonstrate blood remains in an Eocene mosquito (Greenwalt et al. 2013; Greenwalt 2021). Although the amount of evidence for parasitism in the fossil record has greatly increased over the last few decades (Conway Morris 1981; De Baets and Littlewood 2015; Leung 2017), it is only rarely considered in evolutionary parasitology (Schmid-Hempel 2011)—the integrated study of infections, immunology, ecology, and genetics—and in paleoparasitology. So far paleoparasitological research has largely focused on archeological finds, but integrating fossil evidence could advance both of these disciplines (Dittmar 2009; Dittmar et  al. 2012) and help build an understanding of the evolution of parasitism over longer, evolutionary timescales rather than ecological timescales (De Baets and Littlewood 2015). Nonetheless, testing evolutionary hypotheses in deep time requires not just a robust phylogenetic tree of parasite and host affinities, but also a detailed stratigraphic framework for dating the ages of fossils and sufficient sample sizes. These prerequisites constrain the exploration of the parallel and convergent evolution of particular traits and life histories as well as testing hypotheses concerning the co-divergence, phylogenetic relationships, and diversity of parasites and their hosts.

1.2  Exceptional Fossil Windows on Parasite–Host Evolution 1.2.1  Modes of Exceptional Fossil Preservation Soft-bodied parasites, particularly those found as intact remains associated with their hosts, are generally preserved under conditions conducive to exceptional fossil preservation of non-biomineralized (“soft”) tissues and/or articulated multi-element

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skeletons. Geological deposits that contain such exceptionally preserved fossils, or Konservat-Lagerstätten (Seilacher 1970), are found throughout the geologic record but are concentrated in certain geospatial (geographic and stratigraphic) locations (Muscente et al. 2017b). Under most circumstances, non-biomineralized tissues and multi-element skeletons are rapidly degraded and disarticulated due to a number of physical, chemical, and biological processes, like decomposition and scavenging. Konservat-Lagerstätten are preserved where organisms survive these processes long enough to be transformed into rock, mineral, and/or recalcitrant material, which may endure over geologic time from their origin e.g., to the present (Muscente et al. 2017b). Exceptional fossil preservation, consequently, occurs when unusual environmental conditions develop in habitats or organisms are transported to locations where and when the setting helps to promote early mineralization, eliminate scavengers (salinity or anoxic conditions), and/or lead to rapid burial (Briggs 2007; see Table 1.1 and Fig. 1.1). There are a number of preservational pathways through which Konservat-­ Lagerstätten may be formed (e.g., Muscente et  al. 2017b)—the most relevant of which here are Ediacaran death mask preservation, Burgess Shale-type (BST) preservation, Orsten-type preservation, lithographic limestones, silicification, amber, and coprolites. Ediacaran death mask preservation is associated with the largely enigmatic, ~570–550  Ma million-year-old, macroscopic fossils of the Avalon, White Sea and Nama assemblages found in Canada, Australia, Russia, China, Namibia and the western US (Narbonne 2005). Such fossils are preserved as sandstone casts that likely formed beneath microbial masks (e.g., Gehling 1999) that led to early mineralization on the decaying carcasses. BST preservation occurs in fine-­ grained sediments deposited in aquatic settings with low dissolved oxygen levels, where the preserved fossils are carbonaceous compressions often associated with clay minerals and pyrite (Butterfield 2003; Anderson et al. 2011). The Cambrian-­ Ordovician Orsten fauna is represented worldwide by a number of sites, most famously in Sweden, where animals were preserved as microfossils through a process called phosphatization, or the precipitation of apatite minerals on and within labile tissues (Maas et al. 2006; Waloszek 2003). Lithographic limestone preservation occurs in very-fine-grained limestones deposited in stagnant, hypersaline, or anoxic and perhaps toxic bottom waters of restricted basins (Seilacher et al. 1985). Such conditions, similar to other preservational settings such as bituminous shales, promoted exceptional preservation by limiting destruction due to scavenging, bioturbation, bacterial decomposition, autolytic decay, and oxidation (Briggs and Wilby 1996). Silicification occurs when silica-rich fluids in sediments precipitate as chert. Fossil preservation can take a number of forms from cellular level preservation as silica precipitates within cells (e.g., silicified wood) to partial to complete replacement of original fossil material in the form of chert nodules. The Devonian Rhynie chert preserves plants at the cellular scale along with a number of algal, fungal and animal forms (Trewin 1993, 2001; Garwood et  al. 2020; Harper and Krings 2021). Nodules of other mineralogies can form in a variety of low-­oxygen environments in concert with bacterial degradation/mineralization. For example, the Carboniferous Mazon Creek flora and fauna are preserved in iron carbonate

Table 1.1  Ancient history of parasite-host associations as told by exceptional fossil finds and paleopathologies. This table is not exhaustive but highlights the oldest and important evidence to constrain particular parasite-host associations Higher Taxon Taxon Fossil Evidence Age Source Host Reference Environment Bacteria Poinar (2015b, T  Coccobacilli ? Direct: Miocene Amber Flea 2021) Erythrocytes (Dominican) (Atopopsyllus cionus)  Spirochaetes Palaeoborrelia Direct: Spirochete-­ Miocene Amber Amblyomma sp. Poinar (2015d, T dominicana like cells (Dominican) 2021)  Rickettsiales Palaeorickettsia Direct: Rickettsial-­ Early Cretaceous Amber Cornupalpatum Poinar (2015c, T protera like cells (Myanmar) burmanicum 2021) Eukaryota T Cretaceous Skeletal Tyrannosaurus Wolff et al.  ?Metamonada ?Parabasalia: Indirect: Erosive deformation rex (2009); Trichomonadida lesions on doubtful see mandibles Rothschild and Martin (2006), Watson and Rothschild (2021)  Gregarinasina Primigregarina Direct: Amber Cretaceous Amber Cockroaches Poinar (2012a, T burmanica (Myanmar) 2021)  Gregarinasina ? Direct: Amber Miocene Amber Springtail Poinar (2012a) T (Dominican) T Coprolite (Saint Archosaur Poinar and  Amoebozoa Entamoebites antiquus Indirect: Cyst Cretaceous (Barremian) Barbe Fm.) Boucot (2006), Poinar (2021) T Tapir polkensis McConnell  Coccidia Coccidia-type Indirect: Oocysts Miocene Lagerstätte and Zavada (Gray Fossil (2013) Site) (continued)

Eimeria lobatoi

Archeococcidia antiquus; A. nothrotheriopsae Paleohaimatus calabresi

 Coccidia

 Coccidia

Palaeoleishmania proterus

?

Paleoleishmania neotropicum

Plasmodium dominicana Vetufebrus ovatus

 Trypanosomatida

 Trypanosomatida

 Trypanosomatida

 Haemosporida

 Haemosporida

 Trypanosomatida

Paleotrypanosoma burmanicus Trypanosoma antiquus

 Trypanosomatida

 Piroplasmida

Taxon Cryptosporidium, Eimeriorina

Higher Taxon  Coccidia

Table 1.1 (continued)

Direct: Erythrocytes Direct: Erythrocytes

Direct: Erythrocytes Direct: Erythrocytes

Miocene

Miocene

Miocene

Miocene

Early Cretaceous

Miocene

Early Cretaceous

Amber (Dominican) Amber (Dominican)

Amber (Dominican) Amber (Dominican)

Amber (Myanmar) Amber (Dominican) Amber (Myanmar)

Amber (Dominican)

Miocene

Direct: Erythrocytes with piroplasms Direct: Erythrocytes Direct: Erythrocytes Direct: Erythrocytes

Coprolite

Pleistocene

Indirect: Oocysts

Poinar (2017, 2021)

Ferreira et al. (1992) Schmidt et al. (1992)

Reference Wood et al. (2013)

Poinar (2008, 2021) Poinar (2005c, 2021) Poinar and Poinar (2004), Poinar (2021) flea (Atopopsyllus Poinar (2015b, cionus) 2021) Lutzomyia Poinar and adiketis Poinar (2004), Poinar (2021) Culex malariager Poinar (2005a, b, 2021) Enischnomyia Poinar (2011a, stegosoma 2021) Leptoconops nosopheris Triatoma dominicana Palaeomyia burmitis

Tick (Amblyomma)

Ground sloth

Source Host Coprolite (Dart Moas River Valley, Euphrates Cave) Coprolite Deer

Holocene

Age Holocene

Indirect: Oocysts

Fossil Evidence Direct: aDNA

T

T

T

T

T

T

T

T

T

T

Environment T

Miller Clay Pit Morphotype 1, Stolzenbach Morphotype Dactylanthus taylorii

Taxon Paleohaemoproteus burmacis

Direct: pollen in Kakapo coprolite

Direct: pollen

Fossil Evidence Direct: Erythrocytes

Beauveria

Paleoophiocordyceps coccophagus

 Cordycipitaceae

 Cordycipitaceae

Direct

Direct

Fungi (see Harper and Krings 2021 for a more comprehensive review)  Ascomycota Paleopyrenomycites devonicus Indirect  Ascomycota Colletotrichum-like acervuli, Erysiphe- and Uncinula-like cleistothecia, black spot-producing microthyriaceous ascostromata  Cordycipitaceae ? Indirect: death-grips

 Santalales (Balanophoraceae)

Plantae  Santalales (Loranthaceae)

Higher Taxon  Haemosporida

Cretaceous

Miocene

Eocene

Late Cretaceous (Maastrichtian)

Early Devonian

Holocene

Eocene

Age Early Cretaceous

Host Proticulicoides sp.

Amber (Myanmar)

Amber (Dominican)

Lagerstätte (Messel)

Lagerstätte (Rhynie Chert) Coprolite (Lameta Fm.)

Scale insect

Ant traces on Byttnertiopsis daphnogenes Worker ant

Asteroxylon mackiei Infested plant remains eaten by sauropods

? Lagerstätte (Miller Clay Pit, Stolzenbach coal mine) ?Hardwood trees Coprolite and shrubs (Honeycomb Hill Cave System)

Source Amber (Myanmar)

Poinar and Thomas (1984) Sung et al. (2008)

Hughes et al. (2010)

Taylor et al. (1999, 2005) Sharma et al. (2005)

Wood et al. (2012)

T

T

T

T

T

T

Grímsson et al. T (2017a, b)

(continued)

Reference Environment T Poinar and Telford (2005), Poinar (2021)

Direct: tube-­ dwellings preferentially attached to shell

?

?

?

Kabatarina pattersoni

?

Phylum Arthropoda  Copepoda

 Copepoda

 Copepoda (Dichelesthiidae)

 Malacostraca (Cryptochiridae)

Indirect

Direct

Indirect: Fossulae and perforations

Indirect: Exocysts

Fossil Evidence

Taxon

Higher Taxon Metazoa  Metazoa indet.

Table 1.1 (continued)

Lagerstätte (Guanshan)

Cambrian

Pliocene Pleistocene

Early Cretaceous

Middle (Givetian) Upper Devonian (Famennian)

Skeletal deformation

Lagerstätte (Santana Fm.)

Skeletal deformation

Middle (Bathonian) - Skeletal deformation Upper Jurassic (Kimmeridgian)

Source

Age

Reference

Corals (Manicina, Siderastrea, Solenastrea)

Placoderms, psammosteid agnathans, sarcopterygians Fish

Crinoids, echinoids

Cressey and Boxshall (1989), Cressey and Patterson (1973) Klompmaker and Boxshall (2015), Klompmaker et al. (2016)

Radwańska and Radwańska (2005), Radwanska and Poirot (2010) Lukševics et al. (2009)

Zhang et al. Lingulid (2020) brachiopod (Neobolus wulongqingensis)

Host

M

M

M

M

M

Environment

Taxon ?

Epicaridea

Urda rostrata

?

Vacuotheca dupeorum

Epicaridea

Higher Taxon  Rhizocephala

 Isopoda

 Isopoda

 Isopoda

 Isopoda

 Isopoda

Source Skeletal deformation

Middle Jurassic

Direct: Late Cretaceous Cryptoniscus larvae Direct: Miocene Cryptoniscus larvae

Amber (Vendean) Amber (Chiapas)

Lagerstätte (Iron-stone geode) Lagerstätte (Solnhofen)

?Early Jurassic; Late Skeletal Jurassic-Recent deformation

Age Cretaceous Miocene

Direct: remains Late Jurassic associated with host

Direct: isolated

Indirect: swellings

Fossil Evidence Indirect

Reference Feldmann (1998), Bishop (1974, 1983) Wienberg-­ Rasmussen et al. (2008), Klompmaker et al. (2014, 2021), Klompmaker and Boxshall (2015), Robins and Klompmaker (2019) Nagler et al. (2017a, b) Ray-finned fishes Nagler and (Pholidophorus, Haug (2015) Amblysemius, Caturus, Anaethalion, Leptolepides) ? Schädel et al. (2019) ? SerranoSánchez et al. (2016)

?

Decapod crustaceans

Host Decapod crustaceans

T

T

M

M

M

(continued)

Environment M

Taxon 4 genera; 9 species

Invavita piratica

?Ascothoracida

?Ascothoracida

Carios jerseyi

Ornithodoros antiquus

Higher Taxon  Pentastomida

 Pentastomida?

 Thecostraca

 Thecostraca

 Acari (Argasidae)

 Acari (Argasidae)

Table 1.1 (continued) Age Cambrian-­ Ordovician

Direct: male and female

Direct: larval stage

Indirect: borings

Indirect: borings

Miocene

Late Cretaceous

Cretaceous

Cretaceous

Direct: remains Silurian associated with host

Fossil Evidence Direct: phosphatized remains isolated from host

Host Reference ? Early chordates Walossek et al. (1994), Walossek and Müller (1994), Maas and Waloszek (2001), Waloszek et al. (2005), Castellani et al. (2011) Siveter et al. Lagerstätte Ostracod (2015), but see (Herefordshire) (Nymphatelina Boxshall and gravida) Hayes (2019), Haug et al. (2021) Skeletal Echinoidea Madsen and deformation Wolff (1965), Bromley (2004) Skeletal Octocorallia Voigt (1959, deformation 1967) ?Bird Klompen and Amber (New Jersey) Grimaldi (2001) Amber ?Rodent Poinar (1995) (Dominican)

Source Lagerstätte (Kinekulle, Green Point)

T

T

M

M

M

Environment M

Compluriscututa vetulum

Ixodes succineus

Deinocroton draculi

 Acari (Ixodidae)

 Acari (Ixodidae)

 Acari (Deinocrotonidae)  Acari (Trombiformes)  Acari (Trombiformes)

 Hemiptera (Coccoidea)

 Acari (Mesostigmata)  Hemiptera (Cimicomorpha)

Cornupalpatum burmanicum

 Acari (Ixodidae)

Flexicorpus acutirostratus, Torirostratus pilosus ?

Myrmozercon sp.

Erythraeidae

Leptus sp.

Taxon Amblyomma birmitum

Higher Taxon  Acari (Ixodidae)

Direct: larvae

Direct: attached to ant Indirect: blood meal

Early Cretaceous

Direct: engorged female Direct: feeding on fly Direct: feeding on midge

Coprolite (Le Quesnoy)

Lagerstätte (Yixian Fm.)

Cretaceous

Eocene (Ypresian)

Amber (Baltic)

Amber (Myanmar) Amber (Spanish) Amber (Canadian)

Amber (Baltic)

Amber (Myanmar)

Amber (Myanmar)

Source Amber (Myanmar)

Eocene

Late Cretaceous (Campanian)

Early Cretaceous

Eocene

Early Cretaceous

Early Cretaceous

Age Early Cretaceous

Direct: Female

Direct: larval stage

Direct: larval stage

Fossil Evidence Direct: unengorged female

Small mammal (early perissodactyls or Plesiadapidae)

Ctenobethylus goepperti Mammals, birds or dinosaurs

Robin et al. (2016b)

Dunlop et al. (2014) Yao et al. (2014)

Reference ChitimiaDobler et al. (2017) Feathered Poinar Jr and dinosaur Brown (2003), Peñalver et al. (2017) ? Poinar and Buckley (2008) ? Dunlop et al. (2016) ?Feathered Peñalver et al. dinosaurs (2017) Burmazelmira Arillo et al. aristica (2018) Metriocnemus sp. Poinar et al. (1997)

Host ?

T

T

T

T

T

T

T

T

T

(continued)

Environment T

Megamenopon rasnitsyni ? Qiyia jurassica

Enischnomyia stegosoma

 Phthiraptera (Menoponidae)  Phthiraptera  Diptera (Athericidae)

 Diptera (Streblidae)

Amber (Dominican) Amber (Dominican)

Miocene

Direct

Miocene

Lagerstätte (Messel) Amber (Baltic) Lagerstätte (Daohugou beds) Amber (Dominican)

Miocene-­Pleistocene Skeletal deformation

Miocene

Amber (Baltic)

Source Lagerstätte (Jiulonshan Fm.) Lagerstätte (Yixian Fm.)

Eocene

Early Cretaceous

Age Middle Jurassic

Direct: with feather Eocene remains in crop Indirect: nits Eocene Indirect: larvae Jurassic

Indirect: perforations in osteoderms

Palaeopsylla: 4 species Direct: isolated from host Rhopalopsyllus sp. Direct: isolated from host Direct Atoposyllus cionus, Eospilopsyllus kobberti, Pulex larimerius

 Siphonaptera s.s. (Ctenophthalmidae)  Siphonaptera s.s. (Rhopalopsyllidae)  Siphonaptera s.s. (Pulicidae)

?Tunga

Direct: isolated from host

Pseudopulex magnus

 Siphonaptera s.l. (Pseudopulicidae)

 Siphonaptera (Tungidae)

Taxon Fossil Evidence Pseudopulex jurassicus Direct: isolated from host

Higher Taxon  Siphonaptera s.l. (Pseudopulicidae)

Table 1.1 (continued)

?Bats

Mammals ?Salamanders

Armadillos, glyptodonts, armadillo-like cingulates Birds

?

?

Host ?Pterosaurs, dinosaurs and/or small mammals ?Pterosaurs, dinosaurs and/or small mammals ?Mammals

Lewis and Grimaldi (1997), Perrichot et al. (2012), Poinar (2015b) Tomassini et al. (2016), de Lima et al. (2018) Wappler et al. (2004) Voigt (1952) Chen et al. (2014); but see Leung (2017) Poinar and Brown (2012)

T

T F

T

T

T

T

T

T

Gao et al. (2012, 2013) Beaucournu (2003) Poinar (1995)

Environment T

Reference Gao et al. (2012, 2013)

 Oxyurida Paleoxyuris cockburni (Heteroxynematidae)

?

 Ascaridida (Heterakoidea)

Indirect: eggs

Direct : eggs, aDNA

Direct : eggs, aDNA

Late Triassic

Holocene

Pleistocene

Pleistocene

Indirect: eggs

Toxocara canis

Toxascaris leonina

Pleistocene

Indirect. eggs

Toxocara sp.

Pleistocene

Miocene

Indirect. eggs

Indirect: eggs

Ascaris lumbricoides

Bauruascaris adamantinensis, B. cretacicus Ascarid type

Direct: egg with Early Cretaceous developing juvenile Direct: eggs with Late Cretaceous developing embryo (Maastrichtian)

Late Triassic

Indirect: eggs

Ascarites rufferi

Ascarites gerus

Age

Fossil Evidence

Taxon

 Ascaridida (Toxocaridae)

 Ascaridida (Ascarididae)  Ascaridida (Toxocaridae)  Ascaridida (Toxocaridae)

 Ascaridida

 Ascaridida (Ascarididae)  Ascaridida (Heterocheilidae)

Higher Taxon Phylum Nematoda  Ascaridida (Ascarididae)

Coprolite (Haro River Quarry) Lagerstätte (MenezDregan) Coprolite (Peñas de las Trampas) Coprolite (Dart River Valley, Euphrates Cave) Coprolite (Santa Maria Fm.)

Coprolite (Santa Maria Fm.) Coprolite (Saint Barbe Fm.) Coprolite (Adamantina Fm.) Lagerstätte (Gray Fossil Site) Lagerstätte

Source

Hugot et al. (2014), Francischini et al. (2018)

Cynodont

T

T Wood et al. (2013) Moa

Puma concolor

T

T

T

T

T

T

T

T

(continued)

Environment

Petrigh et al. (2019)

Canid (?Crocuta spelaea) Canid (?Crocuta spelaea)

Homo

Tapir polkensis

Crocodylian

Poinar and Boucot (2006) Cardia et al. (2018), Cardia et al. (2019b) McConnell and Zavada (2013) Bouchet et al. (1996) Perri et al. (2017) Bouchet et al. (2003)

Da Silva et al. (2014)

Cynodont

Archosaur

Reference

Host

Early Devonian Eocene

Direct Direct

?

Heydenius antiqua

Heydenius: 7 species

Heydenius: 8 species

Heydenius tabanae

Palaeonema phyticum

Cascofilaria baltica

 Mermithida

 Mermithida

 Mermithida

 Mermithida

 ?Enoplida (Palaeonematidae)  Filarioidea

Direct

Direct

Direct

Direct

Direct

Pliocene

Miocene

Eocene

?Oligocene

Eocene

Early Cretaceous

 ?Mermithida

Direct

Cretacimermis protus, C. chironomae

Early Cretaceous

Direct

 Mermithida (Mermithidae)

Age Holocene

Fossil Evidence Indirect: eggs

Taxon Enterobius vermicularis Cretacimermis libani

Higher Taxon  Oxyurida (Oxyuridae)  Mermithida (Mermithidae)

Table 1.1 (continued) Host Homo

Reference Fry and Moore (1969) Poinar et al. Midge (1994), Poinar (Chironomidae: (2011b) Diptera) Amber Ceratopogonidae, Poinar and (Myanmar) Chironomidae Buckley (2006), Poinar (2011b) Lagerstätte Chlorodema Voigt (1957), (Geiseltal) primordialis Poinar (2011b) Lagerstätte Hesthesis von Heyden (?Rott) immortua (1860, 1862) Poinar (2011b) Amber (Baltic) Arachnida, Diptera, Hemiptera, Hymenoptera Poinar (2011b) Amber Coleoptera, (Dominican) Diptera, Hymenoptera Lagerstätte Tabanus Poinar (Willershausen) sudeticus (2011b), Grabenhorst (1985) Lagerstätte Early land plant Poinar et al. (Rhynie Chert) (2008) Amber (Baltic) Blackfly Poinar (2011b, (Simuliidae) 2012b)

Source Coprolite (Danger Cave) Amber (Lebanese)

T

T

T

T

T

T

T

T

T

Environment T

Indirect: eggs

Fossil Evidence Direct

 Gordioidea Paleochordodes protus (Chordodidae) Phylum Platyhelminthes  Cestoda Eucestoda

Miocene

Permian

Direct: eggs with developing embryo

Eocene

Early Cretaceous

Eocene

Early Cretaceous

Early Cretaceous

Miocene

Age Miocene

Direct

Direct

 Gordioidea?

Gordius tenuifibrosus

Direct

Cretaciaphelenchoides Direct burmensis Proheterorhabdites Direct burmanicus Palaeocosmocerca Direct burmanicum

Taxon Cascofilaria dominicana, C. parva Capillaria-type

Phylum Nematomorpha  Gordioidea Cretachordodes (Chordodidae) burmitis

 Cosmocercidae

 Heterorhabditoidea

 Tylenchomorpha

 Trichinellida

Higher Taxon  Filarioidea

Coprolite (Rio do Rasto Fm.)

Amber (Dominican)

Lagerstätte (Geiseltal)

Amber (Myanmar)

Source Amber (Dominican) Lagerstätte (Gray Fossil Site) Amber (Myanmar) Amber (Myanmar) Amber (Myanmar)

Sharks

Cockroach

?

?Cockroach

Crane fly (Gonomyia) Rove beetle (Staphylinidae) Gastropod

Tapir polkensis

T

T

T

Dentzien-Dias M/F et al. (2013); potentially even older: see Zangerl and Case 1976 (continued)

Poinar and Buckley (2006) Voigt (1938); doubtful: see Poinar (1999) Poinar (1999)

Poinar (2011b) T

Poinar (2011b) T

T McConnell and Zavada (2013) Poinar (2011b) T

Host Reference Environment Mosquito (Culex) Poinar (2011b) T

?Gymnophallidae

?

?Gymnophallidae

?

 Trematoda

 Trematoda

 Trematoda

 Monogenea

Direct: attachment structure

Indirect: encysted cercaria Indirect: pits in shells

Indirect: igloos

Indirect: eggs

Fossil Evidence Indirect: eggs

Indirect: eggs Moniliformidae (e.g., Moniliformis?), Oligacanthorhynchidae (e.g., Echinopardalis)

Dicroelidae

 Trematoda

Phylum Rotifera Archiacanthocephala

Taxon Digenites proterus

Higher Taxon  Trematoda

Table 1.1 (continued)

Holocene

Middle Devonian

Early Eocene-­Holocene

Cretaceous

Coprolite

Lagerstätte (Lode Fm.)

Amber (Myanmar) Skeletal deformation

Mammals (Carnivora, Homo)

Placoderms, acanthodians

Bivalves

Agamid lizard

Bivalves

?Bear

Source Host Coprolite (Saint Archosaur Barbe Fm.)

Coprolite (Caune de l'Arago Cave) Cretaceous-­Holocene Skeletal deformation

Pleistocene

Age Early Cretaceous (Barremian)

Fry and Hall (1969), Noronha et al. (1994)

Rogers et al. (2018), Ituarte et al. (2001, 2005) Poinar et al. (2017) Ruiz and Lindberg (1989), Huntley and De Baets (2015) Upeniece (2001, 2011), De Baets et al. (2015)

Jouy-Avantin et al. (1999)

T

M

M

T

F

T

Reference Environment Poinar and T Boucot (2006)

Taxon ?

?

Vermiforafacta rollinsi

?

Arabella

?Hirudinae

Branchiobdellida

Higher Taxon Archiacanthocephala

 Phylum Tardigrada

Phylum Annelida  Spionida

 Myzostomida

 Oenonidae

 Clitellata

 Clitellata

Direct: isolated coccoons with spermatozoa

Indirect: cocoons

Indirect: galls on crinoid arms Direct: jaw apparatus

Direct: associated with bivalve

Direct: isolated forms

Lagerstätte (Section Peak Fm.) Lagerstätte (La Meseta Fm.)

Eocene

Lagerstätte (Marcellus Form ation) Skeletal deformation Lagerstätte (Tluszcz)

Lagerstätte (Kuonamka Fm.)

Source Coprolite (Adamantina Fm.)

Triassic

Carboniferous-­ Jurassic Jurassic (Oxfordian)

Middle Devonian­

Cambrian

Fossil Evidence Age Direct: eggs with Late Cretaceous developing acanthor (Campanian-­ Maastrichtian)

?Crayfish

?

?Polychaete

Welch (1976), Hess (2010) Szaniawski and Gazdzicki (1978) Manum et al. (1991), Bomfleur et al. (2012) Bomfleur et al. (2015)

Cameron (1967, 1969

Müller et al. (1995)

?

Ptychopteria (Cornellites) flabellum Crinoids

Reference Cardia et al. (2019a)

Host Crocodylian?

F

F

M

M

M

M

(continued)

Environment T

Fossil Evidence

?

Chrysallida minuera

 Pyramidellidae

Direct: isolated shells

Indirect

Direct: attachment, Various genera and negative effect on species including Cyclonema, Platyceras, host Naticonema

Taxon

 Platyceratidae/ Orthonychiidae

Higher Taxon Phylum Mollusca  Platyceratidae/ Orthonychiidae

Table 1.1 (continued)

Middle Jurassic (Bathonian)

Lagerstätte (Ore-bearing clays)

Skeletal deformation

Lagerstätten

Middle Ordovician Late Permian

Middle Ordovician Late Permian

Source

Age

?Polychaetes

Blastoids, crinoids

Blastoids, crinoids and cystoids

Host

Environment

M Bowsher (1955), Baumiller (2002), Webster and Donovan (2012), Baumiller et al. (2004), Baumiller (2003), Baumiller Gahn (2018), Nützel (2021), Thomka and Brett (2021) Baumiller and M Macurda (1995), Baumiller and Gahn (2002), Baumiller et al. (2004), Donovan and Webster (2013) Kaim (2004) M

Reference

?Thyca

Latiaxis serratus

Leptoconchus: 2 species; Coralliophila: 1 species; Galeropsis: 1 species Hyriidae (?Diplodon)

Silesunio parvus

 Eulimidae

 Coralliophilidae

 Coralliophilidae

 Unionida

 Unionida

Taxon Eulima ssp.

Higher Taxon  Eulimidae

Late Cretaceous (Campanian) Oligocene-Miocene

Late Cretaceous (Campanian)

Age Late Cretaceous (Campanian)

Direct: Glochidium Middle Miocene larvae Late Triassic Indirect: adult (Carnian) forms assigned to Unionidae

Direct: isolated shells Direct: shells associated with coral host

Indirect: trace on echinoid hosts

Fossil Evidence Direct: isolated shells

Lagerstätte (Pebas Fm.) Lagerstätte (Krasiejów)

Lagerstätte (Ripley Fm.) Skeletal deformation

Source Lagerstätte (Coffee Sand Fm.) Skeletal deformation

?

Gross and Piller (2019) Skawina and Dzik (2011)

F

F

M

Lozouet and M Renard (1998)

? Corals (Cladocora, Thegioastraea, Pocillopora) ?Fish

M

Environment M

Neumann and Wisshak (2009) Sohl (1964)

Reference Dockery (1993)

Echinoids (Echinocorys)

Host ?Echinoderms

20

K. De Baets et al.

Fig. 1.1  Common depositional environments of Lagerstätten in which parasites have been preserved. Modified from Seilacher et al. (1985)

(siderite) nodules that formed in marginal marine environments associated with river deltas (Baird et al. 1986; Clements et al. 2019). Amber is a material derived from tree resin that often incorporates flora and fauna as it flows under gravity down the external surface of its parent tree (Labandeira 2014). Preservation in amber can be truly exceptional as organisms are often completely engulfed and entombed by the resin—indeed microscopic internal parasites can be preserved in situ within their hosts and examined via micro-computed tomographic (μCT) techniques (Poinar et al. 2017). Amber can be considered a conservation trap, productive places to find possible tiny soft-­bodied unicellular organisms and helminths. Other conservation traps in which organisms become rapidly entombed in a fossilization medium that hampers further decay include leech cocoons (Manum et al. 1991) and coprolites (Qvarnström et al. 2016). Clitellate annelids produce a mucous substance of polysaccharides and fibrous proteins, which may cure up to several days in solid,

1  The Fossil Record of Parasitism: Its Extent and Taphonomic Constraints

21

protective egg capsule or cocoon that is highly resilient toward thermal, chemical, and proteolytic decay, and capture various fossil unicellular and microscopic multicellular organisms (Bomfleur et al. 2012; McLoughlin et al. 2016). Coprolites, fossilized feces, are rich sources of paleoecological information as they provide clues to not only the producer’s diet but also their internal flora and fauna, including parasites and other symbionts (Chin 2021; Qvarnström et al. 2016). Coprolites are often preserved through phosphatization, especially those produced by predators that ingest bones, ready sources of phosphate.

1.2.2  Burgess Shale-Type Preservation and Parasitism Even sites of exceptional preservation and diversity in the early Paleozoic have a dearth of reported parasites. For example, no parasitic organisms have been reported from the Burgess Shale, and only ectosymbiotic worms—potentially ectoparasitic gnathiferans (Herlyn 2021)—have been reported from the Chengjiang Lagerstätte (Cong et  al. 2017). Encrusting tubes on organophosphatic brachiopods from the Guanshan Lagerstätte (Chen et  al. 2021) provide so far the best evidence for a Cambrian kleptoparasite-host interaction (Zhang et al. 2020). Nevertheless, future work on the Burgess Shale, Chengjiang, and coeval BST deposits of the Cambrian may yield additional discoveries of early animal parasites which might not yet have all the characteristics or small sizes of their modern counterparts (Herlyn 2021).

1.2.3  Orsten-Type Preservation and Parasitism Some of the oldest parasitic finds with fine morphological details are phosphatized pentastomid crustaceans from the Cambrian Orsten fauna (Walossek and Müller 1994). Unfortunately, the host associations of the Cambrian-Ordovician pentastomids are speculative as the hosts are not preserved in situ. Nonetheless, the morphology of the pentastomids likely represents unambiguous evidence of parasitism (Haug et  al. 2021). Other arthropods preserved as Orsten-type microfossils may also provide evidence of parasitism (Andres 1989; Labandeira 2002; Dunlop 2021; Haug et al. 2021). Orsten-type microfossils of sea spiders and tardigrades are, in particular, reminiscent of extant parasites belonging to these lineages (Müller and Wallossek 1988; Müller et al. 1995; Labandeira 2002). However, they seemingly represent different stages of development than modern relatives and might only look superficially similar due to the presence of plesiomorphic traits (compare Dunlop 2021). With a preservation similar to the Orsten, the Cretaceous Santana Formation contains some of the most exquisitely preserved phosphatized parasitic copepods, which were preserved in association with fish gills and are ascribed to a modern family (Cressey and Patterson 1973; Cressey and Boxshall 1989). Although not necessarily parasites, phosphatized ciliates associated with ostracods from the

22

K. De Baets et al.

Triassic of Spitsbergen (Weitschat and Guhl 1994) further illustrate the high potential of phosphatization to preserve soft-bodied parasites due to the typically fine detail of microscopic organisms preserved in this fossilization mode.

1.2.4  Petrification, Nodular Preservation, and Parasitism Various other types of Lagerstätten preserved in nodules have yielded evidence for parasites, including a putative pentastomid parasitizing an ostracod (Siveter et al. 2015; but see Boxshall and Hayes 2019; Haug et al. 2021 for alternative interpretations) from calcareous nodules, the Silurian Herefordshire Lagerstätte (Siveter 2008), as well as early representatives of fungi (Taylor et al. 2005) and nematodes (Poinar et al. 2008) in the Devonian Rhynie chert (De Baets et al. 2021b; Harper and Krings 2021). The oldest evidence for parasitic helminths comes from the Middle Devonian Lode Quarry (De Baets et al. 2021b), where the hooks of their anterior attachment organs (rostella) are preserved (Upeniece 2001; De Baets et al. 2015). These structures may be more resistant to decay than other helminth tissues. So far, such structures (apart from those interpreted in eggs) have only been reported from the Lode Quarry, which could indicate that this type of preservation is uncommon. Alternatively, it is possible that such structures are frequently prepared away and/or overlooked due to their small size (Leung 2021). Cyclida (formerly known as Cycloidea) known from siderite nodules in the Carboniferous Mazon Creek Lagerstätte (Schram et al. 1997) has been placed together with extant Branchiura (Dzik 2008), but their affinities with this group as well as their parasitic mode of life remain debated (Schram et al. 1997; Haug et al. 2021). Parasitic isopods inferred to have parasitized fish hosts have been reported from Jurassic calcareous nodules (Nagler et al. 2017b).

1.2.5  Lithographic Limestone Preservation and Parasitism Leeches likely invaded freshwater environments during the Paleozoic (Kuo and Lai 2019). Silurian leech-like body fossils have been reported (Mikulic et al. 1985), but their affinity and mode of life remain unclear (Kuo and Lai 2019). The oldest diagnosable leech fossils come from the Jurassic lithographic limestones (Kozur 1970) and postdate cocoons that are attributable to leeches (Manum et al. 1991; De Baets et al. 2021b). These Jurassic specimens may have been predatory rather than parasitic organisms. Such limestones are also important sources of insects (Martı́nez-­ Delclòs et al. 2004). Although it can be difficult to distinguish parasite and scavenger remains in some lithographic limestone material (Wilson et al. 2011), the Jurassic Nusplingen Limestone has yielded isopods attached to squids possibly representing their hosts (Polz et al. 2006; Haug et al. 2021). Jurassic lithographic limestones also contain exceptionally preserved associations of isopods and their fish hosts (Nagler et al. 2016; Haug et al. 2021) as well as skin nodules in fossil fishes, which might

1  The Fossil Record of Parasitism: Its Extent and Taphonomic Constraints

23

relate to various pathogens (Petit and Khalloufi 2012). Similar skin nodules have been discovered in the Eocene Monte Bolca Lagerstätte (Petit 2010) where also a specimen of the spadefish Eoplatax papilio was discovered with attached, possible parasitic gastropods (Petit et al. 2014). Solnhofen lithographic limestones have also yielded a nauplius larva with a collar, which is similar to extant rhizocephalans that become parasites at maturity (Nagler et al. 2017a; Haug et al. 2021). Engorged fossil mosquito remains in the Eocene Green River Formation have even yielded evidence for their blood meal in the form of porphyrins (Greenwalt et  al. 2013; Greenwalt 2021).

1.2.6  Bituminous/Oil Shales, Coal Deposits, and Parasitism Bituminous and oil shales have also yielded exceptionally preserved parasitic remains, particularly in the Cenozoic. These include an Eocene bird louse from Eckfeld in Germany with preserved crop contents (Wappler et al. 2004) and leaves with death-grip traces in the Eocene Messel Lagerstätte in Germany (Hughes et al. 2010). Coal deposits like Geiseltal in Germany have yielded evidence of nematodes and nematomorphs still associated with their insect hosts (Voigt 1938, 1957).

1.2.7  C  onservation Traps (Amber, Leech Cocoons, and Coprolites) and Parasitism Some of the most spectacular remains of parasites have been found trapped in tree resin that hardens and transforms into amber, trapped in the cocoons of leeches, or isolated in the digestive tracks of their hosts within coprolites (Fig. 1.1). The amber record extends back to the Carboniferous (Bray and Anderson 2009), but the oldest globally distributed amber with inclusions has been reported from the Triassic (Seyfullah et  al. 2018). Massive amber deposits rich in inclusions are largely concentrated in the Cretaceous and Cenozoic (Martı́nez-Delclòs et  al. 2004)—only these so far have yielded a diverse spectrum of parasitic remains (Poinar 2011b, 2014). Due to where it forms, fossiliferous amber predominantly includes terrestrial, rather than fully marine, organisms (Solórzano Kraemer et al. 2018). Marine organisms are sometimes recovered from amber, but they are usually not well preserved (Yu et al. 2019). Terrestrial nematodes and arthropods such as hematophagous insects, mites and ticks are some of the most well-known parasites in amber (Poinar 2011b; Pielowska et al. 2018; Dunlop 2021; Labandeira and Li 2021). In some cases, they are still associated with their pathogens they distribute (see Poinar 2021; Harper and Krings 2021). Other examples include early ontogenetic parasitic stages of epicarid  isopods (Serrano-Sánchez et  al. 2016; Schädel et al. 2019). 

24

K. De Baets et al.

Leech cocoons are quite resistant and represent evidence for leeches in their own right as discussed above (De Baets et al. 2021; Manum et al. 1991, 1994). However, these sometimes trap spermatozoa (Bomfleur et al. 2015), microorganisms like ciliates (Bomfleur et al. 2012), or soft-bodied nematodes (Manum et al. 1994), qualifying them as conservation traps. It might, therefore, be a matter of time that microscopic parasites are also recovered from them. At first sight, the preservation of eggs, cysts, and other propagules in coprolites might not seem so surprising as they are quite resistant and can survive different acid and base treatments (Camacho et al. 2018; Dufour and Le Bailly 2013) and are even recovered from pollen residues (Brinkkemper and van Haaster 2012). Some of these propagules, however, do show exceptional preservation such as remains of still developing early life stages within helminth eggs (Dentzien-Dias et al. 2013; Poinar and Boucot 2006; Cardia et al. 2019a) and have yielded less resistant cysts of coccidians, actinomycetes, or amoebozoa (see Table 1)—only rarely recovered from subfossil coprolites with destructive methods (Chin 2021).

1.2.8  Other Types of Parasite Lagerstätten Some sites yielding parasite evidence do not qualify as conservation or concentration Lagerstätten (Fig.  1.1). Liberation Lagerstätten are defined by fossiliferous sediments from which three-dimensionally preserved macrofossils can easily be extracted (Roden et al. 2019). These are especially relevant for the small parasitic life stage of mollusks (see Table 1.1), which have yielded the oldest evidence for a variety of modern groups of parasitic gastropods (Nützel 2021) and bivalves (Skawina 2021). Such types of preservation also allow to easily detect parasitic traces on shell interiors (Huntley et al. 2021), but similar traces could also be found in Lagerstätten characterized by impregnation of hydrocarbons (e.g., Buckhorn Asphalt) or replacement by silica (Liljedahl 1985). Even internal molds (negative casts) (De Baets et al. 2011; Klug et al. 2008) or cross/thin sections (Kříž 1979; Keupp 1987) can reveal evidence of pearls, igloos, and other pathologies linked with parasitism in shelled molluscs (Huntley and De Baets 2015; De Baets et al. 2021c; Huntley et al. 2021).

1.2.9  E  volutionary History of Parasitism Recorded in Konservat-Lagerstätten Current fossil evidence (Bassett et al. 2004; Zhang et al. 2020), as well as extrapolations from current host associations (e.g., Poinar 2011b), suggests that metazoan parasitism most likely originated for the first time during the Cambrian (De Baets et  al. 2021d). To our knowledge, only the Ediacaran Dickinsonia  (Wade 1972; Conway Morris 1981) has rarely and  speculatively been compared to modern

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parasites (e.g., annelid Spinther ectosymbiotic on sponges: Andrade et al. 2015), but they lack evidence of openings, gut tracts, or even potential hosts (Sperling and Vinther 2010; De Baets and Littlewood 2015). So far, no fossils of metazoan parasites from the Proterozoic have been confidently identified (De Baets and Littlewood 2015), although a diversity of eukaryovorous unicellular parasites (or perhaps more appropriately predators) is presumed from strata as old as the Cryogenian (Porter 2016). Current phylogenetic analyses suggest that parasitism first evolved in the sea (Littlewood 2005), which is consistent with the earliest fossil evidence deriving from marine environments—Orsten- and Burgess Shale-type fossils might be the most suitable for the preservation of parasite–host interactions. Paleozoic coprolites and Lagerstätten with exceptional host remains also provide evidence for marine to lacustrine parasites associated with vertebrates (De Baets et al. 2015; Zangerl and Case 1976; Upeniece 2001; Dentzien-Dias et al. 2013; Chin 2021). That said, what is the age of the oldest evidence for parasites with terrestrial hosts? Evidence from the Devonian Rhynie Chert shows that fungi and nematodes were already associated with early land plants (Harper and Krings 2021; Poinar et al. 2008; Taylor et al. 2005), while evidence from Triassic coprolites shows that nematodes were already associated with cynodonts—part of the lineage leading to extant mammals (Da Silva et al. 2014; Hugot et al. 2014; Francischini et al. 2018; De Baets et al. 2021b; Chin 2021). Evidence from amber shows that complex terrestrial interactions between nematodes, unicellular organisms, arthropods, and vertebrates were probably in place at the latest by the Early Cretaceous (Poinar 2018, 2021). The breadth of parasitic remains in Lagerstätten is still poorly known—we are aware of confidently identifiable parasites in only about 15 of the known Lagerstätten listed in the dataset by Muscente et al. (2017b), which does not include amber. A more comprehensive screening of parasitic remains in Lagerstätten and other deposits, coupled with taphonomic experiments (Klompmaker et al. 2017, 2021) as well as a better understanding of functional morphology (Nagler and Haug 2016), would be necessary to more effectively use and understand the fossil record of parasites in these deposits. This is nicely illustrated for isopods for which a systematic screening and study have led to several major discoveries of fossil representatives of parasitic lineages in Lagerstätten (Nagler et  al. 2016, 2017b; Serrano-Sánchez et  al. 2016; Schädel et al. 2019; Robin 2021) as well as rich record of characteristic swellings in the more continuous fossil record of their hosts (Wienberg-Rasmussen et al. 2008; Klompmaker et al. 2014, 2021; Robins and Klompmaker 2019).

1.3  Potential and Limits of Lagerstätten Exceptionally preserved parasitic remains can provide direct information on the morphology, life history, and host strategies of parasites as well as the ecology of their hosts (De Baets and Littlewood 2015; Leung 2021). They hold the potential to constrain divergence time estimates, aid in ancestral state reconstructions, and reconstruct

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Fig. 1.2  Temporal and environmental distribution of Konservat-Lagerstätten from the Ediacaran through the Neogene (adapted from Muscente et al. 2017a, b) and the number of occurrences of direct evidence for soft-bodied parasites in each period color-coded by mode of preservation. Note the nearly one order of magnitude difference in the number of Lagerstätten versus the number of soft-­bodied parasite occurrences

ancient food webs (Leung 2021; Labandeira and Li 2021; Warnock and Engelstädter 2021). However, because parasite body fossils are generally rare, they have limited utility for addressing large-scale patterns in parasite distribution in space and time. This affects their usefulness to directly address macroevolutionary and macroecological patterns in parasite–host co-evolution (Thomka and Brett 2021;  Robin 2021), extinction (Van Dijk and De Baets 2021), as well as their relationship with environmental changes (Fig. 1.2). Both the temporal patchiness of Konservat-Lagerstätten and the limited search efforts for parasites likely contribute to this pattern. Efforts to elucidate the parasite fossil record in Lagerstätten have only just begun. The majority of discoveries so far have been accidental, with the possible exception of amber, which has been more systematically screened for arthropods and nematodes (Poinar 2011b, 2014, 2018; but see Labandeira and Li 2021). A higher awareness might help to reveal additional finds. Moreover, novel techniques like computed tomography might help in the systematic screening of host remains for parasites (Poinar et  al. 2017). In some cases, the unsuccesfull screening for particular parasitic remains (e.g., helminths) led to the discovery of other parasites (Robin et al. 2016b).

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When searching for parasitic remains, it is necessary to consider the preservation potential of both the parasites and suitable host environments. For example, particular swellings (ichnotaxon Kanthyloma crusta) in the gill region of decapod crustaceans have been interpreted as fossil evidence for parasitic epicaridean isopods by analogy of such swellings containing these isopods in modern decapods (Williams and Boyko 2012; Klompmaker et al. 2014, 2021; Klompmaker and Boxshall 2015). One argument against this interpretation has been the lack of soft-­tissue remains within these swellings. However, a recent experimental decay study demonstrated that the parasitic isopod decays more rapidly than their hosts, thereby limiting their chances for preservation in association with their hosts (Klompmaker et  al. 2017, 2021). Other studies using modern tree resin have demonstrated that minor changes in the composition of gut microbiota could affect the decay rate of their arthropod hosts and therefore their record in amber (McCoy et al. 2018). The preservation of parasites will also be influenced by where their hosts live. Some host environments, like gill chambers of fishes, cocoons, coprolites, or resin, might be conducive for the preservation of evidence of some interactions (e.g., Skawina 2021), while others might not. Experimental taphonomy might be useful to establish which environments were most likely to result in the preservation of parasites in the geological past. Discoveries of fossils representing nonparasitic life stages of groups that currently parasitize hosts might help put constraints on the first appearances of these groups. However, their presence or even that of their host does not necessarily coincide with the presence of their parasitic stages which could have evolved at a later stage (Nagler and Haug 2015; Nützel 2021; Okamura and Gruhl 2021). The same goes for the constraints derived from their hosts where parasites might have evolved earlier and exploited different hosts before their putative host switches (Siveter et al. 2015). We would need a lot of direct evidence in the form of fossil parasites or direct associations to meaningfully infer a precise timeline for their evolution. The molecular clock in combination with well-preserved fossils or other evidence from the geological record might, however, aid to constrain the timing and dynamics of evolutionary events in soft-bodied organisms like parasites (De Baets and Littlewood 2015). Applying traditional molecular clock methods to the study of parasitic organisms is challenging, not only due to the nature of their genomes or the complexity of parasite–host interactions, but also the incompleteness of their fossil record (Warnock and Engelstädter 2021). Novel developments in models of molecular evolution and Bayesian approaches to deriving temporal constraints from geological evidence (De Baets et  al. 2016; Warnock et  al. 2017; Landis 2020) can overcome at least some of these issues. Promising new methods and future developments relax the null model of strict congruence, allow parasites to have multiple host species (Braga et  al. 2020), and capitalize on the lateral transfer of genetic material (Cai et al. 2021; Suh 2021). Amber can be particularly useful for studying changes in terrestrial parasites and pathogens associated with arthropods, fungi, and plant remains as they are commonly trapped in resin (Poinar 2011b, 2021; Harper and Krings 2021). Remains of marine or other pathogens in amber are too rare to support a comparative study of

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Fig. 1.3  The Devonian through Holocene number of nematode species of parasitic and nonparasitic nematode data (data updated from Poinar 2011b, 2015a)

interactions in high resolution across environmental perturbations or mass extinctions. This lack can be illustrated for nematodes where Maastrichtian-Paleogene or pre-Cretaceous amber data are missing (Fig. 1.3), which makes it hard to evaluate the impact of the end-Cretaceous mass extinction or Paleogene-Eocene Thermal Maximum (PETM). In some cases, meaningful studies can, however, be done on the stage level by combining amber deposits with data from other Lagerstätten (e.g., insects: Martı́nez-Delclòs et  al. 2004). Labandeira and Li (2021) used such an approach to efficiently quantify the Mid-Mesozoic Parasitoid Revolution in insects at the family level. Although amber has to some degree been systematically screened for parasitic arthropod and nematode remains (Poinar 2011b, 2015a), there is still some way to go to understand the history of unicellular pathogens in amber (Poinar 2021).

1.4  Host Remains as Proxy for Parasite–Host Interactions Host remains with a high preservation potential provide a resource for tackling questions related to the deep evolution of parasitic diseases and their relationship with host extinction and environmental perturbations. Genetic analyses of ancient

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DNA (aDNA) have revolutionized the study of subfossil coprolite collections (Lafferty and Hopkins 2018), making it possible to assess the extinction of symbionts and their putative hosts from New Zealand (Wood et  al. 2013; Boast et  al. 2018). Even so, additional studies are necessary to reproduce these results at other localities. Regardless, the usefulness of this technique to study mass extinctions in deep time is limited by the degradation rate of DNA (Greenwalt 2021; van Dijk and De Baets 2021). Conserved regions of DNA in extant forms might also aid to reveal now extinct interactions (Suh et al. 2016; Cai et al. 2021). These can, however, not strictly be called fossils as they represent relictual genetic elements (De Baets and Littlewood 2015) and also become challenging to infer changes in deeper time (Suh 2021). Parasitic interactions preserved in amber, coprolites, or pathologies are useful for investigating parasitism further back in time (Harmon et  al. 2019; De Baets and Littlewood 2015). In particular, the study of propagules in coprolites (Chin 2021; Qvarnström et  al. 2016) and the prevalence of characteristic pathologies in host assemblages could allow the evaluation of parasite–host interactions more continuously and deeper in time into the Paleozoic (De Baets and Littlewood 2015; De Baets et al. 2021d; Robin 2021). Such evidence might be of great interest to constrain changes in the evolution of certain parasite–host associations and parasite prevalence as well as their relationship with host evolution and extinction.

1.4.1  P  ossibilities and Limits of Decay-Resistant Propagules in Host Coprolites The oldest evidence for multiple lineages of endoparasitic helminths comes from coprolites (Chin 2021) including acanthocephalans (Herlyn 2021), flatworms, and ascarid to oxyurid nematodes (De Baets et  al. 2021b). Resistant propagules (i.e., thick-shelled eggs and cysts) may have a high potential for preservation in coprolites because they have often evolved anatomical and physiological characters to ensure survival in the digestive tracks of their hosts (Chin 2021). These characters may also help them to survive various preparation methods (Dufour and Le Bailly 2013; Camacho et al. 2018). Studies should focus on decay-resistant propagules that possess characters that permit their assignment to particular taxa. Coprolites, which are frequently isolated from their progenitors’ remains, are difficult to assign to particular species (Hunt et al. 2012; Wood and Wilmshurst 2014). Even so, coprolites can often be assigned at least to higher taxonomic groups and clades on the basis of size, shape, food content, and composition (Qvarnström et al. 2016). For some questions, host identification might not matter to a degree (Leung 2021). In any case, the presence of parasitic remains within coprolite samples could be evaluated over time and space. Such an exercise would require the development of a subsampling protocol, similar to the one used in the study of subfossil coprolites (Wood and Wilmshurst 2016). At the moment, most species of parasitic remains have been described from

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Quaternary coprolites (Frías et al. 2013; Sianto et al. 2009; Araújo et al. 2015; Chin 2021), but finds going back to the Permian (Dentzien-­Dias et  al. 2013, 2017)  or potentially even Carboniferous (Zangerl and Case 1976; compare De Baets et  al. 2015, 2021b) in the marine realm and the Triassic (Da Silva et al. 2014; Hugot et al. 2014) in the continental realm highlight their further potential to study ancient mass extinctions or environmental perturbations (Fig. 1.3). Coprolites are found in most intervals (Hunt et al. 2012). Computed tomography might potentially aid in the identification of coprolite producers and/or food remains (Qvarnström et al. 2017). Due to the relative sizes of the small parasitic propagules and the large host coprolites, as well as the manner of preservation of the substrates, most computed tomography systems and methods may lack sufficient resolution and image contrast to detect the propagules in larger samples. In these cases, the study of coprolites must rely on destructive methods, like thin-section preparation and acid maceration approaches (reviewed in Chin 2021). When performing destructive analyses, it might particularly make sense to introduce a subsampling protocol (Wood and Wilmshurst 2016). Nevertheless, when propagules can be identified, they may archive the composition and/or position of the parasite before destructive analysis, and thereby help identify parasitic remains as well as their hosts (=coprolite producers). Most studies so far have focused on the Cenozoic (Robin et  al. 2016b; Dentzien-Dias et  al. 2018; Chin 2021) – particularly the Quaternary (Gonçalves et al. 2003; Sianto et al. 2009), but several studies demonstrate the potential to expand such an approach to the Mesozoic (Da Silva et al. 2014; Hugot et al. 2014; Cardia et al. 2018, 2019a, b; Francischini et al. 2018) and even the Late Paleozoic (Dentzien-Dias et al. 2013, 2017; Bajdek et al. 2016). This would, however, demand a more systematic screening of coprolites for parasites in deep time.

1.4.2  Possibilities and Limits of Pathologies in Skeletal Hosts A number of parasite–host interactions can be inferred from (paleo)pathologies in the skeletons of hosts. The fossil record of parasite–host interactions is numerically dominated by traces and malformations in biomineralized skeletons of hosts (Figs. 1.4, 1.5). Indeed, the majority of our knowledge of parasitism throughout the Phanerozoic comes from such records (Figs. 1.4 and 1.5). Hosts are known from seven phyla and the most temporally complete records are found among mollusks (De Baets et  al. 2021c; Huntley et  al. 2021), echinoderms (Baumiller and Gahn 2002; Donovan 2015; Thomka and Brett 2021), brachiopods (Bassett et al. 2004; Rodrigues et al. 2008; Vinn et al. 2014), and arthropods (Klompmaker et al. 2021; De Baets et  al. 2021a). Parasites, on the other hand, have been identified from among 12 phyla (Fig. 1.5). Annelids (Cameron 1969; Bromley 2004) and mollusks (Nützel 2021; De Baets et al. 2021c) comprise the parasitic taxa with the most complete time series of occurrences during the entire Phanerozoic, though a substantial portion of parasitic interactions detected on skeletal hosts are attributed to parasites

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Fig. 1.4  The Ediacaran through Neogene record of selected parasitic and facultatively parasitic organisms (*) based on the range of paleopathologies/trace fossils, body fossils, and extrapolation based on extant host associations (data updated from Baumiller and Gahn 2002; De Baets and Littlewood 2015)

of uncertain affinity. This is particularly the case when going back to the Paleozoic (Baumiller and Gahn 2002; De Baets et al. 2021a, c; Thomka and Brett 2021; Vinn and Wilson 2021).  Cameron (1967, 1969) for example  attributed a peculiar preserved annelid within a Middle Devonian bivalve boring as well as Paleozoic borings in brachiopods  as old as the Late Ordovician to spionid annelids. However, reliably identifiable spionid trace fossils associated with mudblisters  can only be traced back to Jurassic-Cretaceous or Triassic at best (Bromley 2004; Huntley et al. 2021).  Skeletal pathologies represent the oldest unequivocal evidence for metazoan parasitism in the form of tube-dwelling organisms on lower Cambrian brachiopods (Bassett et al. 2004; Peel 2014; Zhang et al. 2020). The parasitic culprits here too are unknown. In some cases, particular pathologies can be linked to parasite–host interactions with taxa that are now extinct including Phosphannulus (Welch 1976; Werle et  al. 1984) and platyceratid-echinoderm associations (Baumiller 2002; Baumiller and Gahn 2002, 2018; Webster and Donovan 2012; Donovan and Webster 2013; Thomka and Brett 2021), various bioclaustrations in Paleozoic corals and stromatoporoids (Vinn and Wilson 2021), as well as more speculative graptolite parasites (Bates and Loydell 2000). Geologically younger parasite–host associations tend to involve better known taxa and interactions. Trematode-bivalve (Ruiz and Lindberg 1989; Huntley and De Baets 2015; Rogers et al. 2018; Huntley et al. 2021), arthropod-arthropod (Klompmaker and Boxshall 2015; Klompmaker et al. 2014, 2021), echinoid-gastropod (Neumann and Wisshak 2009; Farrar et  al.

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Fig. 1.5  Genus-level occurrence of parasite–host interactions among Phanerozoic marine invertebrates. (a) Host occurrence data by phylum. (b) Parasite occurrence by phylum. Data compiled from the published literature

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2020) and polydoran annelid-bivalve/brachiopod (Blake and Evans 1973; Huntley 2007; Rodrigues et al. 2008; Riascos et al. 2009; Huntley et al. 2021) tend to dominate the Mesozoic-Cenozoic record. As the fossil records of invertebrate hosts are more continuous, they should in principle have great potential to track the association of parasitic disease (De Baets et al. 2021d). Regardless, even collectively, the studies in this area do not yet allow an adequate sample size for assessing changes in the prevalence of these pathologies over time or their relationships with environmental perturbations or extinctions in high resolution. Ideal subjects for such studies should fulfill some criteria: 1. A system with a modern analogue that can be used to understand the parasitic nature of the interaction 2. A demonstrated impact of parasitism/pathology on host populations 3. Easy recognition and attribution to a parasitic culprit 4. Possibility to quantify the prevalence of pathology in species samples 5. Sample sizes per assemblage should be adequate Trematode-bivalve interactions are one such system that meets these criteria and holds great promise for studying prevalence through time, environmental change, and extinction events (Huntley and De Baets 2015; Huntley et al. 2021). Digenean trematodes are complex-life cycle helminth parasites that infest as many as three host taxa through their ontogeny. They negatively impact their hosts in a number of ways, including castration, dwarfism, gigantism, and inducing risky behavior relative to the host’s predators—the definitive host (Ruiz 1991; Ballabeni 1995; Hechinger et  al. 2008; Swennen 1969; Lim and Green 1991; Taskinen 1998; Thieltges 2006). Trematodes induce the growth of characteristic pits and igloos on the interior of the bivalve shells—their second intermediate host—and are known from modern ecosystems, death assemblages, and the  fossil record (Ruiz and Lindberg 1989; Ituarte et al. 2001, 2005; Huntley 2007; Huntley et al. 2014, 2018, 2021; Huntley and De Baets 2015; Rogers et al. 2018). Systematic surveys have revealed that trematode prevalence tends to increase significantly during sea-level rise in shallow marine, estuarine, and lagoonal settings over centennial and millennial timescales (Huntley et al. 2014, 2012; Huntley and Scarponi 2015; Scarponi et al. 2017). These initial studies have ruled out changes in host availability, biodiversity, and community structure as drivers of this biotic response. Huntley et al. (2021) have recently used trace element composition of bivalves to test the influence of temperature, salinity, freshwater runoff, and nutrient availability in addition to testing the response of this interaction to mass extinctions. Other promising study systems involve the isopod-decapod (Klompmaker et al. 2014, 2021) and gastropod-­ echinoderm (Baumiller and Gahn 2002; Neumann and Wisshak 2009; Farrar et al. 2020; Nützel 2021; Thomka and Brett 2021) associations, and various bioclaustrations and parasites in colonial organisms (Tapanila 2008; Taylor 2015; Vinn and Wilson 2021), although these datasets still need to be further expanded (De Baets et al. 2021d).

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1.5  Conclusions The fossil record represents a relatively untapped source of information on the evolution of parasite–host interactions, even though the probability of preservation for the body fossils of parasites is often considered relatively low in comparison to other organisms. The majority of parasite fossil occurrences have been published as reports of unusual features on fossils by researchers pursuing other questions. Meta-­ analyses of these data, nonetheless, can shed light on major trends in the macroecology and macroevolution of parasite–host interactions within ecosystems. Overall, future work focused on informed and systematic screening of parasitic body and trace fossils may lead to a transformative understanding of these subjects. Well-­ maintained samples of host remains in museum collections as well as targeting field collections might be a good place to start such an endeavor (e.g., Farrar et al. 2020). Major gaps remain for particular groups as diverse as parasitic rotifers (Acanthocephala), parasitic crustaceans (e.g., amphipods and Branchiura), cnidarian Myxozoa, and lophotrochozoan orthonectids/dicyemids (De Baets et al. 2021b; Haug et al. 2021; Herlyn 2021; Okamura and Gruhl 2021). For some unicellular parasites and extremely simplified soft-bodied and unicellular organisms like Myxozoa and orthonectids/dicyemids, direct evidence of ancient parasites may never be recovered. In such cases, molecular clock approaches might provide a viable way to constrain their evolutionary history, although new developments are necessary to make these approaches robust and meaningful. For others, their absence could be related to a lack of research. Systematic efforts may rapidly help close some gaps in knowledge, as highlighted by recent discoveries of remains of acanthocephalans (Cardia et al. 2019a) and parasitic isopods (Nagler et al. 2016, 2017b; Serrano-Sánchez et  al. 2016; Haug et  al. 2021), which had previously only been known from Holocene eggs or trace fossils (Klompmaker et al. 2014), respectively. These discoveries have also instigated research into the functional morphology of parasitic isopods (Nagler and Haug 2016; Haug et al. 2021). Additional reports of insect parasitoids (Antell and Kathirithamby 2016), mites (Konikiewicz et al. 2016; Robin et al. 2016a), scale insects (Robin et al. 2016b), and ticks (Dunlop et al. 2016; Poinar 2017; Peñalver et al. 2017; Dunlop 2021) have also recently found their way into the literature. These arthropod studies demonstrate the potential value of innovative analytical methods, like X-ray microtomography (De Baets and Littlewood 2015), for critically assessing the taxonomic assignments and functional morphologies of parasites and vectors alike (Dunlop et  al. 2016; Nagler and Haug 2016; Robin et al. 2016a; Peñalver et al. 2017). Host remains in the form of coprolites or skeletal (paleo)pathologies have the great potential to study the parasite–host interactions across environmental perturbations and extinctions, but their presence needs to be established more continuously throughout the Phanerozoic and their prevalence in species samples needs to be more consistently reported. Acknowledgements  We are grateful for the enriching conversations and suggestions of many colleagues and collaborators. This research was supported by the Alexander von Humboldt Stiftung (JWH), the Friedrich-Alexander University Erlangen-Nürnberg (Emerging Talents

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Initiative Grant to KDB), the National Science Foundation (NSF CAREER EAR 1650745 to JWH; NSF CAREER 1652351 to JDS), the University of Missouri Research Council (JWH), and a Paleontological Society Arthur James Boucot research grant (to AAK).

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Waloszek D (2003) The ‘Orsten’ window—a three-dimensionally preserved Upper Cambrian meiofauna and its contribution to our understanding of the evolution of Arthropoda. Paleontol Res 7(1):71–88. https://doi.org/10.2517/prpsj.7.71 Waloszek D, Repetski JE, Maas A (2005) A new Late Cambrian pentastomid and a review of the relationships of this parasitic group. Trans R Soc Edinb Earth Sci 96:163–176. https://doi. org/10.1017/S0263593300001280 Wappler T, Smith VS, Dalgleish RC (2004) Scratching an ancient itch: an Eocene bird louse fossil. Proc Roy Soc Lond Ser B Biol Sci 271(Suppl 5):S255–S258. https://doi.org/10.1098/ rsbl.2003.0158 Warnock RCM, Engelstädter J (2021) The molecular clock as a tool for understanding host-­ parasite evolution. In: De Baets K, Huntley JW (eds) The evolution and fossil record of parasitism:Coevolution and paleoparasitological techniques. Topics in Geobiology 50. Springer Warnock RCM, Yang Z, Donoghue PCJ (2017) Testing the molecular clock using mechanistic models of fossil preservation and molecular evolution. Proc Roy Soc B Biol Sci 284(1857). https://doi.org/10.1098/rspb.2017.0227 Watson V, Rothschild B (2021) Deep origin of parasitic disease in vertebrates. In: De Baets K, Huntley JW (eds) The evolution and fossil record of parasitism: Coevolution and paleoparasitological techniques. Topics in Geobiology 50. Springer Webster G, Donovan SK (2012) Before the extinction–Permian platyceratid gastropods attached to platycrinitid crinoids and an abnormal four-rayed Platycrinites ss wachsmuthi (Wanner) from West Timor. Palaeoworld 21(3–4):153–159 Weinstein SB, Kuris AM (2016) Independent origins of parasitism in Animalia. Biol Lett 12(7). https://doi.org/10.1098/rsbl.2016.0324 Weitschat W, Guhl W (1994) Erster Nachweis fossiler Ciliaten. PalZ 68(1-2):17–31 Welch JR (1976) Phosphannulus on Paleozoic crinoid stems. J Paleontol 50(2):218–225 Werle NG, Friest TJ, Mapes RH (1984) The epizoan Phosphannulus on a Pennsylvanian crinoid stem from Texas. J Paleontol 58(4):1163–1166 Wienberg-Rasmussen H, Jakobsen SL, Collins JSH (2008) Raninidae infested by parasitic Isopoda (Epicaridea). Bull Mizunami Fossil Mus 34:31–49 Williams JD, Boyko CB (2012) The global diversity of parasitic isopods associated with crustacean hosts (Isopoda: Bopyroidea and Cryptoniscoidea). PLoS One 7(4):e35350. https://doi. org/10.1371/journal.pone.0035350 Wilson GD, Paterson JR, Kear BP (2011) Fossil isopods associated with a fish skeleton from the Lower Cretaceous of Queensland, Australia–direct evidence of a scavenging lifestyle in Mesozoic Cymothoida. Palaeontology 54:1058–1063. https://doi. org/10.1111/j.1475-­4983.2011.01095.x Wolff EDS, Salisbury SW, Horner JR, Varricchio DJ (2009) Common avian infection plagued the tyrant dinosaurs. PLoS One 4(9):e7288. https://doi.org/10.1371/journal.pone.0007288 Wood JR, Wilmshurst JM (2014) Late Quaternary terrestrial vertebrate coprolites from New Zealand. Quat Sci Rev 98:33–44. https://doi.org/10.1016/j.quascirev.2014.05.020 Wood JR, Wilmshurst JM (2016) A protocol for subsampling Late Quaternary coprolites for multi-­ proxy analysis. Quat Sci Rev 138:1–5. https://doi.org/10.1016/j.quascirev.2016.02.018 Wood JR, Wilmshurst JM, Worthy TH, Holzapfel AS, Cooper A (2012) A lost link between a flightless parrot and a parasitic plant and the potential role of coprolites in conservation paleobiology. Conserv Biol 26(6):1091–1099. https://doi.org/10.1111/j.1523-­1739.2012.01931.x Wood JR, Wilmshurst JM, Rawlence NJ, Bonner KI, Worthy TH, Kinsella JM, Cooper A (2013) A megafauna’s microfauna: gastrointestinal parasites of New Zealand’s extinct moa (Aves: Dinornithiformes). PLoS One 8(2):e57315. https://doi.org/10.1371/journal.pone.0057315 Yao Y, Cai W, Xu X, Shih C, Engel MS, Zheng X, Zhao Y, Ren D (2014) Blood-feeding true bugs in the Early Cretaceous. Curr Biol 24(15):1786–1792. https://doi.org/10.1016/j. cub.2014.06.045 Yu T, Kelly R, Mu L, Ross A, Kennedy J, Broly P, Xia F, Zhang H, Wang B, Dilcher D (2019) An ammonite trapped in Burmese amber. Proc Natl Acad Sci U S A 116:11,345–11,350. https:// doi.org/10.1073/pnas.1821292116

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Chapter 2

Importance of Data on Fossil Symbioses for Parasite–Host Evolution Ninon Robin

Abstract  Because it is biased compared to the reality of ancient life, the fossil record requires specific terminology when dealing with possible ancient biological associations of organisms. Among the range of interactions between ancient organisms, paleosymbioses are noticeable representatives of paleoecological diversities and key elements to understand the evolution of lineages over time. They may provide evidence for unsuspected associations because they involve extinct organisms or simply because they are not maintained anymore among modern representatives. They may allow one to constrain the evolution of organisms by dating the ancestry of large lineage pairings over time and are often a favorable material to discover ancient minute-sized phyla. When sufficiently expressed over time and lineages, paleosymbioses can inform directly on large biological questions (e.g. selection toward life cycle diversity), but also on ecological issues (e.g. the general processes that lead to the internalization of a symbiont). Consequently, paleosymbioses are highly worthwhile components of the paleontological record. Keywords  Paleosymbioses · Fossil associations · Symbiosis · Parasitism · Syn-vivo · Post-mortem · Selection · Ancestry · Continuum · Fitness

2.1  Importance of Meanings to Address the Fossil Record The field of biological associations includes a rich terminology utilized by neontologists (Moran 2007; Miller and Spoolman 2012; Martin and Schwab 2013; Morales-Castilla et al. 2015). This terminology aims to define categories within the broad spectrum of biological associations. Most of these categories seem to be N. Robin (*) School of Biological Earth and Environmental Sciences, University College Cork, Cork, North Mall, Ireland Centre de Recherche en Paléontologie, Paris (UMR 7207 Sorbonne Universités, MNHN, UPMC, CNRS), Muséum National d’Histoire Naturelle, Paris, France

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 K. De Baets, J. W. Huntley (eds.), The Evolution and Fossil Record of Parasitism, Topics in Geobiology 50, https://doi.org/10.1007/978-3-030-52233-9_2

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based on the evolutionary success of both organisms through living in association. This success is known to vary throughout the evolutionary history of associations. The objective variations of this selective value may be assessed from modern associations by the observation and quantification of the reproductive success of organisms, or their success at colonizing new niches over a series of generations (see Lewis 1985; Combes 2001). When attempting to investigate ancient biological associations using fossilized associations of organisms, these elements are not easily available due to the limitation of fossil occurrences (see Zapalski 2011; Littlewood and Donovan 2003; De Baets et al. 2021b). As a result, dealing with fossil associations requires the use of terms encompassing a range of different types of associations that could secondarily be identified thanks to the accumulation of fossil occurences. Fossil associations (i.e. contacts between organisms) do not necessarily result from syn-vivo associations but potentially also from the (1) post-mortem colonization of an organism carcass  by another one, (2) colonization of resedimented remains before diagenesis, or even (3) the establishment on already diagenetically transformed organisms. When involving marine organisms, type (1) has been referred by Taylor and Wilson (2002) as an epi/endoskeletobiosis. The term opposes to epi/endozoobiosis designating a syn-vivo association, and is suitable to post-­ mortem colonization in all other types of environments. I use and recommend using this terminology over that of epibiont (or -zoa)/epicoles (Davis et al. 1999) which evidenced previous confusions about the nature of the “biont” (or “-zoa”) partner (host or substrate, see Taylor and Wilson 2002).

2.1.1  Symbioses and Paleosymbioses as Primary References For epistemologists, the usage of symbiosis still is a puzzling case within biological concepts. Interactions between organisms and their environment characterize the so-called ecological relationships, at the base of ecology and therefore of paleoecology. Ecological relationships encompass both organism-abiotic components and organism–organism interactions, the latter defining interspecific relationships, also called biological interactions (see Starr 1975). Among the latter, some involve a direct contact between the organisms characterizing the biological associations in which contact can include a variety of forms. The term symbiosis—and its multiple confusing usages—originates within the spectrum of these biological associations. In evolutionary biology, symbiosis is a decisive concept; it has indeed been an important driver of the complexity of organic systems along with the progressive association of the simplest structures (see Douglas 1994; Sapp 1994, 2010; Margulis 2008; Selosse 2000; Peacock 2011; Lipnicki 2015). However, the usage of symbiosis often implies variations of meaning that are specific to the studied field, most of the time out of authors awareness (e.g. degree of organisms’ interdependency, relative impact on organisms). These differences result from 130  years of confusing usage of a term described as one of the main enigmas of the history of biological

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terms by Martin and Schwab (2012). They carried out the historical review of the term usage and evidenced various trends over time with a global one among biologists adapting the term to the needs of their own research field, which is problematic when these needs differ from the purpose of the original term (see Goff 1982). Symbiosis was introduced by the German botanist and physiologist Anton De Bary in 1879. He described it as the “living together of dissimilarly named organisms” (p. 5). To this stage, the definition was in no aspect prejudging the effects of the association caused to the partners. De Bary’s expertise in vegetal pathologies though implies he would have been fully aware of the harmful and beneficial relationships between symbiotic organisms (Douglas 1994), but he did not include these notions into his definition. He did include however in his definition several types of complex associations belonging to a continuum getting from parasitism and commensalism to mutualism (Sapp 1994, see Fig. 2.1). De Bary’s original statement itself relied on the Latin term Symbiotismus already suggested two years before by the German physiologist Albert Frank (1877). The term defined “an integrative concept focusing on the role played by both individuals and based on the simple coexistence of the two different species, one living on, or inside the other”. There is therefore no ambiguity on the original meaning of symbiosis: an association of organisms. Other and less precise usages of that term, however, exist. Indeed, if the first definition of Frank (1877) clearly mentions a contact between the partners (“on” or “inside”), that of De Bary was vague about this aspect, which has been misleading

Fig. 2.1  Heuristic scheme combining the eight criteria proposed in Starr (1975) on which symbioses can be categorized through a continuum. Criteria 1 and 2 (relative fitness for symbionts; duration of the symbiosis) are the most used by biologists for the categorization of associations; then come criteria 7 and 5 (dependence of symbionts and specificity). We note here that the criteria of specificity could be refined depending on biological entities (individuals, species and more inclusive taxa). Reformatted after Lewis (1985)

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subsequent authors about the necessity of a symbiosis to imply or not a direct contact between symbionts. Another criterion is “durability” of the association, which is adressed in none of the two original definitions. Despite that lack, many authors interpreted the symbiosis as excluding short-term associations like pollination of flowering plants by insects (protocooperation; Scott 1969; Douglas 1994) while others chose to include them. But the main confusion on its definition still has relied on its assimilation to the notion of reciprocal benefit, i.e. to mutualism. Hertwig (1906) was the first to use it with this meaning. This confusion seems to have appeared without reason, like a simple historical mistake (Ahmadjian and Surindar 1986). That was the beginning of 70 years of common usage of symbiosis in the meaning of mutualism with and without reference to De Bary’s original definition (see Hegner et al. 1938; Caullery 1950; Scott 1969). This misunderstanding subsequently developed with the attempt of formalization of the term in 1937 by the American Society of Parasitology (Hertig et al. 1937). Although it acknowledged the broad meaning proposed by De Bary’s definition, the society did not express any official recommendation, thereby authorizing biologists to keep on defining symbiosis following their own preferences. From this time until today, some authors tried to return the term to its original meaning, i.e. whatever interspecific association (including predation, competition and even sometimes saprophagy, that is at the boundary with asymbiosis; see Lewis 1985). Finally, we observe in the last 40 years an increased return to De Bary’s definition (Martin and Schwab 2012) with textbooks defining symbiosis in its original meaning (see Walter and Proctor 2013). Given the difficulty to identify and categorize fossil associations at first sight, it appears necessary when dealing with their study to have a terminology that could (1) encompass their potential diversity and (2) exclude at the same time purely taphonomic associations between species. The term symbiosis in its original meaning exactly covers this range of associations and provides a perfect framework to define “an ancient biological association between organisms dissimilarly named” as a paleosymbiosis. The potential of paleosymbioses for the study of the evolution of ecological interactions is the purpose of this chapter.

2.1.2  Parasitism as Subclass of Symbioses A new vision in the categorization of symbioses emerged in the late 1970s, with Starr’s model (Starr 1975; Fig. 2.1). The latter considers that all possible associations rank along a continuum based on eight different criteria, later refined by Lewis (1985; Fig. 2.1). These criteria are for instance (1) the interdependance of symbionts, (2) the engaged trophic relation, (3) the duration of the association or (4) the type of contact engaged. Despite this vision encompassing a variety of criteria, the most widespread type of categorization only relies upon two of them: the association duration and its impact on the selective value of the partners (compare Conway-­ Morris 1990). This second feature, also called fitness, can be observed at many

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levels: anatomical, physiological, reproductively, locomotory, food availability (Fig. 2.1). The relative fitness of an association is the combination of each partner’s fitness (negative, positive or neutral), with positive versus negative effects defining the parasitism. The semantics of parasite refers in its Greek origin to one host sharing the table of another (para = near; sitos = food). This term has been transposed into the natural world by Van Beneden (1875) in reference to the social behavior of parasites. He described the parasite through its “ability to live at the expense of its neighbour, exploiting it with economy without impending over his life” (p. 83). Many subsequent authors have defined the parasitism through its harmful impact over one partner while benefiting to the other (Leuckart 1879; Brumpt 1913; Whitfield 1979; Lewin 1982; Zapalski 2007; Caullery 1950) in addition to other criteria (e.g. the dependence of the parasite on its host, the engagement of the parasite in a trophic relationship). This extra meaning again appeared unconsciously, often without being explicit in authors’ writings. Some others chose to consider parasitism as a synonym of symbiosis, without integrating any notion of benefit or pathogenicity (e.g. Baker 1994). In order to use a sufficiently self-explicit meaning, we choose to use in this chapter parasitism in unique reference to the combination of a positive versus a negative fitness for associated organisms. Therefore, criteria of long-lasting interaction, food-mediated relation or dependence onto the host are excluded from our herein usage of parasite (compare Conway-Morris 1990; Zapalski 2011).

2.2  Evidence of Past Symbiotic Interactions As fossilized organisms give insights into past biodiversity, fossil symbioses provide a window onto the reality of ancient ecological interactions (Boucot 1990a, b; Boucot and Poinar 2010). By evidencing direct contacts, paleosymbioses are even the most direct testimony of these interactions, which can most of the time only be inferred from the co-occurence of organisms in the same sedimentary layer. These ecological interactions may have been different from those existing nowadays, although this degree of difference is a relative concept. Paleosymbioses may distinguish from modern symbioses in the partners they involve. They may for instance involve taxa extinct today, both as host and symbiont. But their identification as extinct types of symbioses is far from being unbiased—most extinct associations might also simply have gone unnoticed.

2.2.1  Involving Extinct Taxa Identifying a fossil association as a paleosymbiosis often relies on the fact that a possible host—today extinct—displays a phenotype that is relevant to the needs of the associated second taxon, itself known for performing nowadays its life in

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symbiosis. In this context, and if other clues support a syn-vivo interaction, paleosymbioses involving extinct hosts can be identified. As Hosts The most readily accepted cases are those involving sessile symbionts, for which the modalities of hard substrate selection (settlement and recruitment) are most of the time only generally understood in modern environments (see Wahl 2009). It encompasses organisms like bryozoans or tabulate corals that were easily identified as the epizoans of many extinct organisms including hyoliths (Galle and Parsley 2005), nautiloids (Wyse Jackson and Key 2014) or trilobites (Brandt 1996), usually from their specific distribution on exoskeletons. Cemented bivalves (e.g. gryphaeids or anomiids) or even barnacles have been easily interpreted as the commensals of ammonites or extinct mecochirid lobsters based on certain criteria (Hauschke et al. 2011, Ifrim et al. 2011, Misaki et al. 2014, Robin et al. 2016a, Hautmann et al. 2017). This is also the case of brachiopods identified as the commensals of different motile organisms: the Cambrian Wiwaxia (Topper et al. 2014), the eldonioid Rotadiscus (Dzik et al. 1997) or Jurassic extinct crustaceans (eryonoids, Audo et al. 2019). Likewise, Peñalver et al. (2017) managed quite directly to identify Cenomanian ticks in amber as the ectoparasites of non-avian dinosaurs, as well as Poinar and Boucot (2006) identified endoparasitic helminths from presumed dinosaur coprolites. Cases of ancient epi/endoskeletobioses are also easily interpreted when the extant representatives of the fossil taxa are known to have a typical symbiotic behavior. An eloquent example is the association of an Early Cretaceous hermit crab from the Speeton Formation, UK, found inside the inhabitation chamber of an ammonite (Fraaije 2003; Klompmaker and Fraaije 2012). From this very first insight and the absence of in situ fossil hermit crabs in gastropod shells before the Late Cretaceous, Fraaije, suggested a shift in paguroid inquilinism from cephalopod hosts (ammonites) to gastropods over this transitory period. Comparable observations were led on ammonite body chambers hosting other crustaceans like lobsters (Glypheidea and Erymidae) that are thought to have used dead ammonite remains as food source and shelter (Posidonia Shales of Dotternhausen for the Toarcian; Portland Limestones for the Tithonian; Fraaye and Jäger 1995). From the Tithonian, it has also been inferred that caenogastropods used ammonite body chambers to deposit their egg capsules (Zatoń and Mironenko 2015). As Colonizers Contrary to the above types of fossilized associations, identifying symbiotic behaviors in extinct colonizing organisms is much more difficult. It strongly relies on (1) the clear observation of their impacts on the host, like growth anomalies, (bio)erosion or perforation; (2) their location on this host; and (3) the existence of an

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equivalent behavior among their modern relatives. For instance, in the case of the infestation of echinoderms (crinoids, cystoids and probably blastoids) by the extinct platyceratid gastropods, parasitism has been inferred from drill holes penetrating the echinoderm skeletal plates (Baumiller 1990, 1993, 1996, 2002; Baumiller and Macurda 1995; Baumiller and Gahn 2002; Gahn et al. 2003; Gahn and Baumiller 2003). The same relationship has further been evidenced on brachiopods from boreholes displayed by Palaeozoic representatives (Baumiller et al. 1999; Deline et al. 2003). For those cases, the relevance of the relation is supported by the fact that modern capulid gastropods display comparable behaviors on modern epifaunal bivalves, and occasionally on gastropods, brachiopods or annelids (Baumiller et al. 1999). Aside of these examples, the intergrowth of sessile colonial organisms (e.g. corals, sponges, bryozoans) and preservation of soft-bodied symbionts by bioclaustration (i.e. by mould in the host skeleton) may allow the recognition of associations between extinct groups of colonizers (e.g. Vinn et al. 2015; Vinn 2017; Vinn et al. 2017; Vinn and Wilson 2021) as well as the inference of some feeding and developmental impacts (see Taylor 2015). Besides these specific—but numerous and diverse—cases, the understanding of the behaviors of extinct organisms is limited to traditional sessile foulers. For example, extinct trepostome bryozoans or cornulitids could be interpreted as the commensal epizoans of Ordovician cephalopods or as sessile animals (conulariids and cornulitids; Baird et al. 1989, Gabbott 1999, Wyse Jackson and Key 2014, Vinn and Wilson 1995, Vinn et al. 2018, 2019). In General If actualism is the only tool that palaeontologists have to interpret (1) fossil associations of two species and (2) damage on the associated organisms, it may also be a source of biases. Indeed, it cannot be excluded that some interspecific encountering/ associations (the less intricate ones) occurred several times in the history of their lineages. These occurrences could have provided a more or less selective value to the partners, with sometimes quite high levels of interaction that simply have not been further selected. Therefore, paleosymbioses might have been much more superficial or intricate than in their modern close representatives, but we might not necessarily be able to detect it. Despite such limitations, by studying large samples, it is also possible to disentangle the potential impact of extinct symbionts on their hosts (e.g., kleptoparasitic tubes of unknown affinity encrusting Cambrian brachiopods; Zhang et al. 2020). This is especially obvious when dealing with host and colonizer differing much from their extant representatives like the extinct Palaeoscolecidae (Ecdysozoa, Cycloneuralia) colonized by extinct protostomes (potential stem gnathiferans: Herlyn 2021; Vinther and Parry 2019) from the Early Cambrian of Chengjiang, China (Cong et al. 2017). With this finding, the original authors tentatively identified the interaction by elimination, estimating probable hindering for the host (inhibited locomotion but no perforation of the cuticle) and potential benefits for the colonizer (facilitate dispersal, protection, access to food). In this case, the suggested

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benefits rely on general ideas about living as an ectosymbiont, which actually can be much more specialized and complex depending on the species. This shows us that when a fossil association involves extinct hosts and colonizers that differ much from their extant relatives and do not especially live in symbiosis, very little can be inferred with confidence about the relationship, even if this one was in fact highly specialized. Only very striking morphological features could help in determining a certain degree of relationship. This observation limits questions on (1) the constancy of types of biotic interactions over time, (2) the rapidity of the associations’ apparition in environments differing from extant ones and finally (3) the possibility to access these elements by strict actualism.

2.2.2  Unreported in Modern Nature Paleosymbioses can also involve colonizers and hosts existing today without their association having ever been reported. These paleosymbioses may illustrate associations that had a specific biological meaning in the past, but no more in modern ecosystems. More commonly, they correspond to associations that are likely to exist in modern environments and have simply never been reported. Poinar et  al. (1997) reported the Cretaceous case of an erythreaid mite (Trombidiformes, Acari) on a chironomid midge (Culicoidea, Diptera), a relation not reported today. In this case, the amber preservation caught the mite mouthparts attached onto the host abdomen node, arguing for its syn-vivo feeding position. The authors explained the unique fossil representation of this relationship by the fact that erythreaid host habitats were less determined in the Cretaceous and that the chironomid physiological responses for avoiding parasitism by erythraeid mites must have appeared later. The association of a probable pentastomid on a Silurian ostracod displaying no modern counterpart has been determined as a case of ectoparasitism (Siveter et al. 2015; see also De Baets et al. 2015; Haug et al. 2021; Klompmaker and Boxshall 2015; Klompmaker et al. 2014, 2017 for alternative opinions). The original authors suggested that the parasitic relationships of pentastomids must have originated along a progressive level of integration, starting with early ecto- and mesosymbiosis (integration into open organs like gills) with marine invertebrates since at least the Silurian, toward the endosymbiosis with modern terrestrial tetrapods. They suggested that the observed external attachment may have represented an early life stage, preceding a second for which the pentastomid would have migrated into the ostracod domicilium, a favorable site for the colonization of ostracods by modern arthropods. The authors did not exclude the possible ongoing existence of the relationship nowadays, but other authors argued they were possibly extinct if the attached structures actually represent pentastomids (De Baets et al. 2015; De Baets and Littlewood 2015).

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Likewise, Robin et  al. (2013) identified some nubeculariid foraminifera (Miliolina, Foraminiferida) as encrusting ectosymbionts of the carapace of Late Jurassic lobsters (Erymida, Astacidea). Symbiotic foraminifera have never been reported on modern decapod crustaceans, neither internally nor externally. The authors argued that the relationship could still occur in extant reefal decapods, generally underexamined for their microscopic ectosymbioses. The latter consideration relies on the fact that, for a long time in the study of natural history, specimens sampled for collections and studied for their taxonomy were almost systematically cleared of their ectosymbionts, limiting the reports of many interactions, although possibly collected (see Waugh et al., 2004, for biases in decapod crustaceans). This can be illustrated by the report by Robin et al. (2015a, b) of ectosymbiotic calcifying bacteria on the carapace of Jurassic bathyal shrimps that had no modern counterpart at first sight. After examining carefully hundreds of samples of modern comparable groups (Penaeoidea) kept in collections, the authors found the modern counterparts of these bacterial colonies, strikingly comparable in morphologies and distribution on their hosts. Likewise, in terrestrial habitats, possible phoretic behaviors in springtails have been reported from occasional fossil occurrences (Poinar 2010; Penney et al. 2012; Grünemaier 2016), last report in date emphasizing a full group of 25 springtails attached on an alate termite and ant from Dominican amber (Robin et al. 2019b). This type of association has never been reported among modern springtails. However, this association is proposed to be at the origin of the worldwide dispersal of symphypleonan springtails over time, a dispersal mechanism that should, in all likelihood, continue today and even be quite common. Contrary to slower phoretic wingless arthropods (acari and pseudoscorpions), the reflexive detachment of springtails’ appendages of attachment (antennae) would have hindered their observation through traditional collecting techniques used in entomology. In this context, the immediate embedding by tree resin of springtails on insects would characterize a unique situation enabling the preservation of these associations, making amber fossils of high significance to document sometimes still ongoing associations (Robin et al. 2019b). The absence of a modern counterpart for a paleosymbiosis in which both partners are still existing is very differently interpreted depending on authors, and seems highly dependent on the type of interaction involved. Differences rely on the fact that specialists of the intricate parasitic relationships more easily refer to low taxonomic ranks to compare relationships (e.g. the family level; Boucot 1990a, b, Poinar et  al. 1997), whereas researchers focusing on commensal interactions, like fouling, often compare interactions at much more inclusive clade scales. There are also variations in the vision of interactions between specialists of the terrestrial and marine realms. Scientists generally show more proclivity for recognizing important knowledge limits when working on marine ecosystems, where interactions are often less characterized or understood, than on terrestrial ones (Lafferty and Kuris 2002; McNamara Jones 2007).

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2.3  Constraints on the Evolution of Associations Besides permitting access to the patterns of unknown ancient interactions, paleosymbioses can also enable one to document their evolution over time and sometimes even to understand part of the processes behind their evolution.

2.3.1  Ancestry of Organisms and Associations At the phylum level, paleosymbioses can provide direct evidence for the timing of associations between taxa, but also for the age of particular taxa themselves. Indeed, contrary to sediments that could never be exhaustively investigated for their content in minute organisms of low potential of preservation, larger fossil organisms are especially worthy material for the detection of potentially preserved inconspicuous taxa. As an example, old traces of unicellular eukaryotes and bacteria are retained through preservation in association. Those were recovered from the guts of early Cretaceous and Miocene termites trapped in amber (Dominican amber, Wier et al. 2002; Burmese amber, Poinar 2009), representing the earliest direct record of mutualism between microorganisms and metazoans. The identification of identical flagellate groups (Trichomonada, Hypermastigida and Oxymonada) in early Cretaceous and modern insects confirmed that these xylophagous endosymbionts had been inherited from associations much older than the oldest termites (Poinar 2009). The oldest endosymbiotic bacteria are so far known from the guts of Miocene termites (Wier et al. 2002), questioning the timing of bacterial integration into the process of wood digestion by termites. The oldest known fossil nematode was evidenced thanks to its association with the oldest terrestrial plants (non-tracheophyte). It was found dwelling into the stomatal chamber of the Devonian Aglaophyton (Rhynie cherts, Scotland; Poinar et al. 2008; see also De Baets et al. 2015; De Baets et al. 2021a). Likewise, the so far oldest fungi are reported from silicified paleosymbioses. Indeed, the oldest ascomycetes are recovered through asci hosted in the vascular tissues of Devonian lycophytes (Aglaophyton; Rhynie cherts, Scotland; Taylor et al. 2003), and the oldest basidiomycetes from hyphae and reproductive structures in the stem of late Carboniferous ferns (Botryopteris; Esnost cherts, France; Krings et  al. 2011; see Harper et al. 2019; Harper and Krings 2021). The oldest observations of flatworms (Platyhelminthes) also correspond to preservations onto or inside ancient hosts. Indeed, aside of the case of cestode eggs preserved into Permian coprolites of elasmobranchs (Dentzien-Dias et  al. 2013), trematode flatworms are evidenced to be at the origin of igloo-like deformations in the pallial region of bivalve shells, as described from modern homologous structures (Ituarte et al. 2001, 2005). These deformations can be confidently traced back to the Late Cretaceous and potentially even further to the Silurian (De Baets et al. 2015; Rogers et  al. 2018). Putative remains of flatworm hooks are also reported attached onto the tegument of Devonian gnathostomes (Upeniece 2001).

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Among marine symbiotic lineages, a dozen of tiny—less than a millimetre— copepod crustaceans were reported from the gill cavity of an early Cretaceous teleost (Santana Formation, Brazil; Cressey and Patterson 1973, Cressey and Boxshall 1989). They are the oldest body fossils of these crustaceans, with cysts attributed to parasitic copepods being already reported from marine invertebrates since the mid-­ Jurassic (see Radwańska and Radwański 2005; Klompmaker and Boxshall 2015). These fossils indicate the rapid engagement of copepods in symbioses with both vertebrates and invertebrates. Likewise, in terrestrial environments, mites, which have occasionally been reported from Devonian sediments (Norton et  al. 1988; Subías and Arillo 2002), display one of their oldest members preserved as a paleosymbiont. It corresponds to a one mm oribatid mite (acariform) on the thorax of a Carboniferous relative of grasshoppers, crickets and katydids (Ningxia, China; Robin et al. 2016b). The mite is suggested to have died in its original sequestered position on the insect, revealing the extent to which life in association with larger organisms arose early in the evolution of mites.

2.3.2  Evolution of Associations over Time  eneral Rules in Species Encountering, Attachment G and Symbiont Internalization If it is nowadays well accepted  that associations range along a continuum (Sapp 1994) with evolutionary transitions of these associations from one category to another, the process of these transitions remains almost untested. These transitions are suspected to have occurred following a constant pathway—naturally selected— from the least (neutralism, commensalism) to the most intricate types of symbioses (mutualism and parasitism) once a significant benefit arose for one partner (see Lewis 1985, Combes 2001, Poulin 2011, Fig. 2.1). These transitions may/may not fit with direct nutrition on the host/victim. But when it occurs, it is often along with a transition toward (1) the internalization of one of the symbionts (criterion of integration), (2) the decrease in size of one of the symbionts (criterion of relative size), (3) the permanency of the association (criterion of duration), and therefore (4) the obligate and (5) high degree of specificity of the association (criteria of interdependency and specificity, Fig. 2.1). But how fast these different features arise and stabilize in the history of associations through natural selection is very superficially considered. Are there general rules governing the rise of all types of associations between organisms (type of contact, nutritive benefit)? To what extent do different (1) environments (aquatic vs. terrestrial) and (2) phyletic contexts impact the scenarios of associations over time between comparable partnerships? How fast are behaviors selected through genetics in addition to morphology? These aspects can be addressed from the extensive study of paleosymbioses (see Robin 2015; Nagler et al. 2017). Modern marine lice, i.e. isopod crustaceans, display a variety of lifestyles related to their various feeding habits. With the exception of Epicaridea, which live in the

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branchial chamber of decapod crustaceans, most parasitic isopods belong to the clade Cymothoida (Brandt and Poore 2003) and are found on or in actinopterygians. Therefore, the understanding of anatomies within cymothoid groups is expected to provide information on their adaptation to multiple carnivorous behaviors, including parasitism. Aside of being scavengers, predators and more or less temporary parasites, many cymothoids are also known to perform micropredation on larger hosts (see Poore and Bruce 2012). Micropredators distinguish from parasites in their ability to take their meals from several victims in one life stage, whereas parasites stay on a unique host during their larval and adult stages (Lafferty and Kuris 2002). From phylogenies (Brusca 1991; Brandt and Poore 2003) and analysis of Cretaceous isopods found isolated and their close extant relatives, some adaptations of their buccal/limb appendages to an attached lifestyle were identified (see Nagler and Haug 2016; Nagler et al. 2017). Although most of the time it is the case, evidences for possible attachment do not necessarily attest to ancient behaviors (innovations not always being directly selected), making observations of fossil associations other substantial elements to document the evolution of symbioses. Cases of cymothoid body fossils attached to larger organisms have been differently interpreted by paleontologists. Until recently, they were only mentioned, without attempt from the authors to analyse the meaning of the association (Frickhinger 1999; Polz 2004; Polz et al. 2006). Recently, fossil Cirolanids—that are saprophagous today—were identified scavenging a Cretaceous actinopterygian (Wilson et  al. 2011), and a second case involving Eocene numbfishes (Chondrichthyes, Batoidea) was interpreted as an equiprobable situation of scavenging or micropredation from various types of criteria (Robin et  al. 2019a; Fig. 2.2a, b). For ancient syn-vivo interactions, only the case of early Cymothoidae whose deformed bodies were supporting a long-lasting residence on their living host (late Jurassic teleosts), and that of the isolated Cretaceous Urda, enabled the identification of fossil parasitic behaviours among Cymothoida (Nagler et  al. 2016, 2017). Consequently, patterns of (1) morphologies and (2) host/victim selections over time were demonstrated from the study of paleosymbiotic cases. However, most elements documenting the steps and the time frame of their internalization into their vertebrate or invertebrate hosts, as well as the role of larvae in this process, remain unknown. This is partly explained by the fact that no epicarid body fossil has ever been found within the swellings of fossil crustaceans (not preserved internally, see Klompmaker et al. 2017, pers. obs. 2018 from CT scan tests) nor other isopods from gills of fossil actinopterygians. Patterns of internalization are easier to identify in cases of epi/endoskeletobioses where the host—a dead corpse—opposes no answer to the endobiont progression. This is for instance the case of xylophagous bivalves (including shipworms) that are obligate colonizers of drifted and floating woods. Their evolution corresponds to an adaptation to wood as food and habitat. The use of the shell as a wood drill has resulted in its reduction over time, whereas the animal soft parts have extended and migrated posterior to it, giving the bivalves a vermiform body plan. The progression of the bivalves within dead wood over time is documented by woods drilled and

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Fig. 2.2  Exemplified cases of fossil associations of invertebrates, vertebrates and plants from aquatic (a–f) and terrestrial (g–j) ecosystems. (a, b) Isopods on Eocene numbfishes from Monte-­ Postale, Bolca, Italy. (a) The large numbfish Titanonarke molini, Jaekel (1894), exhibiting 1 cm large isopods (MCSNV IG.135576). (b) Cirolana titanophila, Robin et  al. (2019a), displaying heads (green), thorax (yellow), pleon (blue) and telson (purple), performing scavenging or micropredation onto the numbfish body (MCSNV IG.135576B-C). (c–f) Xylophagous (Robin et  al., 2018) (shipworm-like) bivalves preserved in silicified Cenomanian logs of the Vienne department, France. (c) Wood log specimen showing emerging bivalves (UP.SCF.17.002). (d) 3D reconstruction of (c) showing the internal distribution of preserved bivalves (green) and empty burrows (brown). (e) Exceptionally preserved bivalve emerging out of the log UP.SCF.17.001. (f) 3D reconstruction of the (e) individual showing the preserved visceral pouch (red) extending posterior to the shell (yellow), an anatomical adaptation to life inside wood. (g–j) A minute acari on a Pennsylvanian Archaeorthoptera from Ningxia, China. (g) Specimen CNU-NX1-171 of Miamia maimai, Béthoux et al. (2012), displaying a 0.8 mm long mite. (h) Interpretative drawing of (g). (i) SEM view of the oribatid mite Carbolohmannia maimaiphilus, Sidorchuk and Robin (Robin et al. 2016b). (j) 3D reconstruction of (i). Squares show the location of the symbiont on their larger hosts. Scale bars = 200 mm (a); 50 mm; (e, f); 5 mm (b, e–h); and 0.25 mm (i, j)

calcareous lined burrows, respectively, reported up to the Lower and Upper Jurassic (Kelly 1988; Vahldiek and Schweigert 2007; Schweigert and Schlampp 2014). In order to document the adaptations of the bivalves to their woody environment, shelly and soft tissues both need to be observed, which is limited in fossil occurrences. When both are preserved, the shell and soft parts can even display internal

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organs (see Kiel et  al. 2012; Robin et  al. 2018). Lately, internal structures were investigated with tomography on bivalves preserved with soft parts and shell in midCretaceous small logs of France (Fig.  2.2c–f). The preserved viscera, extending much posteriorly to the shell, attested to the advanced adaptation of these early shipworms to endoxylophagy (Robin et al. 2018, Fig. 2.2e, f). Traits of transitory internalization could be expected in earlier representatives that would display both soft and mineralized structures preserved. In the cases of symbiotic isopods or skeletobiotic bivalves, the encountering and internalization of the symbionts over time have occurred in aquatic systems. Are interactions that originate in a terrestrial environment expected to undergo the same rules? Are the larvae expected to have the same impact on the host colonization in terrestrial ecosystems and does the selection of interspecific associations follow the same types of pressures? As for fossil mites preserved in association with larger organisms, most records correspond to preservation in amber (see Poinar 1985; Kosmowska-Ceranowicz and Konart 1989; Poinar and Grimaldi 1990; Poinar et  al. 1991, 1997; Dunlop et  al. 2012, 2013, 2014). As a consequence, they are limited to Mesozoic-Cenozoic with the earliest records on feathered dinosaurs from the early Cretaceous Burmese amber for vertebrates (Peñalver et al. 2017), and on late Cretaceous scale insects from the Siberian amber for invertebrates (Magowski 1995). As they exhibit characteristics of derived parasitic families, the Cretaceous symbiotic mites were easily interpreted as blood suckers. But how did mite behaviors evolve through time to originate adaptations such as obvious feedings on hosts? The role of phoresy, namely an association in which an organism benefits of migrating from its natal habitat while attached to an host for some portion of its lifetime (Farish and Axtell 1971), is to this end of primary interest; especially given that larvae do not face the same constraints for substrate selection in the terrestrial realm than in aquatic environments. This aspect must have affected the selection of terrestrial dispersive strategies in a certain way, making data on Palaeozoic mite associations especially worthwhile. One has recently been reported from the Pennsylvanian of China with a 0.8 mm mite preserved as imprint on an extinct relative of grasshoppers, crickets and katydids (Robin et al. 2016b, Fig. 2.2g–j). The attached mite was an oribatid, a group mostly known today as free-living saprophages, although representatives are found on various invertebrates and vertebrates (Lindquist 1975; Miko and Stanko 1991; Townsend et al. 2008; Beaty et al. 2013). Taphonomic data, as well as mite location, argued for its syn-vivo attachment on the insect, showing that phoretic behaviors (temporary or long-lasting) were performed by adult oribatids as early as 320  Mya ago (Robin et  al. 2016b). But how this phoresy has been selected depending on acari/host lineages is totally unknown. When documented enough, paleosymbioses could inform about the arachnid morphotypes that supported the first acquisitions leading to parasitic attachment. This could also address (1) if life cycles with metamorphosis would have emerged in the context of phoresy and (2) which have been the constraints that made the phoresy emerged twice into arachnids, given the possible polyphyly of mites (Parasitiformes and Acariformes).

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Resistance Stages and Symbiotic Lifestyles Besides being essential to dispersion, the multiplicity of life stages in organisms’ life cycles may also be considered as an innovation to the symbiotic lifestyle, with life stages displaying adaptations to attachment or specific resistance to the inner hostile environment of some hosts. Resistant life stages are likely to be preserved as fossils (see Dufour and Le Bailly 2013; Camacho et  al. 2018; Chin et  al. 2021; Wood et al. 2013 for sub-recent) and therefore to be recovered in fossilized associations, providing insights onto the shaping of organisms’ life cycles over time along with the recovery of ancient symbiotic behaviors. Resistant structures include eggs and cysts, the latter corresponding to dormant or resting stages of the organism. Parasite eggs are reported up to the late Carboniferous preserved in coprolites (Zangerl and Case 1976; Dentzien-Dias et al. 2013). The oldest amoeba corresponds to a fossil cyst preserved in Cretaceous theropod faeces (Poinar and Boucot 2006). But cysts can also be recovered from even more internal parts of their host (not open onto the outside) like muscles and organs. A possible trematode cyst (metacercaria stage), for example, has been identified inside a mid-Cretaceous lizard preserved in amber (Poinar et al. 2017). Located at the base of the squamate femora, the presence of this resistant structure on this animal implies that the metacercarian cyst was already well established in trematode life cycles at this period, and that its emergence may have occurred along with the colonization of intermediate hosts, which here are squamates. Nowadays, the definitive hosts of comparable trematode cysts are birds and mammals (Heidebegger and Mendheim 1938, see Poinar et al. 2017). Their presence in mid-Cretaceous squamates raises questions on (1) the role of these host squamates at that time, intermediate or definitive, and (2) the timing of co-evolution of trematode life stages within dinosaur and mammal lineages in the Mesozoic. This could be addressed through the fossil trematode stages preserved in those lineages. Infestations and Host-Symbiont Resilience When enough paleosymbiotic records are available, quantitative data can provide insights onto the evolution of symbiont-host infestations. It includes both the propensity of symbionts to colonize hosts and the associated response of hosts, which have the potential of being traced over time. This type of response might have been evidenced over deep time for isopods (Epicaridea) that inhabit the branchial chamber of decapod crustaceans by Klompmaker et  al. (2014). From previously published data and a set of hundreds of newly studied Late Cretaceous brachyurans and anomurans, the authors revealed a significant peak in the prevalence of isopods on decapods in the Late Jurassic. This peak was observed both for the global number of swellings and the percentage of infested species per epochs (with a standardization allowing the comparison of epochs of different durations). After this apogee, there seems to have developed a constancy of the infestation prevalence with much less infested species from the Early Cretaceous until today (only from 5 to 10 fossil species known to be infested). This decrease toward a stable lower rate of

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infestation may correspond to a resilience of the decapod fitness from the late Jurassic, with a selection of innovations allowing repelling isopod larvae or removing adults when installed (Klompmaker et al. 2014). It may also result from other factors on the parasite side (e.g., being less pathogenic), calling therefore for testing these hypotheses (compare Klompmaker et al. 2021). In this regard, large paleosymbiotic datasets can permit one to address the resilience of the host fitness to infestations over time (De Baets and Littlewood 2015). On the opposite, the case of platyceratid gastropod associations, which were never reported after the PermianTriassic crisis that caused the extinction of their crinoid hosts, reveals the non-resilience of some ancient symbionts to the disappearance of their usual type of host (Baumiller and Gahn 2002).

2.4  Conclusions Defined as any “ancient biological association (brief and long) between organisms dissimilarly named”, paleosymbioses are among the most direct evidence of paleoecological interactions and key elements to understand the evolution of lineages over time. Indeed, they are screenshots of the reality of unsuspected ancient ecological interactions involving extinct taxa, or simply modern taxa that are not involved in the same interactions today. In addition, they are elements to date the ancestry of large lineage pairings over time and often a favourable material to discover ancient minute-sized phyla. Finally, when sufficiently expressed in terms of individuals, ages and lineages, paleosymbioses can directly inform on broad biological questions (increasing number of life stages over life cycles), but also directly about ecological processes (existence of general trends ruling for organisms encountering and symbiont internalization, selection pressures on “arms” acquisition in host-symbiont couples). Consequently, even if fossil associations are today still sensibly explored, they are highly worthwhile components of the paleontological record in general, as well as key to the understanding of parasite-host evolution.

References Ahmadjian V, Surindar P (1986) Symbiosis: an introduction to biological associations. University Press of New England, Hanover Audo D, Robin N, Luque J, Krobicki M, Haug JT, Haug C, Jauvion C, Charbonnier S (2019) Palaeoecology of Voulteryon parvulus (Eucrustacea, Polychelida) from the middle Jurassic of La Voulte-Sur-Rhône fossil-Lagerstätte (France). Sci Rep 9:5332 Baird GC, Brett CE, Frey RC (1989) Hitchhiking epizoans on orthoconic cephalopods: preliminary review of the evidence and its implications. Senckenb Lethaea 69(5–6):439–465 Baker JR (1994) The origins of parasitism in the protists. Int J Parasitol 24(8):1131–1137 Baumiller TK (1990) Non-predatory drilling of Mississippian crinoids by platyceratid gastropods. Palaeontology 33(3):743–748

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Chapter 3

Biodiversity and Host–Parasite (Co)Extinction Jeroen van Dijk and Kenneth De Baets

Abstract  Parasitism is one of the most common modes of life, and yet it is often disregarded or ignored in nature conservation. We are at the brink of the sixth mass extinction and in order to assess the extinction risk of both parasites and their hosts, we first need to fully understand the role and function of parasites in ecosystems. Parasites might play an active role in their host’s extinction, and coextinction has been postulated to be the most common mode of extinction. However, parasites may be able to survive their host’s extinction through host switching, perhaps to a more abundant host, for example. The dilution effect has been described as an important natural defense mechanism for the host: higher biodiversity is associated with lower infection risk. Discussed here is the importance of biodiversity and host–parasite associations and (co)extinction, and the role the fossil record has in filling the knowledge gap regarding deep-time host–parasite interactions. Keywords  Biodiversity · Co-extinction · Dilution effect · Host–parasite associations · Fossil record · Host switching

3.1  Introduction We are currently witnessing the sixth mass extinction or at least its beginning, as became clear in the last decades (Wake and Vredenburg 2008; Barnosky et al. 2011; Payne et al. 2016). The Earth’s biodiversity is decreasing, with more and more species disappearing. Even more worrying though is that a large portion of the estimated number of existing species today are still awaiting description (Mora et al. 2011). There is some bias in human pity: it seems dramatic when wild cats and rhinoceroses disappear, but who will cry for mites, fleas, and lice? Costello et al.

J. van Dijk () · K. De Baets Friedrich–Alexander University Erlangen–Nürnberg, Faculty of Science, GeoZentrum Nordbayern, Erlangen, Germany e-mail: [email protected]; [email protected] © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 K. De Baets, J. W. Huntley (eds.), The Evolution and Fossil Record of Parasitism, Topics in Geobiology 50, https://doi.org/10.1007/978-3-030-52233-9_3

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(2013) famously asked whether we can name all species before they go extinct. The question raised is not trivial: Is naming every single species necessary, or is the cessation of some groups a loss that we can easily bear? Parasites, for example, are more or less considered species non gratae in nature conservation (Strona 2015; Dougherty et al. 2016; Carlson et al. 2020). The macroevolutionary point of view defends parasites, arguing that they might fulfill an important stabilizing function for maintaining the balance of ecosystems (Seilacher et al. 2007; Lafferty 2012), a balance that might shift during mass extinctions (Seilacher et al. 2007). Dougherty et al. (2016) and Carlson et al. (2020) suggested to include parasites into nature conservation, but this requires a framework that tests for the viability of host–parasite assemblages within a population in order to assess extinction risk. And here is where we come to some quite important and interesting questions: How important are parasites to an ecosystem (beyond being a nuisance to their hosts)? And, if they are important, what is their role? More importantly, how does parasite diversity and extinction relate to host diversity and what happens to parasite diversity during mass extinctions?

3.2  Host–Parasite Biodiversity Parasitism is one of the most common modes of life on Earth (Poulin and Morand 2000), which has independently evolved at least 223 times within metazoa (Weinstein and Kuris 2016), but also throughout the entire tree of life (Bass et al. 2015). Parasites can be highly abundant in ecosystems, and not only reach high diversity levels, but also take up a substantial part of an ecosystem’s biomass (Kuris et al. 2008). Indeed, ecosystem functioning seems to improve with increased diversity of parasite species (Hudson et al. 2006). Nonetheless, parasites are often seen as disgusting, associated with diseases and low hygienic conditions, and are therefore probably the most ignored group of organisms in nature conservation (see Dougherty et  al. 2016). When it comes to protecting the natural world, parasites are often overlooked (e.g., biodiversity counts), because they do not come to mind (e.g., too small), or because they simply lack charisma (Dunn et al. 2009). Instead, they are often seen as part of the problem: a threat to wildlife, and should therefore be eradicated. Medical and veterinary sciences attempt to remove parasites from both human and animals by all means necessary, as evidenced by the tragic fate of the condor louse (Colpocephalum californici) that went extinct during the captive breeding program of its host, the highly endangered California condor, Gymnogyps californianus (Pizzi 2009). This example demonstrates that we care more for the hosts than for their parasites, and that hosts may survive with the help of our conservation programs, while their parasites go extinct. Emiliani (1993) and also Vredenburg et al. (2010) have postulated that, potentially, parasites and viruses could even drive their host to extinction during particular conditions. A strong decline has been observed in the total number of adult and subadult frogs in three metapopulations after the detection of amphibian chytrid fungus, Batrachochytrium dendrobatidis (Fig.  3.1; Vredenburg et  al. 2010).

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Fig. 3.1  The number of adult and subadult frogs in the different metapopulations before and after detection of Bd. Studied sites: Milestone Basin (a), Lake Basin (b), and Barrett Lake Basin (c). Image from Vredenburg et al. (2010)

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However, the evidence for this dynamic is lacking from deep time, and the total exclusion of a species by another species is considered rare in nature (Vermeij 2004). Traditionally, disease models suggest that parasites driving their host to extinction are highly unlikely to nearly impossible, and often the parasites go extinct before the hosts (De Castro and Bolker 2005). Some conditions, however, may allow for parasite-driven extinctions of a host, for example, a parasite which significantly reduces the reproductive capacity of infected hosts (Boots and Sasaki 2002), or the evolution of costly host defense that is limited by resource availability (Boots 2011). However, resource availability and cost of resistance may actually play a more important role in the so-called killing the winner motifs (Våge et  al. 2013; Våge et al. 2018). In this particular motif, the parasite (or virus) selectively attacks the “winner” (i.e., superior competitor or abundant) populations, preventing any single host from dominating a community and thereby promoting diversity (Thingstad and Lignell 1997). Empirical examples are few and far between, but they have been observed in land snails (Cunningham and Daszak 1998), and the red flour beetle, Tribolium castaneum (Rafaluk et al. 2015). It is safe to assume that parasites and pathogens must have played an important and active role in past extinctions as evidenced by the global decline of amphibians caused by virulence, which is here defined as the parasite-induced reduction in host lifetime reproductive success (Herre 1993), and the emerging infectious disease chytridiomycosis, which was likely spread through the introduction of exotic species, and was enhanced by climate change and habitat destruction (Wake and Vredenburg 2008). While plausible in theory, it is challenging to track host–parasite relationships empirically in the fossil record. It is reasonable to assume that parasitism has existed in one form or another since the beginning of early life. However, most parasites are small, and their soft bodies hardly fossilize (Leung 2017). However, some types of host–parasite collections allow us to track parasitic infestation in deep time (De Baets and Littlewood 2015; De Baets et al. 2021a, b; Wood et al. 2017). Parasites can leave traces in their host’s remains, which can be studied, as well as traces and (resistant) propagules in coprolites, the host’s fecal remains. Yet it is difficult to gather enough evidence to precisely identify host and parasite. In some cases, it is possible to track hosts and their associated parasites and/or characteristic pathologies, as with platyceratid gastropods in the fossil record (Baumiller and Gahn 2002).

3.3  Co-extinction Global change is expected to typically lead to co-extinction of hosts and their specific parasites (Dunn et al. 2009; Carlson et al. 2017; but see Strona 2015). Some models that account for host-driven co-extinctions predict that up to 30% of the parasites go extinct in the form of such secondary extinctions (Fig.  3.2; Carlson et al. 2017). However, such a perspective would strongly depend on to what degree

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Fig. 3.2  Dispersal (a) and no dispersal (b) scenarios and the effects on the primary (due to climate change), secondary (co-extinction with hosts), and combined (total) extinction rates for major helminth clades. Figure from Carlson et al. (2017)

parasites specialize on niche specialists or top predators (Lafferty 2012). Models of parasite co-extinction with host decline differ from models that are based on host extinction alone. Such models of co-extinction only focus on the outcome after complete host extinction, but a species will generally show a significant decline in abundance and range size well before it finally goes extinct (Farrell et al. 2015). Parasite survival has often been closely linked to the survival of its host; it can therefore be expected that when the host goes extinct, so will the parasite (Koh et al. 2004). Many tick species, for example, are endangered (Mihalca et al. 2011). Dunn et  al. (2009) rightly posit that with current species’ declines and extinctions, the most endangered species will actually be parasites and mutualists. This is because all species with a symbiotic lifestyle naturally depend on the availability of a host. Additionally, each host species likely harbors just as many, if not more, in symbiosis living species: from the mutualistic bacteria in our intestinal tract, the ones on our skin (e.g., lice and ticks), to parasitic flatworms and viruses. Endoparasites are especially vulnerable to host-driven co-extinction (Carlson et al. 2017). Some are specialists, being highly host species specific, and thus potentially more prone to co-extinction, while others are generalists that may be able to adapt to the change in host availability. Co-extinction has a high chance to occur when the parasites are specialized on niche specialists or hosts higher on food chains (Lafferty 2012). However, this does not need to be the case when the host has a wide distribution and high abundance (Strona et al. 2013; Strona 2015). Highly specific parasites predominantly use low-vulnerability hosts (Fig. 3.3), and thereby reduce the risk of a co-extinction (Strona et al. 2013). Parasite and host co-­extinction are often overlooked, but may have occurred throughout Earth’s history, especially during mass extinction events (e.g., Seilacher 2007).

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Fig. 3.3  3D representation of the relation between host vulnerability and host specificity. Image reproduced from Strona (2015)

Co-extinctions can be expected at a much broader scale and are not only restricted to host–parasite relationships, but concern all types of species that depend on one or more species in general: from the many forms of symbiosis to predators and their prey, to key species in an ecosystem. In a predator-prey relationship, for example, where the predator is highly specialized on just one type of prey, the predator has a high risk of co-extinction if it does not change its diet, but also herbivores with a very specific diet can fall victim to co-extinction (Labandeira et al. 2002). Another, highly relevant, coevolutionary relationship is that between plants and pollinators. One-third of Europe’s crop plants depend on pollinators (Kearns and Inouye 1997). Local extinctions of bee populations and the parallel decline of insect-pollinated plants due to anthropogenically modified landscapes have been observed in several parts of Europe and are of much concern (Biesmeijer et  al. 2006). Co-extinctions of plants and their pollinators is nothing new and has happened in the deep past as well (Bascompte and Jordano 2007). Thus, co-extinction may be the most common form of species loss (Koh et al. 2004; Dunn et al. 2009). The disappearance of key species should thus be our main concern as that could result in a cascade of secondary extinctions and co-extinctions of the parasites and others that depend on them (Stork and Lyal 1993). The assumption has been that threatened hosts have relative fewer single-host parasites (Dunn et al. 2009; Lafferty 2012), but host extinction may vary across groups of hosts. Threatened ungulates were found to have a higher proportion of single-host parasites compared to non-­ threatened ungulates, a result related to a disproportionate decrease in richness of multi-host parasites, but among carnivores this relation does not exist (Farrell et al. 2015).

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3.4  Dilution Effect The current biodiversity loss and disease emergence have become two of the most challenging issues confronting science and society (Johnson et al. 2008). Different authors have found a strong correlation between parasite success in ecosystems and biodiversity of their ecological communities (Johnson et  al. 2013; Lagrue and Poulin 2015), and many of them underline that the rapid loss of populations and biodiversity significantly increases overall disease risk. Studies concerning the causal relationship between biodiversity and disease emergence in a particular environment are focused on testing the “dilution effect” model (Ostfeld and Keesing 2000), which parasitologists refer to as the “decoy-effect” hypothesis (Combes and Moné 1987; Johnson and Thieltges 2010). According to these researchers, the mechanisms of the decoy effect, as observed in the case of high biodiversity in ecological communities, concern (1) the physical degeneration of parasite life history stages infecting a nontarget host, (2) the encounter reduction caused by infecting a nontarget host, and (3) the stimulation of defense mechanisms in nontarget hosts against the infectious stages of the parasite. Regardless of the mechanism, the nontarget host becomes a dead-end host, which is the real factor reducing the emergence of parasitic disease (Mehlhorn 2008). Essentially, this is in the same line of thought as Keesing et al. (2006), who propose that the term “dilution effect” should be interpreted as “the net effect of increased species diversity reducing disease risk.” The dilution hypothesis has been in particular investigated for zoonotic diseases, like Lyme disease, but has also been reported to be more widespread (Civitello et al. 2015), and has even been reported for zooplankton (Hall et al. 2009). However, a meta-analysis of classical studies with new approaches has demonstrated that research is heavily biased towards studies presenting the dilution hypothesis, which yield biased results (Young et al. 2013). When correcting for this, a meta-analysis could not find strong evidence for the dilution hypothesis (Salkeld et  al. 2013). Further analyses suggest that there is a slight publication bias towards negative relationships between biodiversity and disease risk (Fig. 3.4; Salkeld et al. 2013). The generality of the dilution hypothesis is still debated and might be context dependent. It might particularly work on local scales, while large-scale analyses usually find a positive correlation between host and parasite diversity (Wood and Lafferty 2013). In that sense, it is mostly a matter of scale whether one observes a dilution effect or not (Fig. 3.5; Hopkins 2013), and may further depend on the characteristics of host communities (Halliday et al. 2020) and species interactions, such as predation (Su et al. 2020). Large-scale studies show mostly the traditional patterns, and this is potentially also the dominant relationship we might find on longer evolutionary patterns observed in the fossil record. Preliminary data compiled by Baumiller and Gahn (2002) on the prevalence of parasitic pathologies in  marine invertebrates are very reminiscent of the traditional perception of metazoan diversity (the so-called Sepkoski (1981) curve). A similar positive relationship also exists between infested species of crinoids and crinoid diversity  (Fig.  3.6; compare Baumiller and Gahn 2002; Baumiller et al. 2004). Irrespective of the presence of the

Fig. 3.4  Funnel plot of the relation between the Fisher’s Z effect size and the standard error for studies on biodiversity and disease risk. Adapted from Salkeld et al. (2013)

Fig. 3.5  As forest area increases, tick density will increase, but less fragmentation will lead to a decrease of infection prevalence. Lime green is used to indicate Lyme infection. Figure by Hopkins (2013)

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Fig. 3.6  Crinoid genera parasitized by platyceratids during the Paleozoic. Entire bars show the crinoid generic diversity based on sampled-in-bin diversity downloaded from the Paleobiology Database (PBDB, accessed in 14/11/2019). Co-occurrences of crinoids and platyceratids are shown in the solid blue part with error bars for 95% confidence levels. Based on data from Baumiller and Gahn (2002)

dilution effect or opposite patterns—this context dependency is still of great interest on larger timescales. How can we extrapolate anything like the dilution effect to deep time, especially when there is no general consensus on the dilution effect occurring in the modern world? In fact, some workers even question how effective a dilution effect actually is in reducing disease risk. Critique on the dilution effect model concerns the issue that it may only work if the parasite is (more or less) a host specialist, and increasing host diversity will also increase infection prevalence; thus the addition of host species may actually increase parasite abundance (Randolph and Dobson 2012; Wood and Lafferty 2013). The mechanisms behind the dilution effect are complicated, even if some aspects of it might be applicable to the fossil record, e.g., trace fossils

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that indicate a parasite with host preference, and high vs. low variation in potential hosts; but these findings will first and foremost indicate density dependence. Let us not forget that the dilution effect itself refers to the reduced disease risk for a vulnerable focal host at higher biodiversity due to the presence of more diluter species (Keesing et al. 2006). These diluter species can in several ways decrease transmission: they can affect focal host behavior, reduce focal host population density so it may become fragmented, or may feed on the disease vectors, e.g., the parasites (Keesing et al. 2006; Keesing et al. 2010). Thus, parasites do play a role here as a vector transmitting the disease (e.g., ticks spreading Lyme disease), but the transmitting-­part is hardly observed in the fossil record, if at all. To actually observe this in the fossil record we would need to investigate three things: (1) an indication that the mortality of selected fossils was caused by disease, (2) the prevalence of parasite traces, and (3) whether 1 and 2 are related, or not. Morphological studies of fossil remains could be one approach, as disease may affect morphology as well as size. Infected organisms may compromise with reduced growth (Ruiz 1991), a phenomenon reminiscent of the “Lilliput effect,” which was observed in the context of mass extinctions (Urbanek 1993). However the opposite may also have happened in some cases, in the form of pathological gigantism, possibly caused by parasitic castration (Manger et al. 1999; but see De Baets et al. 2015). Modern studies show that skeletal pathologies observed in helminth-infested frogs are inversely correlated with survival (Johnson et al. 2011). The number of malformed amphibians has markedly risen (Fig. 3.7, Johnson and Chase 2004)—making it tempting to attribute this to anthropogenically induced factors (Johnson and Chase 2004).

Fig. 3.7  The number of articles published on, and the number observed in (line), malformed amphibians in wild populations in North America (USA and Canada). Figure from Johnson and Chase (2004)

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An observed dilution effect may well be a “chicken or the egg” causality dilemma, and in fact, there may be more a “killing the winner” dynamic going on, than an actual dilution effect. Indeed, it may be a matter of scale as some workers have pointed out, but it may also depend on the moment in (long-term) time. Much like the “Red Queen” dynamics in predator-prey interactions, populations of hosts will likely follow a sinusoidal pattern through time. In turn, Red Queen dynamics might be one mechanism that promotes host switching (Rabajante et al. 2016). A highly successful and abundant species may attract more parasites, and then decline because of parasite load, which then allows the host’s competitors to rise. As a result, parasite density may fall and/or the parasites may switch to a new host, which, in turn, would allow the original host population to strengthen and increase again. The presence of competition may in fact be beneficial to the host, driving rapid evolution of hosts with high phenotypic variation and may thereby “rescue” the host’s population densities despite larger epidemics (Strauss et al. 2017). The notion that diverse communities inhibit the proliferation of parasites (Civitello et al. 2015) is in that sense incorrect, because in reality it is more likely that parasites inhibit the proliferation of any single (or multiple) host species. Much like the “paradox of the plankton,” which addresses the situation where a number of phytoplankton species are able to coexist in the same environment while competing for the same resources (Hutchinson 1961). Here, the parasites play an important role in facilitating diversity by allowing multiple species to exploit a certain niche (Våge et al. 2018). The deep-time fossil record could well play an important part here if only we could find an effective way to reconstruct these dynamics. A complicating factor here might be that an increase of host pathologies in the fossil record could relate to an increase in parasitized specimens, but could also reflect an increase in abundance of hosts that can better cope with being parasitized, or at least with the developing pathologies. A positive relationship between sampling opportunity and finding pathologies might also affect such a relationship (cf.) as it has been suggested for predation prevalence (Huntley and Kowalewski 2007). However, by looking at larger samples of hosts from various localities and time intervals one could get an idea about the relationship between host population structure and prevalence of pathology changes through time. Such a larger sampling would also avoid the pitfalls of small sample size.

3.5  Host Switching Host switching, e.g., parasites “jumping” from one species to the other, broadly speaking, occurs naturally as part of the life cycle of many species of parasites. On evolutionary timescales this usually refers to events where parasites switched host, which is usually inferred from coevolution patterns in phylogenies (Page 2003; Martínez-Aquino 2016). However, these phylogenies might be hard to resolve and not entirely equivalent (e.g., De Vienne et al. 2013; Poisot 2015). The biology of host switching revolves around three factors: (1) the rate of exposure of the new host

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to the parasite, (2) the compatibility of the pathogen towards the new host, and (3) whether the pathogen is sufficiently transmissible between individuals within the new host population (Woolhouse et al. 2005). Host switching has played an important role in the evolution of many parasite groups, but most of these host-switch events have been inferred solely from molecular phylogenies of extant taxa (e.g., Badets et al. 2011). Fossil parasites may help us to calibrate molecular clocks in such trees, as well as confirm past host-switching events (De Baets and Littlewood 2015; Leung 2017; Warnock and Engelstädter 2021). The fossil record has also revealed various combinations of parasite and host (e.g., arthropod and their pathogens) that have no extant equivalents (see De Baets and Littlewood 2015; Leung 2017, 2021 for reviews). Ticks (order Ixodida) are known to have switched hosts many times during their evolution. It is therefore likely that host specificity is merely temporal and determined by biogeography and ecology (Klompen et  al. 1996). One example is Nuttalliella namaqua, a monotypic tick species (the only representative of its genus). Phylogenetic analysis placed N. namaqua basal to the Ixodida, and can therefore be considered a “living fossil,” with its ancestors originating in the Late Carboniferous to Early Permian (Mans et al. 2011; Mans et al. 2012). These ancestors must have parasitized early reptiles and evidently changed host preference to mammals and lizards (Mans et al. 2014; but see Dunlop 2021). Traces of host switches can also be identified via horizontal gene transfers (HGT) or horizontal transfers of retrotransposons (HTT) in the genomes of hosts and parasite species. For example, lymphatic filariasis and loiasis are two widespread human diseases caused by insect-borne filarial nematodes Brugia spp., Wuchereria bancrofti, and Loa loa. These nematodes were likely endoparasites of tropical birds during the Oligocene/Miocene epochs (Suh et al. 2016; Suh 2021)— both of these groups were at least present at the same time in the same regions, as evidenced by amber records (Poinar et al. 2007; Poinar 2010, 2011a, b). Evidence was found that the genomes of these nematode species share the retrotransposon AviRTE with seven lineages of tropic birds, which must have come from two waves of horizontal gene transfer (Suh et al. 2016).

3.6  Parasites as Drivers and Regulators Parasites have various ways to affect the lives of their host. They can, for example, deteriorate the host’s health, or influence the host’s reproductivity or even host behavior, as seen in rats and mice. The common brain parasite, Toxoplasma gondii, influences the behavior of rats and mice (the intermediate hosts) to become easier prey for cats (the target host). Infected intermediate hosts show more exploratory behavior and are less fearful of cats. Humans can also be infected, but normally serve as a dead end, although it is interesting to hypothesize how T. gondii may have influenced our behavior and culture in the long term, after centuries of exposure. Climate change and biotic invasions of disease vectors promote the transfer of novel diseases and parasites to native species (Tylianakis et  al. 2008). Higher

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temperatures can both enhance host susceptibility to parasites and reduce host survival and fertility (Traill et al. 2010). The most optimal parasite and host phenotype, in terms of infectivity and resistance, respectively, vary from one time point to the next leading to fluctuating selection dynamics (Hall et al. 2011). In turn, this may result in fluctuating “Red Queen” coevolutionary interactions, where the parasite is locally adapted to infect sympatric host species, but has trouble infecting allopatric hosts (Brockhurst et al. 2014). In natural systems this leads to negative frequency-­ dependent selection, where the parasite follows the most common host over time (Decaestecker et al. 2007; Wolinska and Spaak 2009). Parasite diversity can then be maintained through negative frequency-dependent selection and multiple-niche polymorphism (Radolf and Samuels 2010; Strona et al. 2013; Strona 2015). The occurrence of diverse natural populations of asexual organisms can be explained by the presence of parasites, which seem to play an important role in maintaining host genetic diversity (Turko et  al. 2018). Sexual reproduction may exist for the same reason: instead of clonal reproduction where each generation is basically a copy of the previous, sexual reproduction creates diversity, which enables populations to cope with parasite infection (Jokela et al. 2009). Competition and defense could be central structuring factors in some microbial communities (Våge et al. 2018). This may also lead to diversification of both host and parasite, even in a homogenous environment, such as with the prey and predator leading to the paradox of the plankton (Hutchinson 1961). This process has also been termed “killing the winner,” where a parasite or virus prevents a susceptible competitive host (the winner) from monopolizing a limiting resource (Thingstad and Lignell 1997). This in turn allows the coexistence of resistant hosts, even when their defense is associated with a cost in the form of reduced competitiveness. While competitive hosts tend to be infected by virulent specialists, less virulent generalists infect more hosts with higher resistance. Species that have found a way to reduce the costs of defense against parasitism without losing too much in competitive ability may reach the highest abundances (Våge et al. 2018), although other factors such as predation may still prevent this. The resistant hosts may be resource controlled, disappearing at low resource levels and dominating at high resource levels (Våge et al. 2018). Highest diversity would then be found around intermediate resource levels, which seems to be a general pattern found in both microbial and macroorganism ecosystems (Smith 2007). Lower amounts of remaining resources will likely slow down the Red Queen arms race based on the reduced probability that resistant hosts can successfully exploit them. Over geological time, these arms races may have played an important role in structuring the food webs with its major functional groups (Våge et al. 2018).

3.7  What Can the Fossil Record Tell Us? Host–parasite associations in the fossil record can be studied by comparing trait variation through time of the host, and whether or not they show signs of having been parasitized. The host may have reached adulthood, but compensated with

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decreased growth, abnormal growth response, or some visible pathology, for example (Hengsbach 1990; Rothschild and Martin 1993; Dittmar et al. 2012). Certain defensive traits may have come about as a response to parasitism as well, as is the case with the tubed crinoids that evolved in response to parasitization by platyceratids (Baumiller and Gahn 2002). In some cases, targetting of parasites by predators might also induce changes in the hosts such as spinosity in crinoids as a defense mechanisms against predation on platyceratid gastropods (Syverson et al. 2018). Traces of parasites have also been found in coprolites, in the form of tapeworm eggs in ancient shark coprolites, for example (Dentzien-Dias et  al. 2013). New methods such as using the synchrotron phase-contrast microtomography and high-­ quality virtual 3D reconstructions of coprolite inclusions may reveal ancient trophic relations (Qvarnstrom et al. 2017). An integrated approach of scanning combined with dissolving coprolites might be the most effective way forward (but see Wood and Wilmshurst 2016). Each of these systems has its own challenges. The direct fossil record of viruses and unicellular pathogens is very limited, making it hard-to-test hypotheses about their origins and coevolution directly (Hayward 2017; Leung 2017)—other than by attribution of changes in diversity and/or abundance without recorded environmental perturbations. Nonetheless, viruses, and in particular retroviruses, have been found to leave endogenous viral elements (EVEs) behind in the genomes of hosts and previous (ancestral) hosts (Katzourakis and Gifford 2010; Holmes 2011). These EVEs can be used to explore ancient viral evolution and trace their origins (Aiewsakun and Katzourakis 2015; Aiewsakun and Katzourakis 2017). Some of the more spectacular data involve ancient DNA, or aDNA (Lafferty and Hopkins 2018). Ancient DNA (aDNA) extracted from moa coprolites found in New Zealand revealed that some species of parasites survived the extinction of their hosts (Table 3.1), and still exist today (Wood et al. 2013; Boast et al. 2018). This dataset could indicate that since the extinction of moas, as much as 19 species of parasites

Taxon

L. Bush Moa

Giant Moa

Upland Moa

H.-footed Moa

Kakapo

Modern birds

Mammals

Appear

Persist

Disappear

Table 3.1  Chart showing the distribution of parasite taxa across extinct species of moa, modern birds, and mammals, and the total number that appears, persists, or disappears

Eimeriidae Emeria Sarcocystidae Ciliophora Balantiididae b Nematoda Ascaridida Heterakoidea Seuratidae Panagrolamoidea Strongylida Platyhelminthes Notocotylidae

1 0 1 0 0 6 1 0 0 0

3 0 0 0 1 6 1 0 0 1

9 0 1 0 0 7 1 0 1 1

3 0 1 0 0 0 0 0 0 1

0 0 1 0 0 0 0 0 0 0

3 0 0 4 0 0 0 0 0 0

0 1 0 0 0 0 0 2 11 0

0 1 0 4 0 0 0 2 10 0

3 0 0 0 0 0 0 0 1 0

6 0 1 0 1 9 1 0 0 1

Apicomplexa

a

Color fill illustrates presence (green) and absence (red) a Eimeriidae: excluding Eimeria b Ascaridida: unidentified species, excluding Heterakoidea and Seuratidae. Based on data from Boast et al. (2018), SI Appendix, Fig. S20

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went extinct, while as little as 3 species might have survived and up to 4 might have newly appeared in birds. For example, three upland moa’s eimeriid coccidia are still found parasitizing extant kiwis. On the other hand, up to 9 heterakoid nematode species that had coevolved to specialize on moas have disappeared since their host’s extinction. Moreover, the disappearance of moas led to the secondary extinction of their predator and a cascade of secondary extinctions of host-specific parasites of both predator and prey. The extinctions might however be overestimated as in modern birds only one (captive) kiwi and two (non-native) ostriches could be investigated, while the number of survivors and newly appeared species may have been underestimated for the same reasons. This is also supported by the fact that only 18 species of parasites went extinct when modern mammal samples are also included, while as few as 4 and as many as 17 species might have survived or appeared in the modern fauna investigated. Even though this approach might be suitable for investigating extinctions during relatively recent extinction events, it is limited when going further back in time. It does demonstrate that a significant proportion of parasite species can disappear when their hosts go extinct. In more ancient (lithified) coprolite samples, identifying the parasites using aDNA is limited (Chin 2021; De Baets et al. 2021a; Greenwalt et al. 2021). This means eggs themselves can rarely be assigned on the species or genus level, but are usually only attributable to higher taxonomic ranks. Also, precisely identifying the hosts is difficult—especially when found isolated from their producers. This is not an issue per se, as one can still study the diversity and relative abundance of propagules and their relationship/dominance in coprolites assignable to larger groups. However, further work (e.g., Camacho et al. 2018) is necessary to understand the abundance of propagules and their relationship with parasite abundance in hosts as well as loss through preparation. More important, although sampled, their record is still comparatively patchy. Coprolites need to be more systematically investigated for parasitic remains throughout the Phanerozoic (Chin 2021)—ideally covering major climatic and/or extinction events. As it is difficult to assign coprolites precisely to their hosts, their precise relationship with host species might be limited. Although the precise identification of the culprit of a particular pathology will be a challenge, the host can, in most cases, be identified up to genus or species level depending on the state of preservation. Moreover, the expression of the disease (paleopathology) can be precisely measured, and its prevalence in populations can be quantified. Through cost-benefit analysis and population studies it is even possible to establish their impact on growth and fitness of particular host samples (Baumiller 2003; Huntley and Scarponi 2012; Baumiller and Gahn 2018; Klompmaker et  al. 2021; Zhang et  al. 2020). Such an approach is necessary to understand the negative impact of parasites on their hosts. If we have densely spaced samples through time and/or space, we could even track how disease or infestation prevalence relates to characteristics of the hosts, such as abundance, evolutionary persistence, geographic range, mode of life, or degree of specialization. Particularly interesting systems are those that have modern analogues, like the isopod swellings in decapods (Klompmaker et al. 2014, 2021; Robins and Klompmaker 2019), and

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trematode-induced traces in bivalves (Ruiz and Lindberg 1989; Huntley and De Baets 2015; Rogers et al. 2018; Huntley et al. 2021), which can at least be traced back to the Mesozoic. However, such studies are even more important when parasites have a higher preservation potential—like platyceratid gastropods shown to be parasitic on crinoids (Gahn and Baumiller 2003). Considering that remains of shelled invertebrate hosts are more widespread— they do allow us to investigate the precise contribution of shifts in pathology prevalence, environmental perturbations, diversity fluctuations  and mass extinctions. More importantly, the relationship between specificity, or the prevalence of pathologies and host characteristics, can be investigated. This could be used to investigate whether the perception holds true that parasites tend to specialize on a specific host or rather on a number of resistant hosts. A better idea of this on longer timescales would also be crucial to understand the future of parasite diversity, as well as disease prevalence, in their hosts. Climate change for example, and in particular sea-­ level rise, has been linked to an increased prevalence of trematode infestations in bivalves (Huntley et al. 2014; Scarponi et al. 2017). Cost-benefit analysis and modelling can help to establish the nature of this association (Baumiller 2003; Baumiller and Gahn 2018). Furthermore, the relationship between diseased species (specificity) and infested individuals within samples (prevalence) could be investigated. This, in principle, allows us to investigate how these properties relate to host persistence, abundance, and/or geographic range. In the case of amber inclusions, novel techniques, such as phase-contrast synchrotron X-ray tomography (Dunlop et al. 2011; Dunlop et al. 2016), may allow the precise identification of the host, and the identification of the parasite to genus, or (at least) family level, might well be within grasp. However, more quantitative studies of amber inclusions are necessary to establish the prevalence of such associations. Due to a limited number of characters, it is still not that straightforward without knowledge about the life cycle of modern relatives and their host associations, to precisely identify particular parasites with limited external characters such as nematodes (Poinar 2011a, 2011b). Research has, at least, revealed potential new extinct, or rare, host associations (Peñalver et al. 2017), as well as tracked ancient host associations back in time (Haug et al. 2021; Labandeira and Li 2021). Another factor which needs to be considered when using amber deposits remains the debate concerning the age of many deposits, their patchiness in time, and the selectivity of trapping and preserving hosts (McCoy et al. 2018; Solórzano-Kraemer et al. 2018; De Baets et al. 2021a). Despite these limitations, we are convinced that studying these model systems would advance our understanding of host–parasite evolution in deep time, as well as further constrain the modern baseline. Amber inclusions would be particularly good to understand the evolution and extinction of arthropod parasites and vectors, while invertebrate pathologies and propagules in vertebrate coprolites might be the only way to cover the impact of mass extinctions on parasitic disease and their link with host diversity. Before we can fully exploit the fossil record for this purpose, more data needs to be collected still, before such studies become feasible. Currently, most of these systems are incompletely studied—larger samples in particular are rare, and reports of prevalence of certain pathogens or impact on host population are still

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limited or restricted to particular time intervals (e.g., De Baets et  al. 2021b). Systematic screening of museum collections yielding large samples of well-determined hosts from particular localities might help considerably in such an endeavor (Harmon et al. 2019), as well as considering these constraints when sampling and describing new host remains. Acknowledgements  The authors would like to thank Carl J. Reddin and Tatjana E. Döbeling for comments on earlier versions of this chapter. The authors would also like to thank John W. Huntley for reviewing this chapter.

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Chapter 4

Evolutionary History of Colonial Organisms as Hosts and Parasites Olev Vinn and Mark A. Wilson

Abstract  Parasitic associations involving colonial animals are farily evenly distributed through the post-Cambrian Phanerozoic and have a long evolutionary history. Parasitism may have played an important role in the evolution of colonial animals. In the Paleozoic, the majority of marine symbioses involved colonial animals, and it is likely that colonial animals were also important hosts of parasites in the Mesozoic and Cenozoic, but further studies are needed. In the Paleozoic, stromatoporoids and corals were the most common hosts to various invertebrate parasites. Corals continued to be important hosts to parasites in the Mesozoic and Cenozoic. In addition, colonial animals themselves often infest or otherwise live in association with other organisms and can be parasites; however, colonial animals are more often hosts than parasites, and this has been so throughout the Phanerozoic. The stratigraphic distribution of parasitic associations in colonial animals is divided into two separate blocks: Paleozoic (Ordovician to Permian) parasitic associations of colonial animals form the first block and Mesozoic to Recent parasitic associations of colonial animals form the second block. This division of parasitic associations corresponds well to the Sepkoski Paleozoic and Modern faunas and therefore these subdivisions are termed as the Paleozoic and the Modern parasitic associations of colonial animals. Keywords  Parasites · Coloniality · Bioclaustrations · Intergrowth · Phanerozoic

O. Vinn () Department of Geology, University of Tartu, Tartu, Estonia e-mail: [email protected] M. A. Wilson Department of Earth Sciences, The College of Wooster, Wooster, OH, USA e-mail: [email protected]

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 K. De Baets, J. W. Huntley (eds.), The Evolution and Fossil Record of Parasitism, Topics in Geobiology 50, https://doi.org/10.1007/978-3-030-52233-9_4

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4.1  Introduction Parasitic associations involving colonial animals have a long evolutionary history as well as a long history of discovery (Duncan 1876). Reports of parasites are fairly evenly distributed through the post-Cambrian Phanerozoic (Baumiller and Gahn 2002; De Baets et al. 2021). Bioclaustrations and intergrowths of different skeletons are the best ways that parasitic associations are preserved in colonial animals (Zapalski 2007, 2011; Zapalski and Hubert 2010; Taylor 2015). A bioclaustration is created when a skeletonized host organism embeds a symbiont within its skeletal tissues (Palmer and Wilson 1988). Skeletonized invertebrates that live in close proximity can intergrow with each other to form a fused pair of skeletons, which differs from encrustation in that one skeleton overlaps another (Tapanila 2008). The complete intergrowth of two skeletons provides the most definitive evidence of symbiosis of involved animals (Tapanila 2008). All colonial animals are aquatic invertebrates, and coloniality has evolved on multiple occasions in marine animals (Blackstone and Jasker 2003). Several colonial taxa are mainly marine, such as bryozoans and corals (Hughes 1989). Colonial animals have a modular construction comprising zooids (i.e., repetitive clonal units) (Taylor 2015). There can be one or more types of zooids in colonial animals depending on the group. During astogeny, different colonies belonging to the same species may achieve different forms depending on the environmental conditions (Taylor 2015). Modern colonial animals including sponges (here; see Sect. 4.2) are often inhabited by various parasites (Hooper 2005; Boero and Bouillon 2005; Hill and Okamura 2007). Parasites of colonial animals can be unicellular endosymbionts (Okamoto and McFadden 2008) or multicellular macroscopic parasites such as mollusks (Lorenz 2005), arthropods (Lützen 2005), and helminths (Aeby 2003). Colonial animals, such as sponges and cnidarians, can also be parasites of other colonial animals (Hooper 2005; Boero and Bouillon 2005). Parasitism may have played an important role in the evolution of colonial animals. Parasitism in colonial animals has recently been reviewed by Taylor (2015). In the Paleozoic, the majority of marine symbioses involved colonial animals according to Tapanila (2008). It is likely that colonial animals were also important hosts of parasites in the Mesozoic and Cenozoic, but further studies are needed. It has always been difficult to distinguish between different types of symbiosis in the fossil record (Tapanila 2008; Zapalski 2011) and therefore all cases of symbiosis which can be interpreted as parasitism are discussed below. Boucot and Poinar Jr (2010) established reliability classes to rate the evidence of fossil behavior ranging from very certain (category 1) to highly speculative (category 7). Category 1 was used when a small number of examples exist for which there is no question about the reliability of the interpretation, as in the case of insects in copula preserved in amber. All examples studied here correspond to the Boucot and Poinar Jr (2010) category 1 in the sense of symbiosis. However, for rating the likelihood of a parasitic relationship, we introduce here four categories starting with

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very certain parasitism (category 1) and ending with highly speculative parasitism (category 4). Category 1: Infected specimens show poor condition (reduced size) as compared to uninfected specimens; category 2: modern representatives of the symbiont are definite parasites; category 3: symbiont caused definite harm to the host, but it may have also been in other ways beneficial to the host; category 4: unlikely parasitism, no definite harm caused to the host by its symbiont or lack of evidence thereof.

4.2  Sponges as Hosts of Parasites Sponges can be interpreted as colonial animals because many aspects of their growth and life history are closer to colonial than to unitary organisms (Simpson 1973; Taylor 2015). Thus, we have included sponges here as colonial animals. Modern sponges are often inhabited by various invertebrates, such as Hydroides spongicola (Polychaeta), for example (Bastida-Zavala and ten Hove 2002), and so were the sponges in the geological past. Representatives of the neolepadine barnacle Litholepas klausreschi lived partially buried within the Late Jurassic sponge Codites serpentinus. They had either a parasitic or a commensal relationship with their host sponge (Nagler et  al. 2017; Haug et  al. 2021). They are assigned to category 4.

4.2.1  Stromatoporoids Stromatoporoidea is a class of sponges, usually interpreted as sclerosponges, common in the fossil record from the Ordovician through the Devonian but extending into the Cretaceous and there are even somewhat similar sclerosponge taxa in modern seas (Stock 2001). Stromatoporoids are among the most common hosts of other Paleozoic invertebrates. The earliest stromatoporoid symbionts appeared in the Late Ordovician of China (Lee et al. 2016) and some of them may have been parasites (Zapalski 2007, 2011). Stromatoporoids housed various invertebrates such as bioclaustrations of various worms (e.g., Chaetosalpinx and Helicosalpinx), tentaculitoid tubeworms (Cornulites, Trypanopora, and Streptindytes), rugose corals, syringoporids, and lingulate brachiopods (Tapanila 2005; Vinn and Wilson 2010; Vinn et al. 2014). In the Late Ordovician of China, stromatoporoids were inhabited by the tabulate coral Bajgolia and rugosans (Lee et al. 2016). Growth of Bajgolia usually kept pace with its host; in some cases, the growth form of the stromatoporoid changed in response to the coral (Lee et al. 2016). The relationship between Bajgolia and stromatoporoids is unknown, but there is some evidence for parasitism (Lee et al. 2016). We assign category 4. Bajgolia–stromatoporoid associations represent an important stage in the development of complex ecological relationships prior to the common

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and widespread syringoporid-stromatoporoid associations in the Silurian to Devonian (Lee et al. 2016). In the Silurian, stromatoporoids were inhabited by a large number of different invertebrates, including worm bioclaustrations (Chaetosalpinx and Helicosalpinx), tentaculitoid tubeworms (Cornulites stromatoporoides), rugose corals, and syringoporids (Tapanila 2005; Vinn and Wilson 2010; Vinn et al. 2014; Vinn and Mõtus 2014a, b). The worm bioclaustrations were most likely made by some parasitic polychaetes (Zapalski 2007, 2011). Worm bioclaustrations appear in the earliest Silurian of Baltica (Vinn et  al. 2013) and they remain common throughout the Silurian (Tapanila 2005; Vinn and Mõtus 2014b). These stromatoporoid symbionts were possibly suspension feeders analogous to modern polychaete endobionts in corals, and the interaction with stromatoporoids could be interpreted as a feeding competition (Vinn et al. 2013). We assign category 3. About 78% of Katri biostrome stromatoporoids from the late Silurian of Estonia contained worm endobionts (Vinn and Mõtus 2014b). Thus, infestation rate of stromatoporoids with worm endobionts could be locally very high in the late Silurian. Similarly to worm endobionts, rugose corals were common stromatoporoid symbionts throughout the Silurian. They were especially abundant in Silurian biostrome stromatoporoids (Kershaw 1987). The rugosans were usually vertically oriented inside the stromatoporoid skeletons (Vinn and Mõtus 2014a). Often numerous rugosans had their corallites open at the upper, external surface of stromatoporoids, but many could be completely embedded within the stromatoporoids (Vinn and Mõtus 2014a). Stromatoporoid hosts were presumably beneficial for rugosans as elevated stable substrates on a sea floor that offered a higher tier for feeding (Vinn and Mõtus 2014a). It is possible that numerous rugosans in a single stromatoporoid may have decreased the feeding efficiency of the host by occupying part of its feeding surface. Thus, a parasitic relationship is possible in case of rugosan-stromatoporoid associations in the Silurian. On the other hand, assuming that the embedded rugosans had nematocysts, they could have protected against certain predators of the host sponge. We therefore assign category 4. Syringoporids were another common group of stromatoporoid symbionts in the Silurian, especially in the late Silurian (Kershaw 1987). Syringoporids often formed dense colonies within stromatoporoids (Kershaw 1987) and definitely had influence on their hosts. However, it is not certain whether this relationship was parasitic or mutualistic. In contrast to the above-described symbionts, Cornulites was a less common inhabitant of Silurian stromatoporoids (Vinn and Wilson 2010) (Fig. 4.1). In lower Sheinwoodian open shelf marls of Saaremaa Island (Estonia), 30% of stromatoporoids are infested by C. stromatoporoides and 77% of stromatoporoids in upper Sheinwoodian shoal limestones also show this endosymbiotic relationship (Vinn and Wilson 2010). The relatively small number (one to six) of living Cornulites per stromatoporoid (9–21 cm in diameter) presumably did not cause much feeding competition between the suspension-feeding host and the endosymbiont. Moreover, sponges today consume a lot of nanoplankton, whereas one would expect cornulitids, given their size, to have fed on larger plankton. Thus parasitism is not likely, but one cannot rule it out (Vinn and Wilson 2010). We assign category 4.

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Fig. 4.1  Cornulites stromatoporoides Vinn and Wilson in Sheinwoodian stromatoporoids from Saaremaa, Estonia (TUG-1328-1) (after Vinn and Wilson 2010)

In the Devonian, stromatoporoids hosted diverse invertebrates belonging to several phyla, including worm bioclaustrations (Chaetosalpinx and Helicosalpinx) (we assign category 2), tentaculitoid tubeworms (Streptindytes), rugose corals, and syringoporids (Tapanila 2005; May 1999, 2005; Da Silva et  al. 2011). The latter three are assigned to category 4.

4.2.2  Other Sponges Among sponges other than stromatoporoids, chaetetids are known to house symbiotic endobionts. The tentaculitoid tubeworm Streptindytes chaetetiae, Okulitch 1936, occurs in Chaetetes radians in the Carboniferous of Russia (Okulitch 1936). Streptindytes is always completely embedded in the host chaetetid, leaving only its apertures free on the growth surface of host colony. The relatively small numbers of living Streptindytes per chaetetid colony (Okulitch 1936) presumably did not cause much feeding competition between the suspension-feeding host and the endosymbiont, but facultative parasitism cannot be excluded. We assign category 4.

4.3  Corals as Hosts of Parasites Many parasitic associations involving fossil corals as hosts have been reported from Paleozoic tabulate and rugose corals (Tapanila 2005). All tabulate corals were colonial animals, while rugose corals could be solitary or colonial. The earliest macroscopic coral symbionts appeared in the Late Ordovician of North America and Baltica (Tapanila 2005; Vinn and Mõtus 2012) and some of them may have been

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parasites (Zapalski 2007, 2011). However, possible coral parasites were also common and diverse in the Mesozoic and Cenozoic (Voigt 1959, 1967; Zibrowius 1981; Lozouet and Renard 1998; Beuck et al. 2008; Santos et al. 2012; Klompmaker et al. 2016). Macrosymbiosis and coral parasites have been reviewed by Darrell and Taylor (1993) and more recently by Taylor (2015).

4.3.1  Tabulates In the Ordovician, tabulates were inhabited by various symbiotic invertebrates including worm bioclaustrations (Chaetosalpinx and Helicosalpinx) and tentaculitoid tubeworms (Cornulites celatus and Conchicolites hosholmensis). It is likely that worm bioclaustrations were made by some parasitic polychaetes (Zapalski 2007, 2011). We assign category 3. Worm bioclaustrations appear in the Katian of Laurentia (Tapanila 2004) and they remain common throughout the rest of Late Ordovician (Tapanila 2005). These tabulate symbionts were possibly suspension feeders analogous to modern polychaete endobionts in corals. However, their interaction with tabulates was likely not a feeding competition since tentaculitoid tubeworms fed on suspended organic material and tabulates were micropredators. In the Katian of Baltica, tabulate endobionts are represented by cornulitids (Cornulites aff. celatus and Conchicolites hosholmensis) and bioclaustrations (Chaetosalpinx sp.). Infestation rate (i.e., amount of specimens with bioclaustrations) differs among infested Baltic coral species (50% of Protoheliolites dubius specimens versus 10.8% of Propora speciosa specimens). Parasitism or mutualism is difficult to identify in Baltic cornulitid-tabulate associations (Vinn and Mõtus 2012). Tabulate corallites around the cornulitids show some changes in geometry, but their size is not significantly decreased. This can be interpreted as a weak negative influence of cornulitids on the host tabulate (Vinn and Mõtus 2012). Similar cornulitid-tabulate associations occur in the Hirnantian of Laurentia (Dixon 2010). We assign category 4. In the Silurian, tabulates housed various endobiotic symbionts, including rugose corals, worm bioclaustrations (Chaetosalpinx and Helicosalpinx; see Tapanila 2005), tentaculitoid tubeworms (Coralloconchus; see Mõtus and Vinn 2009), and lingulate brachiopods (Richards and Dyson-Cobb 1976). Two endobiotic symbionts, Chaetosalpinx sibiriensis (Fig. 4.2) and Coralloconchus bragensis, occur in Silurian corals of Podolia (Baltica). The endosymbiotic worms responsible for C. sibiriensis bioclaustrations are found only in certain tabulate species. The number of bioclaustrations in a single host varied from one to six in the reef-related community. Chaetosalpinx sibiriensis preferred certain coral species over the others, but showed no preference for the favositid or heliolitid type of morphology. Similarly to their Silurian counterparts, Devonian tabulates were inhabited by various symbiotic invertebrates including worm bioclaustrations (Chaetosalpinx, Helicosalpinx, Hicetes, and Phragmosalpinx; category 4 assigned) and tentaculitoid tubeworms (Torquaysalpinx sokolovi, Plusquellec 1968). The latter is assigned to category 4. The diversity of coral symbionts was higher in the Devonian than in the

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Fig. 4.2  Chaetosalpinx sibiriensis in Paleofavosites cf. collatatus Klaamann, GIT 481-65, Bagovitsa, Muksha Subformation, Ludlow, Podolia, Ukraine (after Mõtus and Vinn 2009)

Silurian, and they infested more coral species than in the Silurian (Tapanila 2005). In the Middle Devonian of SE Australia, Phragmosalpinx australiensis infested tabulate corals Gephuropora duni (Sokolov 1948). It is possible that Phragmosalpinx may have been a parasite similar to Chaetosalpinx (Zapalski 2007). Category 3 is assigned. Another worm bioclaustration, Hicetes innexus, occurs in the tabulate Pleurodictyum in the Devonian of Germany and North America (Tapanila 2005). The relationship of Hicetes to its tabulate host is not known, but parasitism cannot be ruled out. It is assigned to category 3. In the Givetian of NE Australia, tentaculitoid tubeworms Torquaysalpinx sokolovi infested tabulates Alveolites (Zhen 1996). Torquaysalpinx could have benefitted from this relationship by protection from predators, stabilization in agitated environments, and elevation above the sediment-­ water interface (Zhen 1996). The influence of Torquaysalpinx on its coral host is not known, but parasitism is a possibility. It is assigned to category 4.

4.3.2  Rugose Corals In the Ordovician, rugose corals were inhabited by some wormlike invertebrates forming bioclaustrations (Chaetosalpinx ferganensis and Chaetosalpinx sibiriensis) (Tapanila 2005). There is no data on rugosan endobionts from the Silurian (Tapanila 2005), but it is likely that the situation was similar to the Ordovician. In the Devonian, rugose corals housed various endobiotic symbionts including worm bioclaustrations (Chaetosalpinx ferganensis and Helicosalpinx asturiana; assigned to category 4), possible tentaculitoid tubeworms (Streptindytes acervulariae; assigned to category 4), and unidentified paired aperture cavities (Tapanila 2005). The endobiotic symbionts in rugose corals are less diverse than in tabulates, presumably because large tabulates attractive to symbionts are more common than colonial rugosans.

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4.3.3  Mesozoic to Recent Corals There are many records of symbiotic endobionts in the post-Paleozoic corals. Microendoliths are commonly found in the calcareous skeletons of scleractinian corals of Early Cretaceous age (Kolodziej et al. 2012). These traces were made by autotrophic chlorophyte algae and possibly also by fungi. They were capable of weakening the skeletons of the host corals. In addition, the fungal microendoliths may have attacked the coral polyps (Taylor 2015). Thus, they may have been coral parasites. It is assigned to category 3. Extant corals symbiotic with sipunculan worms develop corallum modifications that seem to meet the needs of the coral’s worm partner (Stolarski et al. 2001). The Early Cretaceous of France is the oldest example of sipunculan-coral symbiosis in which the monoporous-type corallum was modified in the same way as in extant monoporous Heterocyathus (Stolarski et al. 2001). The symbiotic relationship starts when a coral larva settles on a substrate already inhabited by a sipunculan. Since the sipunculan also grows, the shell may become too small to shelter it and the coral can provide the necessary protection by growing around the protruding worm to form a sclerenchyme extension in continuation of the shell (Stolarski et  al. 2001). The sipunculans do not cause any damage to the coral skeleton, and it is likely that they were not parasites. It is therefore assigned to category 4. In the Upper Cretaceous of southern Israel, specimens of the small compound coral Aspidiscus cristatus contain evidence of symbiosis with bivalves (Wilson et al. 2014) (Fig. 4.3). The corals

Fig. 4.3  Aspidiscus cristatus oral surface with paired apertures of Gastrochaenolites ampullatus visible in the upper half. Early Cenomanian from Nahal Neqarot, Israel (after Wilson et al. 2014)

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have paired holes on their upper surfaces leading to a common chamber below identified as the bivalve boring trace fossil Gastrochaenolites ampullatus (Wilson et al. 2014). Bivalve larvae settled on living coral surfaces and began to bore into the underlying aragonitic skeletons causing damage to the host coral (Wilson et  al. 2014). Thereafter the corals added new skeleton around the paired siphonal tubes of the invading bivalves, producing a bioclaustration (Wilson et al. 2014). This is early evidence of a parasitic relationship between scleractinian corals and boring bivalves (Wilson et al. 2014). It is assigned to category 3. In the Late Cretaceous of Europe the ascothoracid Endosacculus moltkiae left cysts in the octocoral Moltkia minuta (Voigt 1967). A somewhat similar association occurred between ascothoracids and alcyonaceans in the Cretaceous (Voigt 1967). This ascothoracid-coral association was either parasitic or commensal (Voigt 1959, 1967). It is assigned to category 4. Boring Coralliophilidae gastropods have been inhabiting living corals since the Oligocene (Lozouet and Renard 1998). The evolution of their borer lifestyle is related to the development of modern coral reefs, and their modern representatives are coral parasites (Lozouet and Renard 1998). It is assigned to category 2. Barnacles of the family Pyrgomatidae are among the most common and well-known obligatory associates of host scleractinian corals in modern oceans (Santos et al. 2012) (Fig.  4.4). Their earliest representatives appeared in the Miocene (Santos et  al. 2012). There are several Recent pyrgomatid species that have a parasitic relation with the host coral (Moyse 1971) and fossil pyrgomatids were likely parasites too (Santos et al. 2012). It is assigned to category 2. Some solitary caryophylliid and flabellid scleractinian corals from the Pliocene of the western Mediterranean exhibit long groove-shaped bioersional structures (Sulcichnus) running along the surface of the thecae (Martinell and Domènech 2009). Sulcichnus is attributed to the activity

Fig. 4.4  Coral-barnacle association, sections of several specimens of Imbutichnus costatum from Langhian–Serravallian, middle Miocene, Porto Santo, Portugal (after Santos et al. 2012)

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of polychaetes that infested living corals (Martinell and Domènech 2009). Similar structures are produced today by the symbiotic eunicid Lumbrineris flabellicola (Martinell and Domènech 2009). It is herein assigned to category 4. Cryptochirids are small, symbiotic crabs that live in domiciles in modern corals (Klompmaker et al. 2016). Their crescentic pits occur in Western Atlantic fossil corals from the Pliocene onwards (Klompmaker et al. 2016). Cryptochirids have been considered parasitic to their coral host (Simon-Blecher et  al. 1999), but several authors disagree with this interpretation (Klompmaker et al. 2016). It is assigned to category 2. During the Quaternary, cold-water corals were infested by parasitic foraminifera in the aphotic zone (Beuck et al. 2008; Walker et al. 2017). We assign category 2. In modern seas, six copepod species have been found in cage-like globular galls (walls perforated) on stylasterine corals (Zibrowius 1981). Copepods produced galls in the host coral and likely caused some harm to their host and therefore they could be parasites. Recent pycnogonid arthropods may inhabit galls in gorgonian and scleractinian hosts (Staples 2005), and the gall may have negative effects on the host coral, so parasitism is a possibility. It is assigned to category 4.

4.4  Bryozoans as Hosts of Parasites Throughout the Phanerozoic, bryozoans have housed a variety of endobiotic symbionts, including bioclaustrations, rugose corals, tabulates, cornulitids, and conulariids. Three species of Anoigmaichnus bioclaustrations, and undescribed semi-conical bioclaustrations, occur in trepostomes in the Ordovician of Baltica (Vinn et  al. 2018a) (Fig. 4.5). Anoigmaichnus may have been a bryozoan parasite (Vinn et al. 2016). It is assigned to category 3. Ernst et  al. (2014) reported a new wormlike

Fig. 4.5  Anoigmaichnus zapalskii in trepostome bryozoan Mesotrypa expressa Bassler from Katian of northern Estonia (GIT 770-7-3) (after Vinn et al. 2018)

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bioclaustration, Chaetosalpinx tapanilai, in cystoporate bryozoans of the Middle Devonian of Germany. It is assigned to category 3. Several cases of bryozoan-rugosan symbiosis occur in the Ordovician (Vinn et al. 2017). Endobiotic rugose coral symbionts are known from Upper Ordovician (Katian) bryozoans of Estonia (Vinn et al. 2016). Multiple rugosans were partially embedded in colonies of the cystoporate bryozoan Ceramopora intercellata, leaving only their apertures free on the growth surface of the host (Vinn et al. 2016). Rugosans had a presumably mutualistic relationship with their bryozoan hosts in the Upper Ordovician of Estonia, but parasitism cannot be ruled out. It is assigned to category 4. Symbiosis between the rugosans and bryozoans was likely facultative (Vinn et  al. 2016). Streptelasma divaricans intergrowths have been described in Upper Ordovician (Richmondian) bryozoans of the Cincinnati Arch region, USA (Elias 1982). The coral larvae frequently settled on living bryozoan colonies, which is evidenced by upward growth of the host around these epizoans (Elias 1982). A similar association occurs in the Upper Ordovician (Gamachian) of Missouri in the USA where Streptelasma sp. had a symbiotic relationship with bryozoans (McAuley and Elias 1990). It is assigned to category 4. Similarly to rugosans, tabulates formed symbiotic associations with bryozoans. A species of Aulopora and the bryozoan Leioclema formed a symbiotic association in the Lower Devonian of western Tennessee (McKinney et  al. 1990). Aulopora corallites, except for their calices, were entirely embedded by a thin encrustation of Leioclema. However, this association was presumably mutualistic with benefits including escape from limited space on the substratum into a higher tier of suspension feeders (McKinney et al. 1990). It is assigned to category 4. Other skeletonized endobiotic invertebrates, such as conulariids, are also known in bryozoans. Conulariids have been reported in several bryozoan species in the Sandbian and Katian of Estonia (Vinn and Wilson 2015; Vinn et al. 2019) (Fig. 4.6).

Fig. 4.6  Two conulariids Climacoconus bottnicus (Holm) in Diplotrypa bicornis (Eichwald) from Sandbian, northern Estonia, note the slightly elevated apertures of conulariids (GIT 720-4) (after Vinn et al. 2019)

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They usually were completely embedded in the bryozoans, leaving only their apertures free on the growth surface of the host. Each bryozoan could host several conulariid specimens (Männil 1959). It is possible that conulariids sought additional protection against predators by their embedment within the bryozoan skeleton and a relatively stable growth substrate (Vinn and Wilson 2015). The influence of conulariids on the bryozoans is not known, but a parasitic relationship is possible. It is assigned to category 4. Three species of trepostome bryozoans were infested by cornulitids in the Late Ordovician of Estonia (Vinn et al. 2018b). Among them, Cornulites sp. and Mesotrypa excentrica formed a true symbiotic association that, however, was rare (Vinn et al. 2018b). It is not known whether this symbiotic association was obligatory or facultative for the cornulitid, but it was definitely facultative for the bryozoan (Vinn et al. 2018b). Cornulitids may have competed for the food with bryozoans and the association may have been parasitic (Vinn et al. 2018a, b). It is assigned to category 4. Several genera of modern cheilostome bryozoans are hosts of epibiotic zancleid hydroids that have a diversity of host-guest relationships that in some cases involve parasitism of the bryozoan by the hydroid (McKinney 2009). Devonian fenestrate bryozoans secreted skeletal enclosures for modular systems of curved, distally expanding, distolaterally budding tubes generated by a soft-bodied colonial epibiont called Caupokeras (McKinney 2009). The size and morphology of these tubes are similar to those of extant hydroids, and they represent a symbiotic relationship between the host fenestrate bryozoans and the epibiotic hydroids (McKinney 2009). Caupokeras did not cause much damage to the host bryozoan, but on the bases of modern analogues a parasitic relationship is possible. It is assigned to category 2. Multiple funnel-shaped tubes are described opening on the frontal surfaces of encrusting cyclostome bryozoans from the Lower Cenomanian of Germany (Taylor and Voigt 2006) (Fig.  4.7). These bioclaustrations result from infestation by Fig. 4.7  Hyporosopora sp. with symbiont tubes from Gault Clay (Albian), Cambridgeshire, England (after Taylor and Voigt 2006)

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Fig. 4.8  Culicia parasita Michelin in a bryozoan from Pontlevoy, Loir-etCher, Miocene (after Chaix and Cahuzac 2005)

soft-­bodied symbionts. More than ten symbiont tubes can be found within a single bryozoan colony. Bioclaustrations are similar to tubes made around tanaid crustaceans and spionid polychaetes by recent cyclostomes, but the Cretaceous examples indicate a more intimate symbiosis as the tube interior was evidently lined by bryozoan secretory epithelium rather than cuticle (Taylor and Voigt 2006). This association was either commensal or parasitic (Taylor 2015). It is assigned to category 3. In the Neogene, the bryozoan Celleporaria palmata lived facultatively in association with the scleractinian coral Culicia (Cadée and McKinney 1994) (Fig. 4.8). The association was obligatory for the coral and the symbiosis was most probably mutualistic, but parasitism cannot be ruled out (Cadée and McKinney 1994; Chaix and Cahuzac 2005). It is assigned to category 4. Interestingly, this symbiosis did not initially exist when the taxon Culicia first appeared in the Oligocene (Chaix and Cahuzac 2005).

4.5  Possible Parasites in Graptolites There are several reports of parasitism in pelagic graptoloid graptolites (see Bates and Loydell 2000; Maletz 2017). These reports deal with outgrowths of the periderm in the form of blisters or cysts, or sometimes as small tubes (Taylor 2015; Maletz 2017). Skeletal outgrowth of graptoloids probably influenced the

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hydrodynamics of the floating graptoloid colony (Underwood 1993) and could alter its buoyancy (Taylor 2015; Maletz 2017). Kozlowski (1970) described larger diameter tubes termed as tubothecae in benthic tuboid and dendroid graptolites. These tubes were associated with commensal annelids (Kozlowski 1970). Urbanek and Mierzejewski (1982) demonstrated that tubothecae were secreted by graptolites and constitute a bioclaustration that was formed around symbionts. It is assigned to category 4.

4.6  Colonial Organisms as Parasites Colonial animals often infest or otherwise live in association with other organisms and they can be parasites. Benthic colonial invertebrates often foul or bore into living hosts (Taylor 2015). However, colonial animals are more often hosts than parasites and that has been so throughout the Phanerozoic. Among colonial symbionts, the most abundant fossil record belongs to syringoporid tabulates (Fig.  4.2e). They are known to form symbiotic associations with stromatoporoids from the Silurian to Devonian (Vinn 2016). Syringoporids can grow separately or as symbiotic endobionts within stromatoporoids (Vinn 2016). Endobiotic syringoporid colonies are always completely embedded within a host stromatoporoid, leaving only the corallite apertures free on the growth surface of the stromatoporoid (Vinn 2016). It is likely that the calcareous rigid skeletons of syringoporid tabulates may have reinforced the skeletons of stromatoporoids and had a positive effect on the host. However, large syringoporid colonies could also reduce the feeding surface of the host and thus reduce its feeding efficiency. Therefore a parasitic nature of this association is also possible. It is assigned to category 4. Syringoporid tabulates occur in 27 stromatoporoid genera (Mistiaen 1984). There are five Syringopora species known in the Devonian stromatoporoids of Bohemia (May 2005). The Caunopora type of syringoporid-stromatoporoid symbiosis, which is so common in the Devonian (Mistiaen 1984; May 1999), does not occur in the early Silurian of Anticosti Island, Canada, even though syringoporids were common in the East Point Member and Pavillon Member (Nestor et  al. 2010). Similarly, syringoporid-­ stromatoporoid symbiosis is missing in the Late Ordovician and early Silurian of Estonia and Sweden (Vinn 2016). The Late Silurian examples of such associations are known from Gotland (Sweden) (Kershaw 1987) and Saaremaa (Estonia) (Nestor 1966), though less common than in the Devonian (Mistiaen 1984). Syringoporid-stromatoporoid symbiosis likely evolved in the middle Silurian and achieved its maximum in the Devonian (Vinn 2016). Colonial tabulate corals also settled on living crinoid stems and formed a symbiotic association (Galle and Prokop 2000; Głuchowski 2005; Berkowski and Zapalski 2014; Vinn 2017). This is shown by crinoid pluricolumnals being

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overgrown from all sides (Berkowski and Zapalski 2014). The epizoan influence on the host was presumably negative as it caused a change in the mechanical properties of the crinoid stalk (losing flexibility) (Berkowski and Zapalski 2014). The tabulates profited from the elevated position above the seafloor and access to nutrient-bearing water currents (Berkowski and Zapalski 2014). Berkowski and Zapalski (2014) suggested that the relationship of tabulates and crinoids was close to parasitism. It is assigned to category 3. An important example of corals grown on crinoid stems is that of the tabulate Antholites, which has a specific site of attachment generally just below the crinoid calyx (Stumm and Watkins 1964; McIntosh 1980; Brett 1999). Only four Devonian tabulate species attached to live crinoids have been recorded to date (Galle and Prokop 2000; Głuchowski 2005; Berkowski and Zapalski 2014). This type of association ranges from the Silurian (Gibson and Broadhead 1989) to the Permian (Gerth 1921). Solitary rugose corals also formed similar associations with crinoids in the Devonian of Morocco (Berkowski and Klug 2012). It is assigned to category 3. Symbiosis of crinoids with the possible tabulate Cladochonus occurred during the Mississippian (Donovan and Lewis 1999). Cladochonus corallites grew circumferentially around an erect column of a living crinoid (Donovan and Lewis 1999). Cladochonus often caused malformations in the crinoid stem, and it was partially embedded by the crinoid skeleton (Donovan and Lewis 1999). The influence of Cladochonus on the host may have been negative as it caused a loss of flexibility in the column. This association could have been parasitic (Vinn 2017). It is assigned to category 3. Ascidian tunicates or colonial hydroids are inferred to have formed bioclaustrations in trepostome bryozoans in the Late Ordovician of North America (Catellocaula vallata; Palmer and Wilson 1988). Hydroids sometimes produce horizontal, rootlike stolons, from which arise single upright polyps or branches of polyps, but they are much smaller than Catellocaula bioclaustrations. Ascidiacian tunicates also include stoloniferous colonial forms, which in shape and size correspond well to Catellocaula, supporting its tunicate nature. Catellocaula bioclaustrations are located at the same level within the bryozoan zoarium, and invariably mark growth interruption. These interruptions are interpreted as having been caused by local damage to the bryozoan host. Thus a parasitic relationship seems likely (Palmer and Wilson 1988). It is assigned to category 3. An alcyonarian-Syringopora association is known from the Viséan of Morocco and Spain (Coronado et al. 2015). In this association, an alcyonarian epibiont was attached to the syringoporid (Coronado et al. 2015). The epithecal scales similar to those in Syringoalcyon have also been reported in several genera of tabulate and rugose corals from the Silurian and Lower Devonian (Shurigina 1972; Ogar 1992). The alcyonarians did not cause damage to the host coral skeleton, and they may have not been parasites, though parasitism cannot be ruled out (Coronado et  al. 2015). It is assigned to category 4.

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Serpulid tubes infested by the colonial hydroid Protulophila gestroi, Rovereto, 1901, are common in the Jurassic and Cretaceous of Europe (Jäger 1983; Zágoršek et al. 2009). The hydroid-serpulid association has a stratigraphic range from Jurassic to the Pliocene (Zágoršek et  al. 2009). However, this symbiotic association was likely not parasitic as Protulophila did not cause any damage to serpulid tube. It most likely also did not interfere with the feeding of the serpulid host. It is assigned to category 4.

4.7  Discussion Analysis of the stratigraphic distribution of putative parasitic associations provides us with insights into their evolution. The stratigraphic distribution of parasitic associations in colonial animals is divided into two separate blocks: Paleozoic (Ordovician to Permian) parasitic associations of colonial animals form the first block and Mesozoic to Recent parasitic associations of colonial animals form the second block (Fig.  4.9). This division of parasitic associations corresponds well to the Sepkoski Paleozoic and Modern faunas (Sepkoski 1981; Alroy 2004). Therefore, we call these subdivisions of the Paleozoic and the Modern parasitic associations of colonial animals. The Paleozoic parasitic associations of colonial animals are characterized by abundance of parasites belonging to extinct groups such as tentaculitoid tubeworms (including cornulitids, Torquaysalpinx, Streptindytes), Paleozoic-type worm bioclaustrations (such as Chaetosalpinx, Helicosalpinx, Phragmosalpinx, Hicetes, and Anoigmaichnus), and Paleozoic corals (such as rugosans and tabulates). Modern parasitic associations of colonial animals are characterized by parasites such as various arthropods (ascothoracids, pyrgomatid, cryptochirids, copepods), worms (sipunculans, serpulids, sabellids), foraminifera, and hydroids. A similarity between Paleozoic and modern parasitic associations is the presence of hydroid-bryozoan symbiosis and coral-bryozoan symbiosis both in the Paleozoic and Cenozoic. Another similarity is that corals have been major hosts for both Paleozoic and modern parasites. There is a gap in the distribution of parasitic associations of colonial animals extending the entire Triassic, but it is most likely due to collecting and study biases. The other interesting feature is the subdivision of Paleozoic parasitic associations of colonial animals into Early to Middle Paleozoic associations and Late Paleozoic associations. The Early to Middle Paleozoic associations are more diverse than the Late Paleozoic associations and Cenozoic parasitic associations of colonial animals seem to be more diverse than their Mesozoic equivalents.

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Fig. 4.9  Stratigraphic distribution of possible parasitic associations

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Acknowledgements  Financial support to O.V. was provided by the Estonian Research Council project IUT20-34. M.W. received funding from the College of Wooster Luce Funds.

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Underwood CJ (1993) The position of graptolites within Lower Palaeozoic planktic ecosystems. Lethaia 26:189–202 Urbanek A, Mierzejewski P (1982) Ultrastructure of the tuboid graptolite tubotheca. Paläontol Z 56:87–93 Vinn O (2016) Symbiotic endobionts in Paleozoic stromatoporoids. Palaeogeogr Palaeoclimatol Palaeoecol 453:146–153 Vinn O (2017) Symbiosis between Devonian corals and other invertebrates. PALAIOS 32:382–387 Vinn O, Mõtus M-A (2014a) Endobiotic rugosan symbionts in stromatoporoids from the Sheinwoodian (Silurian) of Baltica. PLoS One 9(2):e90197 Vinn O, Mõtus M-A (2014b) Symbiotic worms in biostromal stromatoporoids from the Ludfordian (late Silurian) of Saaremaa, Estonia. GFF 136:503–506 Vinn O, Wilson MA (2010) Endosymbiotic Cornulites in the Sheinwoodian (Early Silurian) stromatoporoids of Saaremaa, Estonia. Neues Jahrb Geol Palaontol Abh 257:13–22 Vinn O, Wilson MA (2015) Symbiotic interactions in the Ordovician of Baltica. Palaeogeogr Palaeoclimatol Palaeoecol 436:58–63 Vinn O, Wilson MA, Mõtus M-A (2013) Symbiotic worm endobionts in a stromatoporoid from the Rhuddanian (lower Silurian) of Hiiumaa, Estonia. PALAIOS 28:863–866 Vinn O, Wilson MA, Mõtus M-A, Toom U (2014) The earliest bryozoan parasite: Middle Ordovician (Darriwilian) of Osmussaar Island, Estonia. Palaeogeogr Palaeoclimatol Palaeoecol 414:129–132 Vinn O, Ernst A, Toom U (2016) Earliest symbiotic rugosans in cystoporate bryozoan Ceramopora intercellata Bassler, 1911 from Late Ordovician of Estonia (Baltica). Palaeogeogr Palaeoclimatol Palaeoecol 461:140–144 Vinn O, Ernst A, Toom U (2017) Rare rugosan-bryozoan intergrowth from the Late Ordovician of Estonia. Carnets Géol 17:145–151 Vinn O, Ernst A, Toom U (2018a) Bioclaustrations in upper Ordovician bryozoans from northern Estonia. Neues Jahrb Geol Paläont Abh, vol 289, p 113 Vinn O, Ernst A, Toom U (2018b) Symbiosis of cornulitids and bryozoans in the Late Ordovician of Estonia (Baltica). PALAIOS 33:290–295 Vinn O, Ernst A, Wilson MA, Toom U (2019) Symbiosis of conulariids with trepostome bryozoans in the Upper Ordovician of Estonia (Baltica). Palaeogeogr Palaeoclimatol Palaeoecol 518:89–96 Voigt E (1959) Endosacculus moltkiae n. g. n. sp., ein vermutlicher fossiler Ascothoracide (Entomostr.) als Cystenbildner bei der Oktokoralle Moltkia minuta. Paläontol Z 33:211–223 Voigt E (1967) Ein vermutlicher Ascothoracide (Endosacculus (?) najdini n. sp.) als Bewohner einer kretazischen Isis aus der UdSSR. Paläontol Z 41:86–90 Walker SE, Hancock LG, Bowser SS (2017) Diversity, biogeography, body size and fossil record of parasitic and suspected parasitic foraminifera: a review. J Foraminifer Res 47(1):34–55 Wilson MA, Vinn O, Palmer TJ (2014) Bivalve borings, bioclaustrations and symbiosis in corals from the Upper Cretaceous (Cenomanian) of southern Israel. Palaeogeogr Palaeoclimatol Palaeoecol 414:243–245 Zágoršek K, Taylor PD, Vodrážka R (2009) Coexistence of symbiotic hydroids (Protulophila) on serpulids and bryozoans in a cryptic habitat at Chrtníky (lower Turonian, Czech Republic). Bull Geosci 84:631–636 Zapalski MK (2007) Parasitism versus commensalism: the case of tabulate endobionts. Palaeontology 50:1375–1380 Zapalski MK (2011) Is absence of proof a proof of absence? Comments on commensalism. Palaeogeogr Paleoeclimatol Palaeoecol 302:484–488 Zapalski MK, Hubert BLM (2010) First fossil record of parasitism in Devonian calcareous sponges (stromatoporoids). Parasitology 138:132–138 Zhen Y-Y (1996) Succession of coral associations during a Givetian transgressive-regressive cycle in Queensland. Acta Palaeontol Pol 41:59–88 Zibrowius H (1981) Associations of Hydrocorallia Stylasterina with gall-inhabiting Copepoda Siphonostomatoidea from the south-West Pacific. Part I. On the stylasterine hosts, including two new species, Stylaster papuensis and Crypthelia cryptotrema. Bijdragen tot de Dierkunde 51:268–286

Chapter 5

Crustaceans as Hosts of Parasites Throughout the Phanerozoic A. A. Klompmaker, C. M. Robins, R. W. Portell, and A. De Angeli

Abstract  The fossil record of crustaceans as hosts of parasites has yielded three confirmed associations: swellings on Jurassic–Pleistocene decapods attributed to epicaridean isopods, feminization of Cretaceous and Miocene crabs possibly caused by rhizocephalan barnacles, and presumed pentastomids on/in Silurian ostracods. Cestode platyhelminth hooks and swellings by entoniscid isopods have yet to be recognized. Relative to 2014, we report a 45% increase to 128 fossil decapod species with swellings (ichnotaxon Kanthyloma crusta) in the branchial chamber attributed to epicarideans. Furthermore, using a Late Jurassic decapod assemblage from Austria, we find (1) no correlation between genus abundance and prevalence of K. crusta, (2) host preference for some galatheoids (as for a mid-Cretaceous assemblage from Spain), and (3) a larger median size of parasitized versus non-­ parasitized specimens for two abundant species. The latter result may be caused by infestation throughout ontogeny rather than exclusively in juveniles and/or possible selection for larger individuals. Keywords  Barnacle · Biotic interaction · Bopyridae · Cirripedia · Coevolution · Crustacea · Decapoda · Isopoda · Ostracoda · Parasitism

A. A. Klompmaker (*) Department of Museum Research and Collections & Alabama Museum of Natural History, University of Alabama, Tuscaloosa, AL, USA Department of Integrative Biology & Museum of Paleontology, University of California Berkeley, Berkeley, CA, USA e-mail: [email protected] C. M. Robins Alabama Museum of Natural History, University of Alabama, Tuscaloosa, AL, USA Museum of Paleontology, University of California Berkeley, Berkeley, CA, USA R. W. Portell Florida Museum of Natural History, University of Florida, Gainesville, FL, USA A. De Angeli Museo Civico “G. Zannato”, Montecchio Maggiore (VI), Italy © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 K. De Baets, J. W. Huntley (eds.), The Evolution and Fossil Record of Parasitism, Topics in Geobiology 50, https://doi.org/10.1007/978-3-030-52233-9_5

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5.1  Introduction Extant crustaceans (or pancrustaceans) act as both parasites and hosts of parasites (e.g., Yamaguti 1963; Cressey 1983; Boxshall et  al. 2005; Boyko and Williams 2011; Trilles and Hipeau-Jacquotte 2012; Smit et  al. 2014; Klompmaker and Boxshall 2015; Boxshall and Hayes 2019). For this chapter, we define parasitism as a symbiotic relationship in which the parasite is nutritionally dependent on the host for at least part of its life cycle and has a negative impact on the fitness of the host (cf. Combes 2001; Tapanila 2008). Over 7000 extant crustaceans are intermediate and final hosts to parasites from diverse clades such as acanthocephalans, cestodes, crustaceans (e.g., Copepoda, Cirripedia, Isopoda, Tantulocarida), digenean trematodes, monogeneans, nematodes, and protists (e.g., Shields 1994; Boxshall et  al. 2005; Park et al. 2007; Williams and Boyko 2012; Klompmaker and Boxshall 2015; Boxshall and Hayes 2019). Representatives of nearly all to all major clades of crustaceans serve as hosts today, including amphipods, branchiopods, cirripeds, copepods, decapods, euphausiaceans, mysidaceans, ostracods, peracarids, and stomatopods (e.g., Boxshall et al. 2005; Klompmaker and Boxshall 2015; Boxshall and Hayes 2019). The impact of parasitism on crustaceans is likely to be enormous, but understudied in the context of whole ecosystems. The fossil record of parasitism involving crustaceans has been reviewed recently (Klompmaker and Boxshall 2015, for crustaceans as parasites and hosts; Haug et al. 2021, for crustaceans as parasites). Three instances of parasites in crustacean hosts have been reported thus far (Fig. 5.1). This low number and the fact that the stratigraphic coverage of two of these records is spotty can be ascribed to a combination of the small size of parasites, the low preservation potential of parasites due to their general lack of a hard skeleton, the fact that not all parasites leave recognizable traces, and the lack of targeted research. One notable exception is epicaridean isopods, which cause characteristic swellings on decapod crustacean carapaces. This association represents a nearly continuous record since the Jurassic (Klompmaker et al. 2014; Klompmaker and Boxshall 2015), presenting an ideal model system to study various aspects of parasitism through time. The goal of this chapter is to re-review the fossil record of crustaceans as hosts of parasites because ample new evidence has been found in recent years. We focus primarily on swellings in decapod crustaceans attributed to epicaridean isopod parasites by (1) presenting a substantially expanded list of infested decapod species and (2) using a vast Late Jurassic assemblage to test the relationship between taxon abundance and infestation percentage, assess host preference, and evaluate the size of parasitized versus non-parasitized specimens for two species. Subsequently, we briefly review the claimed evidence for parasitism of (1) rhizocephalan barnacles in fossil decapod crustaceans, (2) ciliates on ostracods, and (3) pentastomids on ostracods. Finally, modern parasitism on crustaceans with preservation potential is discussed. Institutional abbreviations: MAB Oertijdmuseum, Boxtel, The Netherlands, MCV Museo Civico D. Dal Lago, Valdagno, Vicenza, Italy, NHMW Naturhistorisches Museum Wien, Vienna, Austria, UF Florida Museum of Natural History at the University of Florida, Gainesville, Florida, USA.

Fig. 5.1  Stratigraphic ranges of crustaceans as hosts of parasites. Black parts represent known occurrences, while grey parts are inferred occurrences. Black occurrences have been plotted at the stage level where possible. The category in bold italic font is based on body fossils of the parasite; others are based on morphologies inferred to have been caused by parasites in the host taxon. Timescale on left produced with TSCreator 6.3 (http://www.tscreator.org). Modified and updated from Klompmaker and Boxshall (2015: Fig. 12)

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5.2  Isopod Swellings in Decapod Crustaceans 5.2.1  General Information Epicaridea (Bopyroidea and Cryptoniscoidea) parasitize calanoid copepods as intermediate hosts and other crustaceans as final hosts, following three larval stages (e.g., Williams and Boyko 2012). Approximately 800 species are known and they are found in all oceans today (e.g., Williams and Boyko 2012). The phylogenetic relationship of epicaridean families has recently been clarified using 18S rDNA, resulting in 13 accepted families to date arranged in two superfamilies, Cryptoniscoidea and Bopyroidea (Boyko et  al. 2013; WoRMS 2019). For Bopyroidea, Ionidae, as currently defined, infest Axiidea; Bopyridae parasitize species of most decapod clades; and Entoniscidae are known from Anomura, Brachyura, Caridea, and Stenopodidea thus far (e.g., Markham 1986: Table 1; Adkison 1990; Boyko et  al. 2013: Fig.  3). Most Bopyroidea are ectoparasitic (Ionidae and Bopyridae, but not the endoparasitic Entoniscidae). Their deformed female individuals often create swellings in the cuticle of one or rarely both branchial chambers of decapod crustaceans (e.g., Markham 1986; Boyko and Williams 2009; Williams and Boyko 2012; Boyko et al. 2013). They feed on hemolymph and ovarian fluids after piercing the inner cuticle of the host (e.g., Bursey 1978; Lester 2005), whereas the much smaller, undeformed, less modified males attach themselves to females subsequently for reproduction and do not form swellings in the cuticle. Effects on the host are manifold and can be dramatic (Table 5.1). Table 5.1  Parasitic epicarideans cause a variety of negative effects on their decapod hosts Effect of bopyroid isopods on decapod hosts Lower fecundity Castration Feminization of males

Altered sexual characters of females Gill damage and scar tissue development Reduced molt frequency (Unintended) mortality Increased predation risk Lower activity levels Lower oxygen consumption Different host sex ratios Sources are not comprehensive

Source(s) Van Wyk (1982), Calado et al. (2006), Hernáez et al. (2010) McDermott (1991), González and Acuña (2004), Markham and Dworschak (2005), Sherman and Curran (2013) O’Brien and Van Wyk (1985), Markham and Dworschak (2005), Petrić et al. (2010), Romero-Rodríguez and Román-Contreras (2011), Yasuoka and Yusa (2017) Lee et al. (2016), Yasuoka and Yusa (2017) Bursey (1978), McDermott (1991), Corrêa et al. (2018) Van Wyk (1982), O’Brien and Van Wyk (1985) Anderson (1990) Brinton and Curran (2015) Bass and Weis (1999), McGrew and Hultgren (2011) Anderson (1975), Neves et al. (2000) Somers and Kirkwood (1991), McDermott (2002), Cericola and Williams (2015)

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Fig. 5.2  Decay of the carapace of the modern hermit crab Clibanarius vittatus (Bosc, 1802), and its parasitic bopyrid [most likely Bopyrissa wolffi Markham, 1978, see Markham 1978 and McDermott et al. 2010] in the swollen right branchial chamber. The carapace is tilted to the left to better observe the decay of the parasite. The bopyrid body outline is still visible on day 20, but much less so subsequently when a smaller red spot is observed. For experimental setup and conditions see Klompmaker et al. (2017). 1st, 2nd, and 4th image modified from same reference. Scale bar: 5.0 mm wide

The body fossil record of epicarideans is nearly nonexistent. No adults have been found in decapod body chambers thus far due to their low preservation potential, as also shown experimentally (Klompmaker et al. 2017; Fig. 5.2). Only some epicaridean larvae have been found in Miocene and Late Cretaceous amber (SerranoSánchez et al. 2016; Néraudeau et al. 2017; Schädel et al. 2019, 2021). However, the swellings in the oft-calcified cuticle of decapod hosts can be preserved and detected relatively easily in the fossil record (e.g., Wienberg Rasmussen et al. 2008; Ceccon and De Angeli 2013; Robins et al. 2013; Klompmaker et al. 2014; Klompmaker and Boxshall 2015; Hyžný et al. 2015). These swellings have been referred to as the ichnotaxon Kanthyloma crusta Klompmaker et al., 2014 (see also Klompmaker and Boxshall 2015). The earliest claimed swelling is in a lobster from the Early Jurassic (Toarcian) of Indonesia, but this record is doubtful (Wienberg Rasmussen et al. 2008; Klompmaker et al. 2014). The Late Jurassic (Oxfordian) yields the first definite examples, suggesting coevolution between epicarideans and their decapod host for at least 160 million years. Most infested fossil species are brachyurans and galatheoids. Recently, Wisshak et al. (2019) considered K. crusta to not represent an ichnotaxon because bioerosion would be a minor factor and not independent from the host reaction. However, the mandibles of epicarideans bore into the inner cuticle of their host (Bursey 1978, for a bopyrid). Moreover, epicarideans grow along with their decapod host (e.g., Allen 1966; Beck 1980; Cash and Bauer 1993; Roccatagliata and Lovrich 1999; González and Acuña 2004; Baeza et al. 2018), suggesting that they actively push aside the cuticle of the host as they grow. They molt (and thus grow primarily) around the time the host molts (Cash and Bauer 1993: p.  118), when they can move the still hardening cuticle to create more space. Thus, they push aside their substrate in a way that is analogous to a footprint, and, therefore, Kanthyloma is a valid ichnotaxon.

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5.2.2  Global Meso- and Cenozoic Data Fossil decapod crustacean species with at least one specimen containing a swelling in the branchial region attributed to an epicaridean parasite have been listed previously (Van Straelen 1928: p.  51; Van Straelen 1931: p.  56; Houša 1963: p.  110; Förster 1969: p. 53–54; Markham 1986: Table 2; Müller et al. 2000: p. 69; Wienberg Rasmussen et al. 2008: Table 2; Klompmaker et al. 2014: Table 3). The most recent report identified 88 parasitized species. Targeted research on Meso-Cenozoic decapod assemblages for evidence of Kanthyloma crusta since the summer of 2017, published research since 2014, and new discoveries of infested species in older literature have led to an increase of 45% of known infested fossil species, totaling 128 infested species (Fig.  5.3, for examples of new and some known occurrences; Table 5.2). This remarkable rise and the total number of infested decapod species today exceeding 550 (Boyko and Williams 2009: Fig.  6, and subsequent papers) suggest that more infested fossil taxa are to be expected. Most infested fossil species represent Brachyura and Galatheoidea (Fig. 5.4b), and are primarily found in Europe (100/128 or 78%, Table 5.2). The highest number of infested species on the epoch level is known from the Late Jurassic (Fig. 5.4a). A Late Jurassic peak was also shown for the percentage of infested decapod species per epoch in the Mesozoic (Klompmaker et al. 2014: Fig. 6). Although they argued that elevated collecting and reporting of K. crusta in the Late Jurassic may explain part of the peak, they found a biological explanation more likely. Variable reporting may indeed be a factor because multiple papers exist specifically dedicated to this type of parasitism in the Late Jurassic (Remeš 1921; Bachmayer 1948; Houša 1963; Radwański 1972), while only two papers have focused on K. crusta from younger, pre-Holocene epochs (Ceccon and De Angeli 2013: Eocene; Klompmaker et  al. 2014: mid-Cretaceous). Whether this type of parasitism is truly reaching its peak in the Late Jurassic can only be assessed by studying the infestation prevalence on the finest possible scale using specimens from many assemblages across time and location. This study is currently ongoing.

5.2.3  Abundance vs. Infestation Percentage per Taxon Multiple studies have shown that host density positively affects the transmission rate of parasites. For example, there is a positive correlation between mammal host density across many species and strongylid nematode parasite abundance in modern ecosystems (Arneberg et al. 1998). For decapods, host abundance was the best predictor of bopyrid infestation prevalence in modern carid shrimp from Florida (Briggs et  al. 2017). A mid-Cretaceous decapod assemblage from Koskobilo in northern Spain yielded a significant correlation between taxon abundance and percentage of Kanthyloma crusta on the species and genus levels (Klompmaker et al. 2014: Fig. 4A, B). These fossil specimens were collected predominantly from the

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Fig. 5.3  Fossil decapod crustacean carapaces with swellings (ichnotaxon Kanthyloma crusta) attributed to epicaridean isopods in one of the branchial chambers. (a) Galathea valmaranensis from the Oligocene (Rupelian) of Sant’Urbano, Italy (left side), MCV.17/0049. (b) Pithonoton marginatum sensu Wehner (1988: pl. 6.1) (right side), NHMW 1990/0041/1373. (c) Pithonoton cf. P. rusticum (right side), NHMW 2017/0089/0028. (d) Longodromites angustus (right side), NHMW 1990/0041/2600. (e) Cyclothyreus cardiacus (left side), NHMW 2017/0089/0026. (f) Distefania oxythyreiformis (right side), NHMW 2017/0089/0002. (g) Cycloprosopon cf. C. octonarium (left side), NHMW 1990/0041/1455. (h) Ovalopus hoheneggeri (left side), NHMW 1990/0041/1519. (i) Abyssophthalmus spinosus from the Late Jurassic (Kimmeridgian) of the Plettenberg, Germany (right side), MAB k3612. (j) Galatheites cf. G. diasema (right side), NHMW 1990/0041/0163. (k, l) Panopeus nanus from the early Miocene of Jamaica (right side), UF 288470. (c–h, j) From the Late Jurassic (Tithonian) near Ernstbrunn, eastern Austria. All dorsal views, except for (l) (frontal view). Scale bars: 5.0 mm wide

southern wall of the Koskobilo Quarry, minimizing the influence of possible spatial and temporal variation. However, they called for more research because of the limited sample size of specimens of many taxa and the fact that the correlation appears driven by one taxon. To address these issues, the Late Jurassic Ernstbrunn coral-associated assemblage (also called the Bachmayer Collection) from eastern Austria (e.g., Schneider et al. 2013) was used. This decapod collection consists of ~6900 specimens according to the latest counts (pers. comm. A. Kroh to AAK, November 2018). Bachmayer

Table 5.2  All known fossil decapod species with a swelling (ichnotaxon Kanthyloma crusta) in the branchial chamber attributed to epicaridean isopods, arranged by clade, family, and genus and species name Added since Klompmaker et al. (2014: Country of Table 3)? Clade Family Genus and species Age origin Source used for data herein Y Anomura Catillogalatheidae Catillogalathea falcula Late Jurassic Austria Robins et al. (2016: Fig. 11.1), Robins et al., 2016 (Tithonian) Robins and Klompmaker (2019: appendix S2) Anomura Catillogalatheidae Galatheites cf. G. diasema Late Jurassic Austria Robins and Klompmaker (2019: Y Robins et al., 2016 (Tithonian) appendix S2), Fig. 5.3J Anomura Catillogalatheidae G. britmelanarum Robins Late Jurassic Austria Robins and Klompmaker (2019: Fig. Y and Klompmaker, 2019 (Tithonian) 3, appendix S2) Anomura Catillogalatheidae G. "zitteli" (Moericke, 1889) Late Jurassic Austria, Czech Bachmayer (1948: p. 265), Houša N (Tithonian) Republic (1963: Table 1) Late Jurassic Austria, Czech Remeš (1921: Fig. 7), Houša (1963: N Anomura Catillogalatheidae Tuberosagalathea Republic pl. 1.3, as Galathea antiquus), neojurensis (Patrulius, 1959) (Tithonian) Bachmayer (1948: Fig. 3, cf. det. (= Galathea antiquus CMR, 10/2018), Boucot (1990: Fig. Moericke, 1889) 47B, as G. antiquus), Robins and Klompmaker (2019: appendix S2) Spain Klompmaker et al. (2014: Fig. 2A, N Anomura Catillogalatheidae Vasconilia ruizi (Van Early 2G) Straelen, 1940) Cretaceous (Albian) Anomura Galatheidae Acanthogalathea squamosa Eocene Italy Beschin et al. (2015: p. 52) Y Beschin et al., 2007 (Ypresian) Anomura Galatheidae Bolcagalathea corallina Eocene Italy Beschin et al. (2016: p. 31) Y Beschin et al,. 2016 (Ypresian)

128 A. A. Klompmaker et al.

Family Galatheidae

Galatheidae

Galatheidae

Galatheidae

Galatheidae

Galatheidae

Galatheidae

Galatheidae

Munididae

Munididae

Munididae

Clade Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Protomunida primaeva (Segerberg, 1900) P. munidoides (Segerberg, 1900)

Palaeomunida multicristata De Angeli and Garassino, 2002 Juracrista sp.

Lessinigalathea regalis De Angeli and Garassino, 2002

G. valmaranensis De Angeli and Garassino, 2002 G. weinfurteri Bachmayer, 1950

Galathea strigifera von Fischer-Benzo, 1866 G. tuscia Pasini et al., 2020

Late Jurassic (Tithonian) Paleocene (Danian) Paleocene (Danian)

Eocene (Priabonian)

Paleocene (Danian) Pleistocene (GelasianCalabrian) Oligocene (Rupelian) Miocene (LanghianSerravallian) Eocene (Ypresian)

Age Early Cretaceous (Albian) E. navarrensis (Van Straelen, Early 1940) Cretaceous (Albian)

Genus and species Eomunidopsis aldoirarensis Klompmaker et al., 2012a

Denmark

Denmark

Austria

Italy

Italy

Austria, Hungary

Italy

Italy

Denmark

Spain

Country of origin Spain

Klompmaker and Boxshall (2015: Fig. 1D) Jakobsen and Collins (1997: pl. 2.11), Wienberg Rasmussen et al. (2008: pl. 3.3)

pers. obs. CMR (external mold)

Ceccon and De Angeli (2013: pl. 1.2–1.7), Beschin et al. (2017: Table 1) Ceccon and De Angeli (2013: pl. 1.1)

Ceccon and De Angeli (2019: pl. 5.8–5.10), Fig. 5.3A Müller (1984: pl. 22.5), Hyžný et al. (2014: pl. 2.3)

N

Y

Y

N

N

N

Y

Source used for data herein Klompmaker et al. (2012a: Fig. 3D, 3I), Klompmaker et al. (2014: Fig. 2E) Klompmaker et al. (2012a: Fig. 4A), N Klompmaker et al. (2014: Fig. 2C, 2D, 2F, 2H), Klompmaker and Boxshall (2015: Fig. 1E) Klompmaker and Boxshall (2015: Y Fig. 1A) Pasini et al. (2020: pl. 1B, 1C) Y

(continued)

Added since Klompmaker et al. (2014: Table 3)? N 5  Crustaceans as Hosts of Parasites Throughout the Phanerozoic 129

Family Munididae

Munidopsidae

Munidopsidae

Munidopsidae

Munidopsidae

Munidopsidae

Munidopsidae

Munidopsidae

Munidopsidae

Munidopsidae

Clade Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Table 5.2 (continued)

Late Jurassic (Tithonian) Late Jurassic (Tithonian)

Late Jurassic (Tithonian)

Late Jurassic (Tithonian)

Late Jurassic (Tithonian) Late Jurassic (Tithonian)

Age Eocene (Ypresian) Late Jurassic (Tithonian) Late Jurassic (Tithonian)

Late Jurassic Gastrosacus tuberosus (Remeš, 1895) [= G. eminens (Tithonian) (Blaschke, 1911)]

C. prolatus Robins et al., 2013 Culmenformosa glaessneri Robins et al., 2013

C. gracilirostrus Robins et al., 2013

Cracensigillatus acutirostris (Moericke, 1889)

Aulavescus tectus Robins et al., 2013 Bullariscus triquetrus Robins et al., 2013

Genus and species P.? pentaspinosa Beschin et al., 2016 Ambulocapsa altilis Robins et al., 2013 A. sentosa Robins et al., 2013

Austria

Austria

Austria

Austria

Austria

Austria

Austria

Austria

Austria

Country of origin Italy

Robins et al. (2013: Fig. 16.3), Robins and Klompmaker (2019: appendix S2) Robins et al. (2013: Fig. 16.4, 16.15), Robins and Klompmaker (2019: appendix S2)

Source used for data herein Beschin et al. (2016: p. 37), Beschin et al. (2017: Table 1) Robins and Klompmaker (2019: appendix S2) Robins et al. (2013: Fig. 9.8), Robins and Klompmaker (2019: appendix S2) Robins and Klompmaker (2019: appendix S2) Robins et al. (2013: Figs. 12.7, 12.8, 16.1), Robins and Klompmaker (2019: appendix S2) Robins et al. (2013: Fig. 16.2, 16.7–16.13), Robins and Klompmaker (2019: appendix S2) Robins et al. (2013: Fig. 16.14), Robins and Klompmaker (2019: appendix S2) Robins et al. (2013: Fig. 13.4)

N

N

N

N

N

N

Y

N

N

Added since Klompmaker et al. (2014: Table 3)? Y

130 A. A. Klompmaker et al.

Family Munidopsidae

Munidopsidae

Munidopsidae

Munidopsidae

Paragalatheidae

Paragalatheidae

Paragalatheidae

Paragalatheidae

Porcellanidae

Porcellanidae

Clade Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Anomura

Paragalathea verrucosa (Moericke, 1889) Lobipetrolistes blowi De Angeli and Garassino, 2002 Petrolisthes magnus Müller, 1984

Lemacola jenniferae Robins et al., 2016 Mesogalathea striata (Remeš, 1895)

Discutiolira moesica (Moericke, 1889)

Genus and species G.? latirostris Beurlen, 1929 G. torosus Robins et al., 2013 G. tuberosiformus (Lőrenthey in Lőrenthey and Beurlen, 1929) G. wetzleri von Meyer, 1851 (= G. carteri Van Straelen, 1925) Austria

Austria

Country of origin France

Late Jurassic (Tithonian) Eocene (Priabonian) Miocene (LanghianSerravallian)

Late Jurassic (Tithonian) Late Jurassic (Tithonian)

Robins and Klompmaker (2019: appendix S2) Robins et al. (2013: Fig. 16.5, 16.6), Robins and Klompmaker (2019: appendix S2) Quenstedt (1856–1858: pl. 95.47), Wienberg Rasmussen et al. (2008: pl. 3.11), Fraaije (2014: Fig. 3A)

Source used for data herein Beurlen (1929: Fig. 6)

Robins et al. (2016: Fig. 7.12, 7.13), Robins and Klompmaker (2019: appendix S2) Austria Robins and Klompmaker (2019: appendix S2) Austria, Czech Remeš (1921: p. 37), Houša (1963: Republic pl. 1.2), Glaessner (1969: Fig. 242.2), Boucot (1990: Fig. 47A), Robins and Klompmaker (2019: appendix S2) Czech Republic Blaschke (1911: p. 149), Houša (1963: pl. 2.1, 2.2) Italy Ceccon and De Angeli (2013: pl. 1.8) Hungary Müller (1984: pl. 23.4), Hyžny and Dulai (2021: Fig. 45.4)

Czech Late Jurassic (Kimmeridgian, Republic, France, Tithonian) Germany Late Jurassic Austria (Tithonian)

Age Late Jurassic (Oxfordian) Late Jurassic (Tithonian) Late Jurassic (Tithonian)

N

N

N

N

Y

Y

N

N

Y

(continued)

Added since Klompmaker et al. (2014: Table 3)? N 5  Crustaceans as Hosts of Parasites Throughout the Phanerozoic 131

Family Porcellanidae

Aethridae

Dromiidae

Dynomenidae

Dynomenidae

Dynomenidae

Dynomenidae

Dynomenidae

Dynomenidae

Clade Anomura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Table 5.2 (continued)

Genus and species Age Pisidia kokayi (Müller, 1984) Miocene (LanghianSerravallian) Miocene Hepatus lineatinus Collins (Serravallianand Todd in Todd and Tortonian) Collins, 2005 Kromtitis cf. K. koberiformis Eocene Beschin et al., 2007 (Priabonian) Cyamocarcinus angustifrons Eocene Bittner, 1883 (Ypresian) Late Jurassic Cyclothyreus cardiacus (Tithonian) Schweitzer and Feldmann, 2009a C. divaricatus Schweitzer Late Jurassic and Feldmann, 2009a (Tithonian) C. latus (Moericke, 1889) Late Jurassic (Tithonian) Late Jurassic C. quadrophthalmus (Tithonian) Schweitzer and Feldmann, 2009a C. "reussi" (Gemmellaro, Late Jurassic 1869) (Tithonian) N

N Czech Republic Bachmayer (1948: Fig. 4 = Cycloprosopon sp. det. AAK 09/2018, NHMW 1990/0041/10161), Houša (1963: Table 1)

Schweitzer and Feldmann (2009a: Fig. 4.3), pers. obs. AAK

Austria

N

Y

N

N

N

N

Todd and Collins (2005: pl. 2.10), Wienberg Rasmussen et al. (2008: pl. 3.2) Ceccon and De Angeli (2013: pl. 1.9) Ceccon and De Angeli (2013: pl. 1.10), Beschin et al. (2017: Table 1) Fig. 5.3E

Source used for data herein Müller (1984: pl. 27.5), Hyžny and Dulai (2021: Fig. 46.2)

Schweitzer and Feldmann (2009a: Fig. 3.1), pers. obs. AAK Czech Republic Förster (1969: p. 53)

Austria

Austria

Italy

Italy

Panama

Country of origin Hungary

Added since Klompmaker et al. (2014: Table 3)? N

132 A. A. Klompmaker et al.

Family Dynomenidae

Dynomenidae

Dynomenidae

Dynomenidae

Dynomenidae

Feldmanniidae

Feldmanniidae

Goniodromitidae

Goniodromitidae

Goniodromitidae

Goniodromitidae

Clade Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Age Late Jurassic (Tithonian) Late Jurassic (Tithonian) Late Jurassic (Tithonian)

Oligocene (Rupelian) Early Cretaceous (Albian) Caloxanthus paraornatus Early Klompmaker et al., 2011 Cretaceous (Albian) Feldmannia wintoni Early (Rathbun, 1935) Cretaceous (Albian) Late Jurassic Cycloprosopon complanatiforme (Moericke, (Tithonian) 1889) C. conspicuum Schweitzer Late Jurassic and Feldmann, 2010 (Tithonian) Late Jurassic C. octonarium Schweitzer and Feldmann, 2010 (Tithonian) Distefania renefraaijei Early Klompmaker et al., 2012b Cretaceous (Albian)

Dynomene lessinea Beschin et al., 2001 Graptocarcinus texanus Roemer, 1887

Genus and species C. strambergensis Remeš, 1895 C. strangus Schweitzer and Feldmann, 2009a C. tithonius (Gemmellaro, 1869)

Remeš (1921: p. 37), pers. obs. AAK N (both countries)

Austria, Czech Republic

Spain

Schweitzer and Feldmann (2010: Fig. 4.4), Fig. 5.3G Klompmaker et al. (2012b: Fig. 4A, 4G), Klompmaker et al. (2014: Fig. 3E, 3F)

Schweitzer-Hopkins et al. (1999: Fig. 3.6)

USA (Texas)

Austria

Klompmaker et al. (2014: Fig. 3G–I) N

Spain

pers. obs. AAK

N

Klompmaker et al. (2014: Fig. 3C, 3D)

Spain

Austria

Y

N

N

Y

N

N

Y

Country of origin Source used for data herein Czech Republic Remeš (1921: p. 37), Houša (1963: Table 1) Czech Republic Schweitzer and Feldmann (2009a: Fig. 5.4) Italy Gemmellaro (1869: pl. 7.55), Schweitzer and Feldmann (2009a: Fig. 1.5) Italy Ceccon and De Angeli (2019: p. 52)

(continued)

Added since Klompmaker et al. (2014: Table 3)? N 5  Crustaceans as Hosts of Parasites Throughout the Phanerozoic 133

Family Goniodromitidae

Goniodromitidae

Goniodromitidae

Goniodromitidae

Goniodromitidae

Goniodromitidae

Goniodromitidae

Clade Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Table 5.2 (continued)

G. polyodon Reuss, 1858 (=G. complanatus Reuss, 1858)

G. laevis (Van Straelen, 1940)

G. globosa (Remeš, 1895)

E. rostratus (von Meyer, 1840) Goniodromites bidentatus Reuss, 1858

Genus and species D. oxythyreiformis (Gemmellaro, 1869) Eodromites grandis (von Meyer, 1857)

Late Jurassic (Tithonian)

Late Jurassic (Tithonian) Early Cretaceous (Albian)

Late Jurassic (Oxfordian) Late Jurassic (Tithonian)

Age Late Jurassic (Tithonian) Late Jurassic (Tithonian)

N

N

Klompmaker et al. (2014: Fig. 3M), http://www.mbfossilcrabs.com/ Dromioidea.html (Accessed 10/28/18) Czech Republic Remeš (1921: p. 37)

Spain

N

N

N

N

Source used for data herein Remeš (1921: p. 37), Houša (1963: Table 1), Fig. 5.3F Schweitzer and Feldmann (2008: pl. 4A–C), Schweitzer and Feldmann (2010: Fig. 5.1), Klompmaker and Boxshall (2015: Fig. 1F), pers. obs. AAK Radwański (1972: pl. 1.2)

Remeš (1921: Fig. 5), Houša (1963: pl. 2.3), Boucot (1990: Fig. 47C), Klompmaker and Boxshall (2015: Fig. 1B, as G. ?dentatus), pers. obs. AAK (Austria) Czech Republic Houša (1963: Table 1)

Austria, Czech Republic

Poland

Country of origin Austria, Czech Republic Austria

Added since Klompmaker et al. (2014: Table 3)? N

134 A. A. Klompmaker et al.

Family Goniodromitidae

Goniodromitidae

Goniodromitidae

Goniodromitidae

Goniodromitidae

Goniodromitidae

Hexapodidae

Hexapodidae

Clade Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Age Late Jurassic (Oxfordian, Kimmeridgian)

Holthuisea cesarii (Beschin et al., 1994)

Palaeopinnixa rathbunae Schweitzer et al., 2000

P. cf. P. rusticum Patrulius, 1966 Sabellidromites scarabaea (Wright and Wright, 1950)

Pithonoton "marginatum" von Meyer, 1842 (sensu Wehner 1988: pl. 6.1)

Austria, Czech Republic

France

Mexico

Country of origin Czech Republic, Germany, Poland

Late Jurassic Austria (Tithonian) England Early Cretaceous (Albian) Eocene (middle) USA (Washington state) Eocene Italy (Ypresian)

Late Jurassic (Tithonian)

Early Cretaceous (Barremian) Palaeodromites octodentatus Early A. Milne Edwards, 1865 Cretaceous (Hauterivian)

Goniodromites sp. (non G. laevis)

Genus and species G. serratus Beurlen, 1929

Y

Y

Schweitzer et al. (2000: p. 62)

Beschin et al. (2009: p. 76)

N

Schweitzer and Feldmann (2008: pl. 5A)

Van Straelen (1928: p. 51, as Xantho N agassizi Robineau-Desvoidy, 1849), Van Straelen (1931: p. 56), Wienberg Rasmussen et al. (2008: pl. 5) Remeš (1921: Fig. 6), Houša (1963: N pl. 1.4), Bachmayer (1964: Fig. 131), Glaessner (1969: Fig. 242.1), Fig. 5.3B Fig. 5.3C Y

Source used for data herein Radwański (1972: pls 1.1, 1.4, 2, as Pithonoton marginatum), Boucot (1990: Figs. 47D, 48B, as P. marginatum), Conway Morris (1990: p. 377, as P. marginatum), Radwańska and Radwański (2004: Fig. 1B, 1D, 1E), Hyžný et al. (2015: Fig. 4A, 4B, 4G), Schweigert et al. (2016: p. 64), Schweigert and Kuschel (2018: Fig. 23A) Vega et al. (2019: Fig. 4.18, as G. Y laevis)

(continued)

Added since Klompmaker et al. (2014: Table 3)? Y 5  Crustaceans as Hosts of Parasites Throughout the Phanerozoic 135

Family Homolidae

Homolodromiidae

Ibericancridae

Jurellanidae

Leucosiidae

Leucosiidae

Longodromitidae

Longodromitidae

Longodromitidae

Clade Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Table 5.2 (continued)

A. spinosus (von Meyer, 1842) Longodromites excisus (von Meyer, 1857)

Abyssophthalmus mirus (Moericke, 1889)

P. syndactyla Ortmann, 1892

Tropidicarcinus starnesi Schweitzer et al., 2019 Ovalopus hoheneggeri (Moericke, 1889) Philyra granulosa Morris and Collins, 1991

Notiodromia australis (Feldmann et al., 1993)

Genus and species Latheticocarcinus atlanticus (Roberts, 1962)

Japan

Brunei

USA (Mississippi) Austria

Late Jurassic (Oxfordian) Late Jurassic (Oxfordian, Tithonian)

Czech Republic, Germany

Germany

Late Jurassic Germany (Kimmeridgian)

Pleistocene (middle)

Late Cretaceous (Maastrichtian) Late Jurassic (Tithonian) Miocene (-)

Late Cretaceous Antarctica (Campanian)

Country of Age origin Late Cretaceous USA (Campanian) (Delaware)

Houša (1963: pl. 1.1, as L. ovalis), Wehner (1988: pl. 7.7), Müller et al. (2000: Fig. 18G)

Morris and Collins (1991: Fig. 37), Wienberg Rasmussen et al. (2008: pl. 3.9) Kobayashi et al. (2008: pl. 1.4), Wienberg Rasmussen et al. (2008: pl. 3.10), Karasawa et al. (2021: pl. 4.6–4.8) Wehner (1988: pl. 4.3), Müller et al. (2000: Fig. 17I), Schweitzer and Feldmann (2009b: Fig. 8.4) Förster (1969: pl. 2.2), Fig. 5.3I

Fig. 5.3H

N

N

N

N

N

Y

Source used for data herein Bishop (1983a: Fig. 4B), Bishop (1986: Fig. 8M), Wienberg Rasmussen et al. (2008: pl. 3.1) N Feldmann et al. (1993: Fig. 27.3), Feldmann (2003: Fig. 1.5), Wienberg Rasmussen et al. (2008: pl. 3.4) Schweitzer et al. (2019: Fig. 21) Y

Added since Klompmaker et al. (2014: Table 3)? N

136 A. A. Klompmaker et al.

Family Longodromitidae

Longodromitidae

Longodromitidae

Longodromitidae

Longodromitidae

Lyreididae

Lyreididae

Lyreididae

Lyreididae

Lyreididae

Clade Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Age Late Jurassic (Kimmeridgian, Tithonian) Late Jurassic (Kimmeridgian)

Country of origin Austria, Germany

Macroacaena succedana (Collins and Wienberg Rasmussen, 1992)

Macroacaena rosenkrantzi (Collins and Wienberg Rasmussen, 1992)

Hemioon cunningtoni Bell, 1863

P. aff. P. hystricosus Schweitzer and Feldmann, 2009b Bournelyreidus eysunesensis (Collins and Wienberg Rasmussen, 1992) B. oaheensis (Bishop, 1978)

Austria

Greenland

USA (South Dakota) England

Late Cretaceous Greenland (CampanianMaastrichtian)

Late Cretaceous (Campanian) Early Cretaceous (Albian) Late Cretaceous (Maastrichtian)

Late Cretaceous Greenland (Campanian)

Late Jurassic (Tithonian)

Germany Pilidromia thiedeae (Schweigert and Koppka, 2011) Planoprosopon dumosum Late Jurassic Germany (Wehner, 1988) (Kimmeridgian) P. heydeni (von Meyer, 1857) Late Jurassic Poland (Oxfordian)

Genus and species L. angustus (Reuss, 1858)

Y

Karasawa et al. (2014: Fig. 14D, 14E)

N Collins and Wienberg Rasmussen (1992: Fig. 15A), Wienberg Rasmussen et al. (2008: pl. 3.5–3.7), De Grave et al. (2009: Fig. 2E) Collins and Wienberg Rasmussen N (1992: p. 24)

Y

Y

Y

N

Y

Y

pers. obs. AAK

Collins and Wienberg Rasmussen (1992: Fig. 10C)

Radwański (1972: pl. 1.3), Boucot (1990: Fig. 48A), Radwańska and Radwański (2004: Fig. 1C) Klompmaker et al. (2020: Fig. 9C, 9E)

Schweigert et al. (2016: p. 64), Schweigert and Kuschel (2018: Fig. 23B), pers. obs. AAK Schweigert et al. (2016: p. 64)

Source used for data herein Schweigert and Kuschel (2018: Fig. 23C), Fig. 5.3D

(continued)

Added since Klompmaker et al. (2014: Table 3)? Y 5  Crustaceans as Hosts of Parasites Throughout the Phanerozoic 137

Family Nodoprosopidae

Nodoprosopidae

Konidromitidae

?Macropipidae

Necrocarcinidae

Orithopsidae

Palaeocorystidae

Palaeocorystidae

Palaeocorystidae

Clade Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Table 5.2 (continued)

Genus and species Nodoprosopon? katholickyi (Remeš, 1895) N. ornatum (von Meyer, 1857) Konidromites gibbus (Reuss, 1858) Faksecarcinus (cf. F.) koskobiloensis (Klompmaker et al., 2011) Necrocarcinus labeschii (Eudes-Deslongchamps, 1835) Bellcarcinus aptiensis Luque, 2014 Cretacoranina testacea (Rathbun, 1926) Joeranina platys (Schweitzer and Feldmann, 2001) Notopocorystes stokesii (Mantell, 1844) (=N. mantelli M'Coy, 1854)

Age Late Jurassic (Tithonian) Late Jurassic (Kimmeridgian) Late Jurassic (Tithonian) Early Cretaceous (Albian) Early Cretaceous (Albian) Early Cretaceous (Aptian) Late Cretaceous (Maastrichtian) Late Cretaceous (Santonian) Early Cretaceous (Albian) Carter (1898, p. 28, as N. bechei), Wienberg Rasmussen et al. (2008: pl. 4) Luque et al. (2020: Fig. 4)

England

USA (Mississippi) Canada (British Columbia) England, France

Y

N

N

Y

N

M'Coy (1854: p. 118), Bell (1863: pl. 3.3), Förster (1969: pl. 3.6, 3.7), Boucot (1990: Fig. 49), Conway Morris (1990: p. 377), Littlewood and Donovan (2003: Fig. D), Wienberg Rasmussen et al. (2008: pl. 1.1–1.8), Breton (2010: Fig. 4A), Van Bakel et al. (2012: Fig. 13A–C)

N

Wienberg Rasmussen et al. (2008: p. N 36), Kornecki et al. (2017: Fig. 15B) Schweitzer et al. (2009: Fig. 7D) N

Klompmaker et al. (2014: Fig. 3J, 3K)

Spain

Colombia

pers. obs. AAK

Wehner (1988: pl. 3.5)

Austria

Germany

Country of origin Source used for data herein Czech Republic Remeš (1921: p. 37)

Added since Klompmaker et al. (2014: Table 3)? N

138 A. A. Klompmaker et al.

Pilumnidae

Portunidae

Portunidae

Prosopidae

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Panopeidae

Brachyura

Portunus woodwardi Morris and Collins, 1991

Charybdis sp.

Galenopsis similis Bittner, 1875

Panopeus nanus Portell and Collins, 2004

Genus and species N. serotinus Wright and Collins, 1972

Miocene (-)

Pliocene (?Zanclean)

Age Early Cretaceous (Albian) Miocene (AquitanianBurdigalian) Eocene (Ypresian)

Acareprosopon bouvieri (Van Early Straelen, 1944) Cretaceous (Albian) Prosopidae Prosopon aculeatum von Late Jurassic Meyer, 1857 (Kimmeridgian) Miocene Pseudorhombilidae Speocarcinus berglundi Tucker et al., 1994 (Tortonian) Raninidae Cristafrons praescientis Late Cretaceous Feldmann et al., 1993 (SantonianMaastrichtian) Raninidae Lophoranina marestiana Eocene (König, 1825) (Lutetian)

Family Palaeocorystidae

Clade Brachyura

Ceccon and De Angeli (2013: pl. 2.1)

N

N

Feldmann et al. (1993: Fig. 25.5)

Italy

Y

Tucker et al. (1994: Fig. 2.1, 2.2)

USA (California) Antarctica

N

N

N

N

N

Y

von Meyer (1860: pl. 23.24)

Ceccon and De Angeli (2013: pls 1.11, 2.2, 2.3), Beschin et al. (2017: Table 1) Karasawa and Nobuhara (2008: Fig. 2.5), Wienberg Rasmussen et al. (2008: pl. 3.12) Morris and Collins (1991: Fig. 47), Collins et al. (2003: pl. 5.1), Wienberg Rasmussen et al. (2008: pl. 3.13) Klompmaker et al. (2014: Fig. 3A, 3B)

Fig. 5.3K, 5.3L

Source used for data herein Wienberg Rasmussen et al. (2008: pls 1.9–1.18, 2)

Germany

Spain

Brunei

Japan

Italy

Jamaica

Country of origin England

(continued)

Added since Klompmaker et al. (2014: Table 3)? N 5  Crustaceans as Hosts of Parasites Throughout the Phanerozoic 139

Family Raninidae

Raninidae

Tanidromitidae

Tanidromitidae

Torynommidae

Torynommidae

Varunidae

Viaiidae

Nephropidae

Nephropidae

Clade Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Brachyura

Astacidea

Astacidea

Table 5.2 (continued)

H. gammaroides Bell, 1858

Hoploparia dentata (Roemer, 1841)

Asthenognathus cornishorum Schweitzer and Feldmann, 1999 Viaia robusta Artal et al., 2012

Genus and species Notosceles bournei Rathbun, 1928 Quasilaeviranina ovalis (Rathbun, 1935) Tanidromites insignis (von Meyer, 1857) Tanidromites sp. (non T. insignis) Torynomma flemingi Glaessner, 1980 Withersella crepitans Wright and Collins, 1972

Early Cretaceous (Albian) Early Cretaceous (Hauterivian) Eocene (Ypresian)

Oligocene (Chattian)

Age Paleocene (Danian) Paleocene (Danian) Late Jurassic (Kimmeridgian) Late Jurassic (Oxfordian) Late Cretaceous (Maastrichtian) Early Cretaceous (Aptian)

Source used for data herein Rathbun (1928: pl. 1.1–1.3)

England

England

Woods (1925–1931: p. 29), Wienberg Rasmussen et al. (2008: pl. 3.15) Wienberg Rasmussen et al. (2008: pl. 3.16)

Artal et al. (2012: Fig. 1.1, 1.4), Klompmaker et al. (2014: Fig. 3L)

Wright (1997: Fig. 12), Wienberg Rasmussen et al. (2008: pl. 3.8), Schweitzer and Feldmann (2011: Fig. 7) Schweitzer and Feldmann (1999: Fig. 14A, 14C)

England

USA (Washington state) Spain

Feldmann (1993: Fig. 11)

Schweigert and Koppka (2011: Fig. 6E) pers. obs. AAK

New Zealand

Poland

Germany

USA (Alabama) Rathbun (1935: pl. 18.6)

Country of origin USA (Texas)

N

N

N

Y

N

N

Y

N

N

Added since Klompmaker et al. (2014: Table 3)? N

140 A. A. Klompmaker et al.

Erymidae

Glypheidea

"Eryma sp."

Country of Genus and species Age origin H. trigeri A. Milne-Edwards, Late Cretaceous France 1886 (Cenomanian) Source used for data herein Breton and Collins (2007: p. 17), Wienberg Rasmussen et al. (2008: pl. 3.17) Soergel (1913: pl. 24.9), Wienberg Rasmussen et al. (2008: pl. 3.14) Bell (1863: pl. 11.10), Wienberg Rasmussen et al. (2008: p. 37)

Early Jurassic Indonesia N (Toarcian) England N Glypheidea Erymidae Palaeastacus? scaber (Bell, Early 1863) Cretaceous (Albian) N Collins and Wienberg Rasmussen Glypheidea Mecochiridae Mecochirus rostratus Collins Late Cretaceous Greenland (Maastrichtian) (1992: Fig. 15A), Wienberg and Wienberg Rasmussen, Rasmussen et al. (2008: pl. 3.18) 1992 Spain pers. obs. AAK Y Glypheidea Mecochiridae Atherfieldastacus magnus Early (M'Coy, 1849) Cretaceous (Barremian) USA (Texas) Franţescu (2014: Fig. 2C) N Early Axiidea Axiidae Axiopsis sampsunumae Franţescu, 2014 Cretaceous (Albian) Bachmayer (1948: Figs. 1, 2) figured specimens containing K. crusta identified as Galatheites meyeri (Moericke, 1889), but these specimens are not G. meyeri and cannot be identified to the species level with confidence. Van Straelen (1928: p. 51) for Eucorystes carteri (M’Coy, 1854) and Boucot and Poinar (2010, Table 2B, for Branchioplax washingtoniana Rathbun, 1916) claimed additional occurrences, which we have not been able to confirm

Family Nephropidae

Clade Astacidea

Added since Klompmaker et al. (2014: Table 3)? N 5  Crustaceans as Hosts of Parasites Throughout the Phanerozoic 141

142

2014 paper

40 30 20 10

Ea

M

rly J id ura dl ss e ic J La ura s Ea te J sic u rly r C as La ret sic ac te e C re ous ta ce Pa ou s le oc en Eo e c O ene lig oc e M ne io ce Pl ne io Pl cen ei H e s ol oc toc en en e e (fo ss il)

0

Number of infested decapod species per 20 my

Added since 2014

B 60 50 40

Clade Brachyura Astacidea Glypheidea Anomura Axiidea

30 20 10 0

rly J id ura dl ss e ic J La ura s t Ea e J sic ur rly C as La ret sic ac te e C re ous ta ce Pa ou s le oc en e Eo c O ene lig oc e M ne io ce Pl ne io Pl cen ei H e s ol oc toc en en e e (fo ss il)

50

Data

Ea

Number of infested decapod species

60

M

A

A. A. Klompmaker et al.

Fig. 5.4  The global number of fossil decapod crustacean species parasitized by epicaridean isopods. (a) Raw epoch-level data split before and after Klompmaker et  al. (2014: Table  3), total n = 128. Research since 2014 has led to an increase of 47% in the number of infested decapod species. (b) Data per clade and normalized per 20 my per epoch. For full data, see Table 5.2

(1945) listed four localities in the Ernstbrunn Limestone in which decapods were found (Dörfles I, Dörfles Werk II, Klafterbrunn I, and Klement I), but decapods were only abundant in Dörfles I and rare in the other three localities. The Dörfles exposures are considered to be middle to late Tithonian in age based on ammonite stratigraphy (Zeiss and Bachmayer 1989; Zeiss 2001; Schweitzer and Feldmann 2009b). All specimens of this collection were identified to the genus and family levels, where possible. Species-level assignments were not consistently possible for all taxa because not all brachyuran species have been studied in detail. As in Klompmaker et al. (2014), both branchial sides needed to be preserved to confirm that specimens were not infested, whereas this was not a requirement for specimens containing Kanthyloma crusta. Our results show that there is no significant relationship between taxon abundance and infestation percentage on both the genus and family levels (Fig.  5.5). Similar results apply when genus-level data is split into Anomura (n  =  6; r  =  −0.28, two-tailed t-test p  =  0.59) and Brachyura (n  =  10; r = −0.16, two-tailed t-test p = 0.67). Sample size is not adequate for such analyses on the family level. Decapods from the Ernstbrunn Limestone assemblage were, however, not all collected at the same location or stratigraphic level (Bachmayer 1945). The precise locality and stratigraphic position are not known for all Ernstbrunn specimens. In situ-collected assemblages from a single bed and small spatial scale with a relatively high proportion of parasitized specimens would be needed to further test the relationship between abundance and prevalence. Brachyurans and galatheoids from the Tithonian Štramberk Limestone in the active Kotouč Quarry (Czech Republic, Fraaije et al. 2013) may be most suitable because decapods from this limestone are occasionally infested (Houša 1963; pers. obs. AAK, CMR). Due to the generally low prevalence of epicarideans within large, diverse decapod assemblages today (Williams and Boyko 2012, and references therein), modern assemblages may not be suitable for this purpose.

5  Crustaceans as Hosts of Parasites Throughout the Phanerozoic A

B 25 % specimens of family with parasite

50 % specimens of genus with parasite

143

40

30

20

10

0

20

15

10

5

0 0

100

200 Specimens

300

400

0

250

500 Specimens

750

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Fig. 5.5  The percentage of parasitized specimens per taxon versus taxon abundance for decapods from the Ernstbrunn Limestone assemblage (Late Jurassic, Tithonian, Austria). (a) Genera, n = 16; r  =  −0.25, two-tailed t-test p  =  0.35. (b) Families, n  =  9; r  =  0.009, two-tailed t-test p  =  0.98. Minimum number of specimens per taxon = 30. Data: Appendix 1

5.2.4  Host Preference Host preference is likely to result in nonrandom patterns of parasite prevalence. Some generalizations have been made concerning epicaridean parasites: Markham (1986) mentioned that host-species specificity appears to be rare among Bopyroidea; McDermott (1991) remarked that most branchial bopyrids infest particular crab families; and Boyko and Williams (2009) noted that some bopyrids infested multiple paguroid hosts, whereas others have been found only on one species thus far. Data in systematic studies on epicarideans echo variability in host specificity: An et al. (2009: Table 1) showed that most Progebiophilus spp. were restricted to one thalassinidean host species and both An et al. (2015) and Boyko et al. (2017) noted epicaridean species infesting only a single host species, whereas other epicaridean species were found on multiple, often related host species. For carid shrimp from Florida, each bopyrid species was found only on one host genus (Briggs et al. 2017). The fact that multiple species from the same genus or family can be infested by the same parasite species does not imply a lack of preference because parasitized hosts can have very different infestation percentages (e.g., Owens and Glazebrook 1985; González and Acuña 2004; Brockerhoff 2004). Host specificity of individual parasite species is impossible to address in deep time because epicarideans tend not to preserve as fossils due to their low preservation potential (Klompmaker et  al. 2017; Fig.  2), but it is possible to assess host preferences for all swellings attributed to epicarideans combined. Very little is known thus far. From the Late Cretaceous (Campanian-Maastrichtian) of Greenland, species-level infestation percentages have been reported from a lobster-brachyuran assemblage preserved in siliciclastic rocks, primarily in shales (Collins and Wienberg Rasmussen 1992; Wienberg Rasmussen et al. 2008). The raninoid crab

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species Macroacaena rosenkrantzi was infested more frequently than the congeneric M. succedana (73/1295 = 5.6% vs. a few out of 193 = 6.26 1990/0041/2089 C 5.75 1990/0041/2803 G 6.92 1990/0041/2892 G 6.8 7.1 1990/0041/5036 G 7.2 1990/0041/4108 G 7.35 7.55 1990/0041/4158 G 8.02 1990/0041/5112 G 8.09 1990/0041/2944 G 8.2 1990/0041/4342 G 8.25 1990/0041/5040 G 8.34 8.32 1990/0041/4167 G 8.2 8.4 1990/0041/3114 G 8.6 8.48 1990/0041/2954 G 8.3 8.66 1990/0041/2817 G 8.14 8.67 1990/0041/5156 G 8.7 1990/0041/5117 G 9.6 9.3 1990/0041/4325 G 9.53 9.6 1990/0041/2848 G 9.73 1990/0041/2901 G 9.75 9.74 1990/0041/3085 G 9.77 1990/0041/4231 G 11.3 9.8 1990/0041/2604 G 9.7 9.98 1990/0041/5038 G 10 1990/0041/3208 G 10.35 10.04 1990/0041/4177 G 10.14 1990/0041/2898 G 10.15 1990/0041/2920 G 10.28

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Geometric mean l and w 4.66 4.64 5.77 6.21 6.26 6.60 6.76 7.07

Left (L) or right (R) if infested (Kanthyloma) R R L L R L L R R L R R R

6.95 7.45

8.33 8.30 8.54 8.48 8.40 9.45 9.56 9.74 10.52 9.84 10.19

(continued)

5  Crustaceans as Hosts of Parasites Throughout the Phanerozoic

NHMW # 1990/0041/4201 1990/0041/2974 1990/0041/4257 1990/0041/2582 1990/0041/2935 1990/0041/2589 1990/0041/4133 1990/0041/4329 1990/0041/4324 1990/0041/5113 1990/0041/5070 1990/0041/2607 1990/0041/2934 1990/0041/5119 1990/0041/2820 1990/0041/5116 1990/0041/2559 1990/0041/5031 1990/0041/2950 1990/0041/5115 1990/0041/4188 1990/0041/2739 1990/0041/2990 1990/0041/2595 1990/0041/2754 1990/0041/2743 1990/0041/4200 1990/0041/4347 1990/0041/1372 1990/0041/0394 1990/0041/3240 1990/0041/3365 2017/0089/0025 2017/0089/0012 1990/0041/4101 1990/0041/3551 1990/0041/2427 2014/0194/0965 1990/0041/1344 2014/0194/1000

Maximum width (mm) [without Length extra width (mm) Taxon [Cracensigillatus anterior part due to Kanthyloma, acutirostris (C) or epigastricif posterior Goniodromites applicable] margin bidentatus (G)] G 10.3 G 10.93 G 11.46 10.97 G 10.99 G 11.2 G 12.44 11.44 G 11.46 G 13.08 11.6 G 11.75 G 11.85 11.8 G 12.16 G 12.2 G 11.8 12.5 G 11.85 12.5 G 13.14 G 13.14 13.2 G 13.22 G 13.4 G 13.5 G 13.7 13.8 G 14.64 G 14.8 14.8 G 14.33 15.05 G 5.44 G 9.7 G 7.24 G 6.46 G 12.05 G 6.95 6.95 G 8.8 8.4 G 8.8 8.7 G 11.4 10.4 G 11.4 G 11.5 11.8 G 12 11.9 G 12.2 G 12.4 12.3 G 13.5 12.4 G 12.7 12.7 G 12.9 12.8

159

Geometric mean l and w

Left (L) or right (R) if infested (Kanthyloma)

11.21

11.93 12.32 11.82

12.14 12.17 13.17

13.75 14.80 14.69

6.95 8.60 8.75 10.89 11.65 11.95 12.35 12.94 12.70 12.85

R R L R L L R L R R R R

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Chapter 6

Trilobites as Hosts for Parasites: From Paleopathologies to Etiologies Kenneth De Baets, Petr Budil, Oldřich Fatka, and Gerd Geyer

Abstract  Extant marine arthropods are afflicted by a variety of parasitic diseases making it plausible that extinct trilobites also had a variety of parasites. Direct evidence in the form of preserved parasite body fossils is lacking to date, which is not surprising considering the poor preservation potential of soft tissues of parasites and their hosts. Some of these interactions might leave traces and pathologies in their exoskeletons, which can be traced in deep time. Knowledge of the parasitic causes of pathologies in modern arthropods such as crustaceans and horseshoe crabs might, therefore, help to better interpret past afflictions and their potential culprits. Our review shows that a variety of structures have been attributed to parasitism—some more confidently than others. The restriction of these structures to particular trilobite lineages might indicate the influence of phylogeny, anatomy, and potential role of ecology (feeding, mode of life) on infestation risks. However, preservation and research biases might also contribute to differences between time intervals and individual trilobite lineages. Other interactions such as epizoa, bioerosion, as well as other structures, which have been confused with parasitic causes are briefly discussed. The culprits of many of these structures remain elusive.

K. De Baets (*) Geozentrum Nordbayern, Friedrich-Alexander University Erlangen-Nürnberg, Erlangen, Germany e-mail: [email protected] P. Budil Czech Geological Survey, Prague 1, Czech Republic e-mail: [email protected] O. Fatka Charles University, Faculty of Sciences, Institute of Geology and Palaeontology, Prague 2, Czech Republic e-mail: [email protected] G. Geyer Institut für Geographie und Geologie, Lehrstuhl für Geodynamik und Geomaterialforschung, Bayerische Julius-Maximilians-Universität Würzburg, Würzburg, Germany e-mail: [email protected] © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 K. De Baets, J. W. Huntley (eds.), The Evolution and Fossil Record of Parasitism, Topics in Geobiology 50, https://doi.org/10.1007/978-3-030-52233-9_6

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Keywords  Paleopathology · Borings · Neoplasia · Shell disease syndrome · Parasitic infestations · Helminths · Bacteria

6.1  Introduction Trilobites constitute a highly diverse group of Paleozoic arthropods. They are some of the earliest known arthropods appearing in the early Cambrian, where they provisionally indicate the base of the Cambrian Series 2 and Stage 3 (e.g., Jell 2003; Hollingsworth 2011; Yuan et  al. 2011; Bushuev et  al. 2014; Geyer 2019). They reach two peak diversities in the late Cambrian and the middle to late Ordovician (e.g., Sepkoski Jr et al. 1981; Adrain et al. 2004) with a subsequent decline until their extinction in the late Permian. This general decline is interrupted by two phases of rapid diversification during the Ordovician and the early to middle Devonian (Bell 2013). Considering their diversity and variety of lifestyles ranging from burrowing to swimming (Fortey 2014), they had ample opportunity to come in contact with a variety of parasites. Unfortunately, no direct body fossil evidence of parasites in trilobites is available, which could be related to a variety of factors including position within or on the host, small size, and/or lack of readily fossilizable hard parts (e.g., Littlewood and Donovan 2003; De Baets and Littlewood 2015; De Baets et al. 2021). However, a variety of abnormalities have been attributed to disease or parasitism so-called (paleo)pathologies (compare De Baets et al. 2021b). Other types of abnormalities in trilobites related to developmental malfunction and injury have been reviewed on a variety of occasions (Owen 1985; Babcock 2003b, 2007). We focus on (paleo)pathologies where parasites could have been the source or have at least been implicated. We herein use a quite broad definition of parasitism as a symbiotic association whereby an individual derives nutritional benefit (or is otherwise metabolically dependent) at the detrimental expense of another (causes damage to its host), by means of a long-term association (compare Conway-Morris 1990; Tapanila 2008; Robin 2021). Parasitism has been particularly implicated in exoskeletal swellings, pits and lesions in the exoskeleton, some types of borings, and possibly other types of pathologies in trilobites (Conway-Morris 1981; Owen 1985; Geyer 1990; Babcock 2007) with various degrees of certainty. For comparative purposes, we also discuss traces attributed to epicoles/epizoa and how they can be differentiated from parasitic infestations during life. Molting in trilobites (e.g., Šnajdr 1990; Brandt 1996) and other marine arthropods (e.g., Messick 1998) might have helped to get rid of epizoans or epiphytes during life as at least some taxa are preferentially encrusted during late ontogeny. The relatively low prevalence of epibionts on most carapaces or gills between molds might suggest that modern decapods have effective antifouling mechanisms (Messick 1998; Becker 1996). Other marine arthropods like pycnogonids that stop molting after reaching adulthood even developed a way to peel parts of their exoskeleton to get rid of attached epizoans and epiphytes and to counter ablation (Meyer and Büchmann 1963; Lotz and

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Büchmann 1968). If trilobites had a similar antifouling strategy, it is yet to be determined. It is, therefore, reasonable to assume that the life cycle of parasites attached to the exoskeleton was somehow limited to between molting phases (Šnajdr 1990). It is rather unlikely that the ectoparasite attached to the animal immediately after the molt so that the exoskeleton has grown over it and been deformed (Jell 1989). We review comparable traces both for agnostids and “normal” polymerid trilobites, although their close relationship is still debated (e.g., Müller 1987; Walossek and Müller 1988, 1990; Cotton and Fortey 2005; Moysiuk and Caron 2019; see Babcock et al. 2017 for a recent review). Nevertheless, both Agnostida and (restricted) Trilobita are traditionally assigned to the trilobites and are treated herein together. Interestingly, agnostids have historically been described as parasitic themselves—mainly due to their small size and possibly well-developed digestive glands (McCoy 1849; Bergström 1973), but no sound evidence has so far been found for this hypothesis (Fortey and Owens 1999). Furthermore, their prolific abundance in rocks, their morphology, and the apparent lack of suitable hosts argue rather for a free-living lifestyle—epiplanktic (Robison 1972, 1975; Pek 1977) or rather epibenthic (Müller 1987; Slavíčková and Kraft 2001; Babcock et al. 2017; Eriksson and Horn 2017)—particularly during the adult stage (e.g., Chatterton et al. 2003; Fatka et al. 2009; Fatka and Szabad 2011; Fatka and Kozák 2014; Esteve and Zamora 2014; Moysiuk and Caron 2019).

6.2  Parasites and Pathologies in Modern Marine Arthropods Crustaceans—a major group of extant marine arthropods—are affected by various parasitic infestations and diseases caused by a variety of culprits including viruses, protists, fungi, and metazoan parasites such as helminths, mollusks, and particularly other crustaceans (Noga et al. 2009). Studies on parasites of modern decapods often focus on damage to soft tissues and only to a lesser degree on damage to the exoskeleton. Best studied in decapods is shell disease syndrome (Fig. 6.1a–d, f) caused by bacteria, fungi, and/or algae (e.g., Andersen et al. 2000; Noga et al. 2000). Not only helminths can puncture or dwell into the carapace, but shell disease syndrome has also been demonstrated to lead to cuticular damage and perforation (Klompmaker et al. 2016). Various proliferative lesions have been described, but evidence for true neoplasia is rare in crustaceans because many of these cases in the older literature appear to be erroneously attributed (see Sparks 1972 and Brock and Lightner 1990 for reviews). Brock and Lightner (1990) noted an association between proliferative lesions and concurrent viral infections in four out of seven cases in shrimps but considered it too premature to attribute an etiological role to these viruses. In some cases, parasitism can also lead to characteristic pathologies which can be traced back in the fossil record. The most well known of such features are swellings in the brachial chambers of a variety of decapods inferred to be caused by bopyrid arthropods and closely related isopods (Klompmaker et  al. 2014, 2021). Other effects such as castration and/or feminization reminiscent of the activity of rhizocephalan parasites could potentially be picked up in large well-preserved fossil samples

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Fig. 6.1  Examples of pathologies in extant decapods [(a, b, d) Callinectes sapidus; refigured from Noga et al. 2000; (c) Paractaea nodosa and (f) Cancer irroratus refigured from Klompmaker et al. 2016]

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(Bishop 1974, 1983; Feldmann 1998), but might be more difficult to tie to a particular type of parasites. These, and other types of crustacean pathologies associated with parasitism, found in the fossil record are reviewed in Klompmaker and Boxshall (2015), Haug et al. (2021) and Klompmaker et al. (2021). Horseshoe crabs are also affected by a variety of diseases caused by algae, fungi, colonial and filamentous cyanobacteria, gram-negative bacteria, and a variety of eukaryotic parasites (Nolan and Smith 2009). Disease causes locally expressed atrophy and parasites force abnormal growth around the infested exoskeleton. The shape of growth can potentially help to diagnose parasites (Bicknell et al. 2018). Pathologies in horseshoe crabs have been reviewed in greater detail by Leibovitz and Lewbart (2004). Discoloration of the carapace to the erosion of the exoskeleton caused by chlorophytal (green algal) infection of the surface of the prosoma is considered one of the most common diseases in both wild and captive horseshoe crabs (Leibovitz and Lewbart 1987, 2004), as the invading rhizoidal processes of algal zygotes can leave deep areas of erosion from the epicuticle into the exocuticle. This creates open wounds that make the host more vulnerable to secondary infections from bacteria and fungi (Braverman et al. 2012). Putative fossil evidence for fungal infections in Late Jurassic horseshoe crabs (Błażejowski et al. 2019) is still debated (Zatoń 2020; Błażejowski et al. 2020). Other parasites include a variety of protozoans, unicellular eukaryotes (Fig. 6.1h), and the digenetic trematode Microphallus limuli using horseshoe crabs as a second intermediate host; a couple of nematodes; and several turbellariid flatworms (Nolan and Smith 2009; Smith 2012). Most of the metazoan parasites do not cause obvious damage to the exoskeleton, but some nematodes (i.e., Monhysteria spp. and Grathponema spp.) have been reported to invade the carapace of horseshoe crabs (Leibovitz and Lewbart 2004). Given modern analogues, it is, therefore, safe to assume that trilobites were also affected by a variety of parasites and pathogens, ranging from viruses, bacteria, and protists to animals and plants and that these might also have resulted in recognizable pathologies of the carapace. However, it is difficult to predict the culprit without primary evidence. In some cases, the putative parasites also remain unidentified in modern marine arthropods (Jell 1989; Bicknell and Pates 2019). Bicknell and Pates (2019) have attributed an o-shaped depression in a specimen of horseshoe crab to parasitism (Fig. 6.1g, i), while Jell (1989) attributed swelling in a crab specimen to an unidentified parasite.

Fig. 6.1 (continued)  and horseshoe crabs [(e, g, h, i) Limulus polyphemus] attributed to parasitism. (a) Grade 2 shell disease syndrome lesion with erosion into calcified endocuticle (EN). (b) Grade 3 lesions with severe pseudomembrane (PM) formation over uncalcified endocuticle (EN). (c) Black spots attributed to SDS; some of these are associated with lesions that sometimes penetrate into the shell. (d) Ulceration attributed to SDS on a chela. (e) Carapace and large compound eye are partially encased by green algae on the cephalothorax (refigured from Braverman et al. 2012). (f) Black spots and lesions— some of which penetrating the shell in some areas attributed to shell disease. (g, i) Location and enlarged view of o-shaped depression attributed to an unknown parasite refigured from Bicknell and Pates (2019). (h) Second instar with evident heavy external growth of protist Zoothamnium duplicatum (refigured from Shinn et al. 2015)

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6.3  Parasites and Pathologies in Trilobites So far, no confidently identified body fossils of parasites have been found associated with trilobites. This means that at this moment we can only constrain the identity of the culprits of trilobite pathologies based on the similarities in morphology and size of particular pathologies which have been linked to parasitism in their extant marine, more distant arthropod relatives. A variety of pathologies have been reported and only four different kinds of pathologies have been attributed to parasitism based on their effect on the host (Conway-Morris 1981; Owen 1985; Jell 1989; Babcock 2007). Such pathologies have been reported in a variety of trilobite orders ranging from the Cambrian to the Devonian. Some have specifically reported on these structures (e.g., Šnajdr 1978a, b, 1981; Jell 1989; Babcock and Peng 2001), while others have at least mentioned or figured them in systematic works or monographs (e.g., Westergård 1936; Ludvigsen 1979; Geyer 1990; Elicki and Geyer 2013; Hughes 1993). Unfortunately, data on the prevalence of these structures within samples are rarely mentioned (see Table 6.1). With prevalence, we mean how many specimens were afflicted relative to the total number of specimens in a particular stratigraphically restricted sample of a certain species (De Baets et al. 2021c). In only about 22.5% of the cases considered here prevalence data is available  or could at least be calculated—which might still be an overestimate as we particularly looked for well-­documented cases. This corresponds with nine records in the literature (see Table 6.1) where both the number of afflicted specimens and total investigated specimens in the samples (in similar preservation) were explicitly mentioned. Prevalence is necessary to disentangle how common these afflictions might have been and to get a grasp on their collection and fossilization potential as well as host selectivity. Apart from the prevalence, the strength of the pathology might also vary considerably; “it might cause death, may disappear through a series of moults of inflicted on a juvenile individual, or, in the case of parasitism, may increase with growth” (Jell 1989).

6.4  Types of Pathologies 6.4.1  Neoplasia Gall-like or tumor-like swellings—named neoplasia in the literature—are the most frequently reported evidence attributed to parasitism (Šnajdr 1978a, b, 1981, 1990; Conway-Morris 1981; Owen 1985; Jell 1989; Babcock 1993, 2003a, 2007; Vokáč 1996). They have been repeatedly reported from Cambrian paradoxidids (Westergård 1936; Šnajdr 1978a; Bergström and Levi-Setti 1978; Babcock 1993, 1994, 2007), bathynotids (Elicki and Geyer 2013), and proasaphiscids (Jell 2003), but are also known from Ordovician asaphids (Owen 1985; Hughes 1993, 2001), cheirurids (Ludvigsen 1979; Conway-Morris 1981; Ludvigsen in Boucot 1981), dalmanitids

Redlichiida, Paradoxididae

Redlichiida, Paradoxididae

Neoplasia

Neoplasia

Neoplasia

Neoplasia

Neoplasia

Neoplasia

Acadoparadoxides oelandicus?

Hydrocephalus carens

Flexicalymene Ptychagnostus atavus Arthrorhachis elspethi Eremiproetus dufresnoyi Asaphida, Dikelocephalidae Dikelocephalus minnesotensis Ptychopariida, Maotunia distincta Proasaphiscidae Ptychopariida, Eymekops hermias Proasaphiscidae ?Redlichiida, Bathynotidae Conomicmacca hyperion Redlichiida, Paradoxididae Hydrocephalus carens

Neoplasia

Phacopida, Calymenidae Agnostida, Ptychagnostidae Agnostida, Metagnostidae Proetida, Tropidocoryphidae

Encrusting epizoans Healed borings Healed borings Healed borings (?)

Species Calymene

Order, family Phacopida, Calymenidae

Type Circular pits

–

Šnajdr (1958, pl. XLII, figs. 1–3, 5), Šnajdr (1978a, pl. VII, figs. 7–8, pl. VIII, figs. 1–4), Šnajdr (1990, p. 55) Westergård (1936, text-fig. 8)

–

–

1/5

–

–

 1/82

– – – –

Prevalence –

Vokáč (1996, pl. VI, figs. 2, 3)

Elicki and Geyer (2013, fig. 15.4)

Jell (1989, fig. 5D)

Hughes (1993, p. 15), Hughes (2001, p. 377, fig. 17.2A) Jell (1989, fig. 5A)

Key Jr et al. (2010, fig. 4, 1–2; fig. 6, 1–2) Babcock and Peng (2001), unfigured Babcock (1993, 2007, text-fig. 2B, C) Šnajdr (1981, pl. 3, fig. 7)

Reference Whiteley et al. (2002, fig. 2.15D–F)

Table 6.1  Pathologies attributed to parasitism in trilobites with various degrees of certainty

(continued)

Cambrian, late Wuliuan–early Drumian? Cambrian, late Wuliuan–early Drumian? Cambrian, Wuliuan

Cambrian Stage 4?

Cambrian, Miaolingian

Cambrian, Miaolingian

Cambrian, Furongian

Age Silurian, Ludlowian, Homerian Late Ordovician Cambrian, Drumian Ordovician, Darriwilian Devonian, Emsian

Neoplasia Neoplasia Neoplasia Scarred glabella

Bohemoharpes ungula Prionopeltis striata Paralejurus campanifer ?Voigtaspis sp. Lepidoproetus lepidus lepiformis Phacopida, Dalmanitidae Zlichovaspis spinifera Corynexochida, Styginidae Platyscutellum castroi Proetida, Tropidocoryphidae Koneprusites moestus Redlichiida, Paradoxididae Centropleura phoenix

Harpetida, Harpetidae Proetida, Tropidocoryphidae Corynexochida, Scutelluidae Proetida, Tropidocoryphidae Proetida, Tropidocoryphidae

Phacopida, Cheiruridae Phacopida, Dalmanitidae

Neoplasia Neoplasia combined with healed injury? Neoplasia Neoplasia Neoplasia Neoplasia Neoplasia

Paradoxides gracilis Asaphus sp. Ceraurinella nahanniensis Ceraurus hirsuitus Dalmanitina socialis

Redlichiida, Paradoxididae Asaphida, Asaphidae Phacopida, Cheiruridae

Neoplasia Neoplasia Neoplasia

Neoplasia

Neoplasia

Species Hydrocephalus sjoegreni Ptychopariida, Conocoryphe sulzeri Conocoryphidae sulzeri Redlichiida, Centropleuridae Centropleura loveni

Order, family Redlichiida, Paradoxididae

Type Neoplasia

Table 6.1 (continued)

1/13 – – – 1/86 – – 1/46 2/34 – –

Šnajdr (1978b, pl. I, figs. 1–5), Šnajdr (1990, p. 63) Šnajdr (1981, p. 48, text-fig. 6, pl. IV, Fig. 6) Šnajdr (1960, pl. 36, fig. 8) Šnajdr (1981, p. 49, pl. III, fig. 3) Šnajdr (1981, p. 49, text-fig. 7, pl. 4, fig. 4) Šnajdr (1987, pl. 4, figs. 3, 4) Rábano and Arbizu (1999) Šnajdr (1981, p. 49, pl. 4, fig. 3) Öpik (1961, p. 7, figs. 4, 5)

– – 2/653

–

Prevalence –

Ludvigsen (1979, p. 34, pl. 14, figs. 16–19) Vokáč (1996, pl. VI, fig. 7)

Babcock (1993, p. 221, fig. 3.1, 3.2), Babcock (2007, text-fig. 2F, G) Šnajdr (1978a, pl. VII, figs. 2, 4–6) Owen (1985, fig. 5u) Ludvigsen in Boucot (1981, fig. 241a)

Vokáč (1996, pl. VI, fig. 1)

Reference Westergård (1936, pl. X (unnumbered))

Devonian, early Emsian Devonian, early Emsian Devonian, Eifelian Cambrian, Miaolingian

Silurian, Ludlow Silurian, Přídolí Devonian, Pragian Devonian, Pragian Devonian, Pragian

Ordovician, Sandbian Ordovician, Sandbian

Cambrian, Drumian? Ordovician, Darriwilian Ordovician, Darriwilian

Cambrian, Drumian

Cambrian, Drumian

Age Cambrian, Wuliuan

Phacopida, Cheirurida

Geyer (1990, pl. 51, fig. 6), Geyer (personal observations) Omamentaspis Geyer (1990, pl. 26, fig. 1a–d), Geyer (personal crassilimbata observations) Olenellus getzi Ruedemann and Howell (1944, pl. 19, figs. 1, 2) “Pagetides? caltraid” Lamont (1975, pl. XXXII, fig. 9) “Trossachia pammicra” Lamont (1975, pl. XXXII, fig. 8) Megistaspis Bohlin (1960, p. 164, figs. 6, 7) Scotoharpes domina Lamont (1948a, b, fig. A)

Prevalence is the number of afflicted specimens divided by the total number of specimens

Redlichiida, Ellipsocephalidae Redlichiida, Ellipsocephalidae Olenellida, Olenellidae Eodiscina, Pagetiidae? Eodiscina, Pagetiidae? Asaphida, Asaphidae Harpetida, Harpetidae

Fatka and Budil (personal observations))

Eccoptochile cf. clavigera Geyerorodes schmitti

Asaphida, Asaphidae

Shell disease syndrome Shell disease syndrome Shell disease syndrome (?) Swellings on the inside of cranidia Swellings on the inside of cranidia Vermiform borings Vermiform borings Vermiform borings Vermiform borings Vermiform borings

Asaphida, Asaphidae

Species Reference Megistaspis Ross Jr (1957, pl. 43, fig. 12) planilimbata cyclopyge Asaphellus desideratus Šnajdr (1980, pl. I, figs. 3, 4; pl. II, figs. 1–7), Fatka and Budil (personal observations) Nerudaspis aliena Fatka and Budil (personal observations) )

Order, family Asaphida, Asaphidae

Type Scarred glabella

Cambrian Stage 4 Cambrian, Wuliuan? Cambrian Stage 4 Cambrian Stage 4? Cambrian Stage 4? Ordovician Silurian, Llandoverian

3/200 – – – – –

Ordovician, Sandbian

Ordovician, Darriwilian

Ordovician, Darriwilian

Age Ordovician

3/40

–

–

–

Prevalence –

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(Šnajdr 1987; Vokáč 1996), as well as Silurian to Devonian proetids (Šnajdr 1981), scutelluids (Šnajdr 1960; Rábano and Arbizu 1999), and harpetids (Šnajdr 1978b; Přibyl and Vaněk 1981). Some of these have been more convincingly linked with parasitic infestation (see Šnajdr 1978a, pls. 7, 8—diverse bosses, neoplasms, tumors, or even neoplasms with crater-shaped depressions infrequently present on exoskeletons of paradoxidid trilobites), while the parasitic origin of many others remains uncertain. They at least represent some of the oldest evidence for “cancerous or other types of uncontrolled tissue growth” in arthropods (Babcock 2007). Many neoplasias have been attributed to ectoparasites or external attacks more generally (Jell 1989; Šnajdr 1990). However, some authors suggested that at least some might have been caused by helminths or endoparasites more generally (Šnajdr 1978a; Jell 1989). For Cambrian proasaphiscids, Jell (1989, p. 496) proposed endoparasitic activity apparently associated with the cecal vascular system. Most of these examples show simple bulbous swellings, in some cases with a central craterlike depression. The perhaps best example is visible in a specimen of Centropleura loveni, Angelin, 1854, from the Drumian Kap Stanton Formation of northern Greenland. The specimen described by Babcock (1993, fig. 3.1, 3.2) in an incomplete carapace with a nearly perfectly circular, prominent bubble-shaped neoplasma of ca. 1.2 mm diameter developed from the anterior pleural ridge of thoracic segment 6. While the thoracic pleurae are beset with relatively coarse and sharp terrace ridge-type wrinkles, the neoplasia appears to show only minute wrinkles or is smooth for the most part. It is fairly obvious that the growth of the neoplasia affected not only the part of the pleura from which it originates but also the posterior part of the anteriorly neighboring pleura, the posterior margin of which is indented. Šnajdr (1978a, pl. VII, figs.  7, 8) figured specimens of the paradoxidid Hydrocephalus carens (Barrande 1846) from the Buchava Formation of the Skryje– Týřovice area (Barrandian region) with bubble-shaped neoplasms of elliptical outline (ca. 2 mm in length and about 1.4 mm in width), situated in the left pleural furrow of a thoracic segment to a slightly larger (ca. 2.6 mm in length and 2.2 mm in width) conical parasitic neoplasm on the left fixigenae of the same species as type X1 neoplasia. Šnajdr (1978a, pl. VII, fig. 5) also described smaller, more irregular (type X2) neoplasia in Paradoxides gracilis. He interpreted that in various unfigured specimens belonging to these two paradoxid species there is a gradual formation of crater-shaped depressions. The neoplasms in Bohemian paradoxidids are often restricted to the thoracic pleural furrows or their immediate vicinity (compare Jell 1989). Similarly shaped, but generally smaller, neoplasms were described in diverse proetid and harpetid trilobites from the same area (Šnajdr 1978b, 1981, 1990; see also Fig.  6.2b–g herein). In the case of Bohemoharpes ungula, Šnajdr (1978b) argued for external attacks (?) and the ectoparasitic nature of the culprits as tracked from bulges with abnormal calcification in early overthinning to bosses with a central craterlike depression and perforation/breakage in the cross section of later ontogenetic stages. These neoplasms were typically found on the brim and genal roll of several specimens belonging to the same species. Increased calcification/thickening of the carapace has not explicitly been reported in relation to shell disease in extant

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Fig. 6.2  Neoplasia and neoplasia-type structures in trilobites. (a) Conomicmacca hyperion (Elicki and Geyer 2013), paratype, FG-602-058c, pygidium with large neoplasm of elliptical to subtriangular outline. Burj Formation, Numayri Member, lower–middle Cambrian boundary interval, Wadi Uhaymir section, Dead Sea region, Jordan. (b, e, g) Zlichovaspis spinifera (Barrande 1846), NML 22571, pygidium with neoplasm located on the left pleural region in the interpleural furrow; originally described and figured by Šnajdr (1987, pl. 4, figs. 3–4). Praha Formation, Pragian, Lower Devonian, Praha-Bráník locality, Barrandian region, Czech Republic. (c) Koneprusites moestus (Barrande 1852), CGS MŠ 5170, pygidium with a tumorlike neoplasm on the left postaxial part; originally figured by Šnajdr (1981, pl. 4, fig.  3), Choteč Formation, Acanthopyge Limestone Facies, Eifelian, Middle Devonian. Červený lom quarry near Suchomasty, Barrandian region, Czech Republic. (d) Voigtaspis? sp., CGS MŠ 6939, pygidium with a tumorlike neoplasm on the left pleural region; originally figured by Šnajdr (1981, pl. 3, fig.  3). Praha Formation, Vinařice Limestone Facies, Pragian, Lower Devonian, quarry at the Homolák hill, Barrandian region, Czech Republic. (f) Prionopeltis striata (Barrande 1846), CGS MŠ 4797, pygidium with a tumorlike neoplasm on the postaxial area; originally figured by Šnajdr (1981, text-fig. 6, pl. 4, fig. 6). Silurian, Požáry Formation, Přídolí, Silurian. Jarov near Beroun, Barrandian region, Czech Republic. Scale bars 5 mm in (a, b) 1 mm in (c–g)

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arthropods, but other factors such as thinning and perforation of the carapace were (Andersen et al. 2000; Noga et al. 2000). Discoloration of the carapace—another feature considered the first stage in shell disease—was so far not reported in trilobite pathologies discussed by Šnajdr (1978a, b, 1981). This is not that surprising as it will only be visible on specimens with a preserved exoskeleton. The sequence described by Šnajdr is also not entirely consistent with the healing of injuries in horseshoe crabs where hemolymph coagulum quickly plugs the wound, pigmented epithelial cells produce a layer of cuticle under the wound, and the enlarged cuticular scar is rapidly lost through changes that eventually restored the original tissue structure (Bursey 1977). Elicki and Geyer (2013, fig. 15.4) figured a pygidium of the bathynotid trilobite Conomicmacca hyperion from the lower-middle Cambrian boundary interval (Dead Sea region, Jordan), which shows large neoplasia (Fig.  6.2a). The structure is located on the posterior pleural region adjacent to the furrow that separates the pygidial axis from the pleuron. It has a slightly elongated elliptical to subtriangular outline, with a maximum length of 4.8 mm. In lateral view, the neoplasia is considerably domed and has an irregular arrangement of cracks composed of three fissures that meet slightly posteroadaxially of the center. This is attributed to a postmortem formation during early diagenesis. The pleural area immediately adjacent to the neoplasm has reduced relief when compared to the opposite side of the pygidium, and the central part of the posterior margin is developed slightly asymmetrically. The neoplasia growth may, therefore, have affected pygidial growth. Westergård (1936, text-fig. 8) figured a librigena tentatively assigned to Acadoparadoxides oelandicus (Sjögren 1872) from the Wuliuan of Öland, southern Sweden, which shows a prominent, transversely oval neoplasm located on the librigenal field a short distance from the posterior end of the eye. The swelling is of considerable height and occupies about one-third of the width of the librigenal field in an oblique direction from the ocular suture. Another, less prominent, swelling is noted from a nearly complete carapace of Hydrocephalus sjoegreni (Linnarsson 1877) from the same strata (Westergård 1936, pl. X). This swelling is again located on the librigenal field, laterally from about the center of the eyes, and has approximately the same relative dimension. In Dalmanitina socialis (Barrande 1846) described by Vokáč (1996, pl. 1, fig, 7), a possible small, inconspicuous neoplasm with a subconical elevation between the palpebral lobe and the posterior margin of the cheek is combined with a healed injury of the right fixigena and librigena. This malformation may also reflect a healing process, but we cannot rule out that the injury might make the specimen more susceptible to secondary infection. As this specimen is only represented by an internal mold housed in a private collection (external mold does not exist) this cannot be further evaluated. Šnajdr (1987, pl. 4, figs. 3, 4; Fig. 6.2b, e, g herein) described interesting neoplasia of subrectangular to elliptical outline on the ventral side of the exoskeleton in Zlichovaspis spinifera (Barrande 1846), situated in the interpleural furrows 3–4 on the left pygidial pleural area. This neoplasia is fairly large (about 4.8 mm long and about 2 mm in width) and of minor convexity.

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The original nature of the agents is usually uncertain. A myzostomid origin for such galls was suggested by Ludvigsen (1979), but the evidence is lacking. Šnajdr (1978a) traced the ontogenetic development of galls in the various molt stages of the trilobite, and this approach makes it possible to uncover external (ectoparasitic?) versus internal (endoparasitic) nature of the agents. This at least allowed Šnajdr to distinguish two main types of neoplasms: those formed by parasites that lived beneath the exoskeleton and survived one or more molting events, and those formed by organisms located at or near the exoskeletal surface and thus got lost during molting. Neither type, however, shows strong site selectivity which might suggest that they were caused by ectoparasites—consistent with their common occurrence in the protective hollows of pleural furrows (Jell 1989). Possible exceptions are described by Jell (1989), which figured five bulges in Moatunia distincta and four bulges in a specimen Eymekops hermias associated with the cecal system suggesting that endoparasites might have been lodged in the respiratory system and bulging the exoskeleton around it. However, he could not entirely rule out that the bulging itself resulted from the disease without physically reproducing an endoparasite.

6.4.2  Borings Borings could have developed in trilobite exoskeletons during the lifetime as well as in carcasses and molts. Most borings in trilobites probably occurred postmortem or post-molting (Dalingwater 1975; Babcock 1993, 2003a; see Babcock 2007 and Bicknell and Paterson 2018 for reviews). Størmer (1931) discussed thin sections showing possible borings of trilobite exoskeletons and interpreted them as being produced by various plants and animals in the living trilobite. Only borings associated with a cellular response could convincingly have been formed while the trilobite was alive. Some authors distinguish between boring and drilling. Borings are thought to develop irrespective of life/death of the host organisms and produced by an organism that typically lives in this structure as a dwelling. Drilling, on the other hand, is seen as punctures that develop during life in response to predation (Bicknell and Paterson 2018; Klompmaker et al. 2019). Even in the presence of host response, it might be difficult to interpret the culprit—particularly when the culprits are not preserved and leave no characteristic traces. We, therefore, prefer to use boring as a more neutral term for punctures formed during life or after death within our chapter. Interestingly, some borings preserved as small pits associated with tissue growth and exoskeletal deformation in agnostoids have been interpreted as potential evidence for parasitism (Babcock 2007). Two specimens of agnostids with such borings were reported thus far: a specimen of Arthrorhachis elspethi (Raymond 1925) from the Middle Ordovician of Virginia, USA (Babcock 1993), and a specimen of Ptychagnostus atavus (Tullberg 1880) were described from the Drumian of the Hunan Province, China (Babcock and Peng 2001). A perforated pygidium of Eremiproetus dufresnoyi (Hawle and Corda 1847) from the Early Devonian of the

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Fig. 6.3  Eremiproetus dufresnoyi (Hawle and Corda 1847), CGS MŠ 5423, pygidium with an irregular, subcircular opening on its left pleural field, with possible traces of healing shown in dorsal (a) and oblique posterolateral (b) views; described and figured by Šnajdr (1981, pl. 3, fig. 7), Daleje-Třebotov Formation, Suchomasty Limestone facies, late Emsian, Middle Devonian. Koněprusy locality, Barrandian region, Czech Republic. Scale bar 1 mm in (a)

Barrandian region, Czech Republic, shows an irregular, subcircular opening with possible traces of healing described by Šnajdr (1981, pl. 3, fig.  7) that may also belong to this type of pathology (Fig. 6.3a, b). In Arthrorhachis elspethi, this type of boring is sealed internally by a pearl-like protuberance. The malformation in Ptychagnostus atavus is described (but unfortunately not figured) as a pit terminating in a bulbous, pearl-like swelling on the internal surface of the cephalon. Babcock and Peng (2001) discussed causes of the two examples of small healed shell damage. They suggested that the position may indicate location bias for putative predation or parasitism or a miscalculation of the drilling location that was nonlethal and repaired by the host. In the first case, the apparent site selectivity, close to the right bacculae, indicates that an internal structure close to the axis (e.g., the intestinal tract) or an adjacent structure (e.g., a brood pouch) may have been the target of parasites—the morphology might suggest that an organism stayed in this structure for some time. However, we cannot rule out that the healed pits might suggest a failed attack, and a drill hole into the intestinal track might have been lethal. However, parasites could be responsible for abnormal growth around the infested exoskeleton. Pearls, blisters, and associated structures have commonly been attributed to endo- or ectoparasitism in other metazoans, like mollusks (De Baets et al. 2011; Huntley and De Baets 2015; De Baets et al. 2021b; Huntley et al. 2021) or

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conularids (Babcock 1990)—particularly in the absence of mechanical injuries. Babcock (2007) compared this type of borings in trilobites with similar ones interpreted as nematode borings in foraminiferans (Sliter 1971). However, although a variety of nematodes dwelling in foraminifers might be parasitic (Hope and Tchesunov 1999), it is unclear if these nematodes produced such borings (at least in foraminifers) as they seem to lack suitable jaw mechanisms (Lipps 1983; Culver and Lipps 2003). Other types of borings have been linked with helminths, but this could not be corroborated. Lamont (1948a, b, 1975) shortly described borings seen in trilobite sclerites, which are difficult or impossible to verify. Lamont (1975, p.  200–201) noted that in the lower Silurian trilobite Scotoharpes domina (Lamont 1948a, b), a “halo-like fringe contains not only borings but also saucer-shaped or hooplike depressions in which a worm about 5 mm long coiled itself up while shell of the trilobite was being deposited.” Unfortunately, the figure presented in Lamont (1948a, b, fig. A) is an imperfect drawing that does not allow us to recognize enough details to confirm the information detailed by Lamont.

6.4.3  Shell Disease Syndrome Shell disease is usually defined as a complex syndrome, which includes several independent and apparently unrelated infections (Klompmaker et al. 2016). It has been best studied in decapod crustaceans, where various levels of damage to their integument have been observed ranging from a singular pitting and discoloration of the carapace to an extensive loss of the integument (Smolowitz et al. 1992; Noga et  al. 2000; Shields and Overstreet 2007). In some cases, it can also result in an exposure of the underlying soft tissue (e.g., Comeau and Benhalima 2009), ulceration, formation of pseudomembranes, and even partial loss of the carapace (e.g., Noga et al. 2000). Typically microbial pathogens (particularly chitinolytic bacteria) have been considered the main agents in shell disease (Shields and Overstreet 2007; Vogan et  al. 2008; Gomez-Chiarri and Cobb 2012), although other agents might also be involved as true fungi and oomycetes are occasionally observed in lesions of marine crustaceans (e.g., Noga et  al. 2000; Quinn et  al. 2009). Infestations with other parasites might also make specimens more prone to shell disease (Vazquez-­ Lopez et al. 2012). Pathogens like bacteria and fungi use a combination of physical and enzymatic processes to breach the arthropod cuticle (Moret and Moreau 2012), and such pathogens have also been identified from some shell lesions of other marine arthropods such as horseshoe crabs (Tuxbury et al. 2014; LaDouceur et al. 2019). Shell disease manifested by discoloration of carapace or erosion of the exoskeleton (Fig. 6.1a) is the most commonly identified diseases in horseshoe crabs (Nolan and Smith 2009), where chlorophytes (green algae) are the most commonly identified pathogen (Leibovitz and Lewbart 1987, 2004; Braverman et al. 2012). In the fossil record, the only case of supposed shell disease syndrome has been documented in Early Cretaceous crabs (Klompmaker et al. 2016). Similar damage

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of the exoskeleton is, however, newly discussed by Fatka et al. (in preparation) for trilobites as well. Numerous swellings and impressions on trilobite exoskeletons have been documented in Asaphellus desideratus (Barrande 1872) (earlier briefly described and interpreted as vermiform structures by Šnajdr 1980) and in Nerudaspis aliena from the Middle Ordovician of the Czech Republic (Fatka and Budil, unpublished observations). The size and shape of these swellings and impressions (occurring sometimes together with more extensive damage of exoskeleton) correspond well to the exoskeletal lesions classified as shell disease syndrome (SDS) with bacteria as major agents in recent crustaceans (Noga et al. 2000; Klompmaker et al. 2016). As all the studied material is represented by internal and external molds in clastic sediments, the original exoskeleton is not preserved. Consequently, discoloration or development of pseudomembranes could not be observed. Shell disease in horseshoe crabs (Brock and Lightner 1990) is often related to green algae, but the pathologic effects on the carapace (as far as they have been studied) are less similar in size and shape to the ones in trilobites discussed here.

6.4.4  Pits A particularly convincing case for endoparasitism is recorded from middle Cambrian ellipsocephalid trilobites. Geyer (1990, pl. 26, Fig. 1a–d) figured malformations on cranidia of Ornamentaspis crassilimbata (Geyer 1990) from lowermost Wuliuan(?) strata of the Jbel Wawrmast Formation in the High Atlas, Morocco. The malformations are circular depressions with a slight central uplift on internal molds of the cranidia, particularly well recorded on a single cranidium, in which these pits are clearly concentrated along the furrows adjacent to the glabella. The depressions on the internal mold indicate that the shell has been swollen at those places, leaving the impressions of larger central pits (Fig. 6.4a–d). Similar structures have recently been found in coeval ellipsocephalids from the Wuliuan of drill core D I/1927 from the Delitzsch–Torgau–Doberlug region of Saxony, Germany (Schmidt 1942). This previously unstudied material provisionally assigned here to “Ornamentaspis” n. sp. includes a cranidium with a preserved test that shows very similar structures as described above from the Moroccan specimens of O. crassilimbata. These structures are developed as shallow depressions on the exterior of the cuticle and again concentrated to the furrows that border the anterior part of the glabella (Geyer, unpubl. data; Fig. 6.4e–g). It is considered that in both cases a similar type of parasite might have been present so that the cranidia from southern Morocco and eastern Germany possibly record the internal and external morphologies of deformation of the cuticle. If so, the cuticle must have been thinner at the affected locations, developed as a central crater-shaped indentation on the exterior and a corresponding internal raise with the central pit on the interior of the cuticle. Both the preferential location along the furrows and developed concentric ridges on the internal side of the cuticle suggest that the obvious preference of the parasites appears to have been stimulated by the soft-part morphology of the trilobite animal.

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Fig. 6.4  Malformations resulting from parasitism below dorsal cuticle. (a–d) Ornamentaspis crassilimbata Geyer 1990; (a) SMF 41879a, internal mold of cranidium with circular depressions concentrated to furrows; note slight central uplift (arrow); figured by Geyer (1990, pl. 26, Fig. 1a–1d). (b–d) SMF 52586c, incomplete, largely exfoliated cranidium with circular depressions, particularly deep in lateral glabellar furrows, dorsal, oblique anterior and oblique anterolateral views. Both specimens from Jbel Wawrmast Formation, Brèche á Micmacca Member, Ornamentaspis frequens Zone, probably base of Wuliuan Stage, Cambrian, from eastern limb of Lemdad Syncline, High Atlas, Morocco. (e–g) “Ornamentaspis” n. sp., GSB X4774, incomplete cranidium with preserved test showing deep circular depressions concentrated to adaxial half of fixigenae and circumglabellar furrows; figured and described as Kingaspidoides frankenwaldensis by Schmidt (1942, pl. 24, fig. 14). Tröbitz Formation, Wuliuan Stage, Cambrian, from drill core D I/1927 near Kirchhain, Delitzsch-Torgau-Doberlug Syncline, Saxony, Germany. All scale bars 1 mm

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6.4.5  O  ther Types of Abnormalities Less Confidently Linked with Parasitism Many additional abnormalities in trilobites have historically been tentatively attributed to parasitism (e.g., Schmidt 1906; Richter and Richter 1934), but most likely arose during molting or other types of injuries (compare Jell 1989). Owen (1985) suggested that scarred glabellas present in two previously illustrated trilobites—a Cambrian Centropleura (Öpik 1961) and an Ordovician Megistaspis (see Ross Jr 1957)—might have resulted from parasitic infection. Indeed, Öpik (1961, p. 7, figs. 4, 5) illustrates a specimen of Centropleura phoenix (Öpik 1961) from the late Drumian to early Guzhangian Devoncourt Limestone of Queensland, Australia, which shows teratological modifications of the test on the cranidium. Visible are bubble-like swellings which are arranged in two series along slightly irregular lines on the right-hand side of the frontal lobe of the glabella Öpik (1961, p. 7, figs. 4, 5). The series to the right consists of fewer, but slightly larger, swellings. These larger swellings occasionally appear to indicate small openings in subcentral positions, whereas the series to the left consists of numerous (more than a dozen) small and low swellings without such openings. If Owen’s (1985) interpretation of parasitism is correct the right series could represent a more advanced development of a parasitic infestation, in which the culprits may have developed to a stage in which grown individuals had left the host, whereas the left series may indicate an earlier stage of development. Ross Jr (1957) described a trilobite from the Lower Ordovician Deadwood Formation of well drilling in the Williston Basin in eastern Montana, USA, determined as Megalaspis planilimbata var. cyclopyge. The only available cranidium is described as having pathologic features. Ross Jr (1957) discussed that large, deep subangular muscle scars exist on the right side of the cranidium as well as a peculiar scar on the left side of the glabella. Unfortunately, the only accessible figure does not allow us to evaluate this in greater detail. One cannot rule out that the scars indicate sites of injury (compare Owen 1985), but perforation, breakage, and loss of carapace have also been demonstrated to be the results from secondary infections and/or shell disease syndrome (e.g., Noga et al. 2000). Meandering vermiform traces have also been occasionally attributed to parasitism (Conway-Morris 1981). Meandering vermiform traces are known from at least three specimens of Geyerorodes schmitti (Geyer 1990) from the latest early Cambrian (latest part of Cambrian Stage 4) part of the Jbel Wawrmast Formation in the western Anti-Atlas, Morocco (Geyer 1990 and unpublished data). The traces are preserved as branched, distinctly curved hollow traces located below the cuticle of the cephalic exoskeleton, particularly below the glabella (including occipital ring, Geyer 1990, pl. 51, figs. 3, 4, 5). The traces were formed below the cuticle (impressions on internal molds or with small remains of the cuticle preserved), and the cuticle does not show any healing response to the infestation. In addition, the traces are distributed over a distance that would have caused severe damage if developed when the trilobite individuals were alive. Thus, the traces rather reflect the consumption of organic matter during the decay of a carapace.

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Similar meandering traces might also have been described by Lamont (1975) and attributed to nematode infestations. Lamont (1975) identified such meandering vermiform traces in lower Cambrian and Silurian trilobites and reviewed various other putative worm traces in trilobites. Unfortunately, Lamont’s material from the Leny Limestone Formation (lower-middle Cambrian boundary Avalonian, Scotland) is too poorly preserved and inadequately documented to allow confirmation of Lamont’s interpretation of “worm infestations.” Such “worms” were reported by Lamont (1975) in a thoracic segment of Pagetides? caltraid (Lamont 1975) (which is a taxonomically undeterminable specimen according to Fletcher and Rushton 2005) and a cranidium of Trossachia pammicra (Lamont 1975) (holotype of the species, lost according to Fletcher and Rushton 2005) from the Leny Formation. Lamont (1948b) also identified “worms” in Praedechenella peeblesi [= Proetus (Lacunoporaspis) sp. according to Clarkson and Howells (1981)] from the upper Llandoverian Wether Law Linn Formation (Pentland Hills, Scotland). However, all features identified by Lamont (1948b, 1975) are suspected to be erroneously interpreted. Furthermore, Lamont (1975) interpreted a “worm tube” to be present on the eodiscoid Mallagnostus? llarenai cephalon (Richter and Richter 1941) from the Cambrian Stage 4 of Cala in Andalusia, southern Spain (Richter and Richter 1941, pl. 2, fig.  25). However, an examination of the specimen by GG did falsify Lamont’s assumption. Peach (1894) detected meandering traces on spines of the olenellid genera Peachella and Olenellus from Laurentian Northwest Scotland, which he interpreted as remains of a nematode. He even named these fossils Cadella flexuosa (Peach 1894, pl. XXXII, figs. 13–15). It should be emphasized that these might be rather commensal than parasitic if one can even rule that they developed postmortem. Šnajdr (1990, p.  54) also described a peculiarly malformed pygidium of Hydrocephalus carens (Barrande 1846) (compare Šnajdr 1958). The pygidium of this specimen has strongly reduced lateral pleural lobes and the postaxial area is fused with four (possibly five) thoracic segments. He noted the reduction of the distal and proximal peripheries of the thoracic segments, transversally shortened pleura, and fused axial rings. He suggested that its stunted and deformed appearance could possibly be explained by the activity of parasites following incomplete separation during molting, but could not rule out partial amputation and deformation by a durophagous predator. Šnajdr (1978a) also described fused axial rings associated with putative parasitic neoplasms in Paradoxides gracilis (Boeck 1827). These hypotheses, however need further testing.

6.4.6  Epizoa and Epicoles Just like borings, sclerobionts might have encrusted the trilobite exoskeleton after death or post-molting. So far well-studied examples include forms with fossilizable hard parts such as bryozoans, brachiopods, crinoids, and edrioasteroids that have been found (Budil and Šarič 1995; Brandt 1996; Kácha and Šarič 2009), while

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soft-­bodied epizoans might preferentially get lost. If encrustation or fouling happened during life, it might have restricted the mobility of its host and affected growth, molting, and functions of several organs (eyes, gills, and appendages) just as in extant crustaceans (Fernandez-Leborans 2010) or horseshoe crabs (Botton 1981). It may cause an increased predation risk, and the encruster (epibiont) and the host (basibiont) may compete for nutrients (Fernandez-Leborans 2010). Usually, isolated epibionts do not cause major damage, but depending on the context and/or heavy infestation, they could harm the host. If the disadvantages suffered by the host outweighed potential benefits—it could be considered facultatively parasitic (compare Becker 1996). Attachment sites of epizoans on trilobite exoskeletons and effects on its hosts could be potentially confused or graded into parasitism (e.g., Šnajdr 1990). Whiteley et al. (2002, fig. 2.15D–F) referred to circular pits with slightly irregular margins that incompletely penetrate the exoskeletons of some Silurian Calymene specimens as borings. Babcock (2007) stated that these shallow pits show no clear evidence of cellular response to injury (e.g., rims characteristic for embedment) and might therefore even be postmortem. Even if they developed in vivo, it is unlikely that the pit formers did much harm to the trilobite hosts as the pits do not penetrate deeply enough to affect the internal soft tissues or even be called borings. Babcock (2007) also compared them with traces reported as Tremichnus from Silurian crinoids (Brett 1985), which have been interpreted as attachment sites of commensal epizoans (Brett 1978). Pitting to perforations in extant decapods can however also be caused by shell disease syndrome (Noga et al. 2000; Klompmaker et al. 2016). The external surfaces of the exoskeleton of extant horseshoe crabs host a number of ectocommensals including bryozoans, sponges, barnacles, blue mussels, lady slippers, snails, oysters, whelks, and a variety of coelenterates, annelids, and free-­living nematodes (Botton 1981; Turner et al. 1988; Deaton and Kempler 1989; Dietl et al. 2000; Grant 2001). However, these rarely cause harm to the horseshoe crab, except when they directly interfere with normal functions such as mobility or respiration. Such ectocommensalism is, most probably, the case for diverse edrioasteroids frequently attaching to articulated exoskeletons of late holaspid Ordovician odontopleurid genus Selenopeltis (see Prokop 1965; Sumrall and Zamora 2011) or other trilobites (Jell 1989). Encrustations of Flexicalymene discussed by Brandt (1996) and Key Jr et al. (2010) mostly correspond with commensalism. However, in some cases, epizoans substantially limited the host’s (e.g., Flexicalymene) mobility and its ability of vision by encrusting almost the entire cephalon or large parts including eyes (Key Jr et al. 2010, fig. 4, 1–2; Fig. 6, 1–2). In such cases, the encrustation can be considered as a kind of parasitism because it caused at least some harm to the host. It is, however, uncertain whether the restricted moving and vision were not overbalanced by some benefits, for example, an effective camouflage of the host. Ruedemann and Howell (1944) reported a comparatively large elliptical groove preserved on a composite mold of an Olenellus getzi cephalon (middle Cambrian Kinzers Formation, Pennsylvania) and considered it as an impression of a worm body in the cuticle of the trilobite. The groove is ca. 7 mm long, narrow, u-shaped

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loop with sharp edges. It must, therefore, be either abrasive remains of an epizoan worm tube that is now completely dissolved or a worm tube etched into the cuticle. Bohlin (1960, p. 164, figs. 6, 7) discussed “branching, winding, and anastomosing ridges” that cover large parts of pygidia of the asaphid species Megistaspis (M.) obtusicauda and M. (Megistaspidella) bombifrons that were developed as irregular nets (Lower Ordovician Vaginatum Limestone, Öland, Sweden). Bohlin interpreted them as calcite infillings of tubes bored into the test or developed as erosive grooves, without proposing their producers. Comparable structures were mentioned already by Portlock (1843) from trilobite specimens collected in Northern Ireland. The tubes were likely formed by bioeroding organisms or sclerobionts after death and should not be confused with evidence for parasitism.

6.5  Possible Culprits The identification of the agents of various pathologies is not always straightforward particularly if these are soft bodied and have a limited preservation potential. Extant analogues might provide some clues, but we can never rule out that more distantly related organisms with similar behavior might cause similar pathologies. Furthermore, the lack of evidence for soft-bodied metazoan parasites does not necessarily implicate viruses or bacteria as the agent might have been transported away or decayed preferentially. More resistant spores of fungi and algae are yet to be found associated with such pathologies. Experimental taphonomy with extant decapods and their isopod parasites show that finding evidence of agents even within swellings might be limited (Klompmaker et al. 2017, 2021). It is, therefore, not surprising that only a subset of the pathologies discussed here has been confidently attributed to particular groups of parasites or pathogens. As explained above some might even be triggered by probable epizoa or mechanical injuries—in the presence or absence of secondary infections. Several traces have been attributed to helminths or at least compared with traces produced by “worms” in absence of direct evidence (Lamont 1948b, 1978; Šnajdr 1978a, b, 1980; Conway-Morris 1981; Babcock 2007). Apart from various meandering traces, healed borings in agnostid specimens (Babcock 2007) have been unlikely compared with traces interpreted to have been produced by nematodes dwelling in foraminifers (Sliter 1971). Ludvigsen (1979) implicated myzostomid annelids in at least one gall-like swelling, but this is rather unlikely (compare Conway-Morris 1981). Myzostomid annelids are typically associated with echinoderms—mainly crinoids and to a lesser degree asteroids and ophiuroids (Summers and Rouse 2014). Various other culprits may have been responsible for diseases including those implicated in diseases of other marine arthropods including viruses, bacteria, protists, fungi, algae, multicellular plants, and parasitic animals (e.g., arthropods, helminths). Direct evidence to implicate most of these groups is, however, lacking to date. A more detailed investigation of specimens with well-preserved exoskeletons using thin-section or computed tomography might help to better characterize the

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morphology and structural changes associated with these pathologies. In turn, this could lead to narrowing down the potential culprits. At least some structures are reminiscent of shell disease in modern crustaceans. Although various pathogens have been implicated in shell disease (and might work in synergy), bacterial agents seem to be a major contributor to shell disease syndrome in extant forms and were likely involved with similar syndromes in trilobites. Given their characteristics (degree of discoloration, type of lesions, and perforations), it might be possible to constrain the culprit more precisely (Andersen et al. 2000; Noga et al. 2000). To clarify this, additional large samples of trilobite species might be necessary through various molting stages as well as histological sections in well-­preserved specimens to understand their nature. Potentially, one could even find more resistant remains of agents in such pathologies (e.g., fungal or algal spores). A better understanding of the characteristics and etiologies of modern pathologies in extant marine arthropods (e.g., horseshoe crabs, decapods) might also help to attribute them to viral, bacterial, algal, or metazoan agents.

6.6  Conclusions At least some paleopathologies can be more convincingly linked with parasitism in trilobites. These include some types of swellings, lesions, borings, and pitting. There is so far no convincing evidence that meandering vermiform traces are formed during life, while swelling or scars associated with mechanical injuries might represent secondary infections at best. The exact agents of particular pathologies are hard to determine, but at least some are consistent with shell disease syndrome in extant marine arthropods where bacteria are often major agents. Historically helminths have often been implicated in pathologies in trilobites, but so far confident evidence is lacking. A better understanding of the contribution of these and other agents in skeletal pathologies in extant marine arthropods as well as a study of large samples of particular trilobite species in suitable preservation and histological to virtual sections might help to further identify the culprits more convincingly. Acknowledgments  The contributions of P. Budil and O. Fatka have been supported by the Grant Agency of the Czech Republic (GACR) Project No. 18-14575S (PB, OF), those of G. Geyer by research grant GE 549/22-1 of the Deutsche Forschungsgemeinschaft (DFG). We would like to thank John Huntley and Russell Bicknell for their constructive comments on a previous version of this manuscript which helped to improve the final product.

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Chapter 7

Evolutionary History of Cephalopod Pathologies Linked with Parasitism Kenneth De Baets, René Hoffmann, and Aleksandr Mironenko

Abstract  Extant cephalopod soft tissues are commonly infested by various lineages of parasites making it plausible that extinct cephalopods also had a variety of parasites. Direct evidence of such a relationship is rare, due to the low preservation potential of soft tissues of fossil cephalopods and parasites alike, and the relatively scarce infestation of mineralized tissue by parasites. Evidence for infestations in the fossil record is, therefore, overall rare and limited to shell pathologies. Comparative studies on these structures in extant cephalopods are also not very numerous. Based on similar bauplans and biomineralization pathways, parasiteinduced pathologies in bivalves and gastropods can inform about their causes. The position of these features might reveal their parasitic nature. The restriction of these structures to certain cephalopod lineages might indicate the influence of phylogeny, anatomy and potential role of ecology (feeding, mode of life) on infestation risks. However, preservation and research biases might also contribute to differences between externally and internally shelled cephalopods. Other long-term associations with detriment to cephalopods such as epizoa and bioerosion as well as other malformations, which can be confused with parasitic causes, are briefly discussed. Keywords  Paleopathology · Blister-pearls · Volume-changing pathologies · Asymmetry · Apertural shell growth · Gigantism · Parasitosis

K. De Baets (*) GeoZentrum Nordbayern, Fachgruppe PaläoUmwelt, Friedrich-Alexander University Erlangen-Nürnberg, Erlangen, Germany e-mail: [email protected] R. Hoffmann Ruhr-Universität Bochum, Institute of Geology, Mineralogy, and Geophysics, Bochum, Germany e-mail: [email protected]; [email protected] A. Mironenko Geological Institute of Russian Academy of Sciences, Moscow, Russia e-mail: [email protected] © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 K. De Baets, J. W. Huntley (eds.), The Evolution and Fossil Record of Parasitism, Topics in Geobiology 50, https://doi.org/10.1007/978-3-030-52233-9_7

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7.1  Introduction Despite the increasing knowledge on diseases in cephalopods, only limited information on etiologies is available (Hochberg 1990; Gestal et al. 2019b)—this is particularly the case with pathologies of mineralized structures (Keupp 2006; Kruta and Landman 2008; Keupp and Hoffmann 2015; Jongbloed et al. 2016; Hoffmann et al. 2018b). Here we consider pathologies as normed abnormalities and follow the framework of the forma aegra system introduced for Jurassic ammonoids by Hölder (1956). The question arises if such pathologies are generally rare or have just been overlooked. It has been shown that all well-studied species of cephalopods harbour specific parasites (Pascual et al. 2007). This is not surprising considering that cephalopods are a key trophic element in marine communities. The widespread distribution of cephalopod and parasite phyla alike in all major oceans and seas, from coastal and shelf to oceanic and deep-sea environments, corroborates this statement (Pascual et al. 2007). It is therefore likely that extinct cephalopods also were infested by a variety of parasites, which could potentially also have left traces in mineralized structures. Research on extant cephalopods has, however, particularly focused on soft-bodied pathogens and pathologies in soft tissues (Hochberg 1990; Castellanos-­ Martínez and Gestal 2013; Roumbedakis et  al. 2018; Gestal et  al. 2019b), while research in the past is targetted towards mineralized structures (Keupp 2012; De Baets et al. 2015b; Mironenko 2016; Fig. 7.1) with a higher preservation potential (Clements et al. 2017). At least since the work of Shufeldt (1892), the latter—occurrences of pathologies in fossils—are called paleopathologies (compare Buikstra and DeWitte 2019).

7.2  Parasites and Pathologies in Cephalopods Extant coleoids (squids, octopuses and their relatives) are known to be the definitive hosts for protists, dicyemids, monogeneans and crustaceans as well as intermediate or paratenic hosts for digenean, cestode or nematode helminths (Hochberg 1983, 1990; Castellanos-Martínez and Gestal 2013; Gestal et al. 2019b). The evolutionary origin of parasites within cephalopods—particularly of enigmatic parasite lineages restricted to coleoids such as Aggregata (Coccidia) and Dicyemida—is still poorly resolved (Weinstein and Kuris 2016; Roumbedakis et al. 2018). Fig. 7.1  (continued) 30  mm height. (b) Blister pearl in Nautilus macromphalus, Recent, New Caledonia, AMNH, max dm of pearl: 6 mm. (c, d) Development of shell lamellae related with a local detachment of the mantle in a captive Nautilus pompilius, Recent (1990–1993), Aquarium of the Jura-Museum Eichstätt, SHK PN-12, dm = 110 mm (c), SHK PN-11, dm = 109 mm (d; taken from Keupp and Riedel (1995)). (e, f) Development of shell lamellae related with a local detachment of the mantle in two specimens of Cleoniceras besairiei, Albian (Cretaceous), Ambatolafia (Madagascar), SHK PA-33582-1, dm  =  85  mm (e), SHK PA-23675a, dm  =  127  mm (f). Scale bar = 1 cm

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Fig. 7.1  Comparison of similar pathologies in extant shelled molluscs and ammonoids (modified from Keupp 2012 unless otherwise stated). (a) Progressive development of a deep slit-shaped recess in the apertural margin attributed to parasitic infestation in Pila sp., Recent, Egypt, about

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Most pathologies, which have been described in extant forms, occur in the soft tissues (Roumbedakis et al. 2018; Gestal et al. 2019b). Recently, some pathologies of mineralized tissues have been tentatively attributed to parasitism in Sepia (Jongbloed et al. 2016) and Spirula (Hoffmann et al. 2018b), but the culprits are uncertain as the cephalopod material was derived from modern death assemblages. Some structures in jaws (Kruta and Landman 2008) and conchs of Nautilus (Landman et al. 2001; De Baets et al. 2015b) are potentially also related with parasitism but might be equally subjective. A variety of pathologies have been attributed to parasitic infestation in externally shelled cephalopods—particularly in fossil forms (Hengsbach 1991b; Keupp 2012; De Baets et al. 2015b; Mironenko 2018). So far, only parasitic copepods residing in the gills are known from extant nautilids (Ho 1980), which eliminates their significance to interpret skeletal pathologies related with mantle damage (De Baets et al. 2015b). However, comparisons with other shelled molluscs like bivalves and gastropods help to interpret the parasitic nature of these structures and their potential culprits (Keupp 2012; De Baets et al. 2015b; Fig. 7.1). We herein assign structures to four categories according to their association with parasitism (compare Vinn and Wilson, 2021). Category 1 refers to structures where parasitism is the most plausible cause and negative effects on growth are evident in multiple specimens. Category 2 refers to specimens where such effects have so far not been unequivocally been demonstrated, but where similar structures are attributed to parasitism in modern organisms. Category 3 refers to cases where the pathologies indicate to have a negative effect on its host, but their relationship with parasitism is unclear. Category 4: The structure does not reliably indicate definite harm to the host and is unlikely related to parasitism.

7.3  P  athologies Attributed to Parasitism in Externally Shelled Cephalopods The main shell pathologies, which have been linked with parasitism, include blister pearls, volume-changing pathologies, symmetropathologies, disturbances in apertural shell growth and pathological gigantism. Parasitism has also been suggested for peculiar cases of other types of pathologies in the absence of external injuries, although these interpretations leave more room for speculation. Epizoa might also result in pathological specimens which should not be confused with parasitism. We will now discuss these structures and their potential relationship with parasitism in greater detail.

7.3.1  Blisters and Pits Shell concretions (without obvious evidence for external injuries) have often been attributed to parasitism in bivalves (Huntley and De Baets 2015). Hengsbach (1996) introduced the term forma aegra concreta for such cases in externally shelled

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cephalopods. Analogous to cephalopods, Keupp (2012, p. 226–227) assigned blisters described for modern mytilids (Götting 1979) as forma aegra concreta. Keupp (1987) was the first to provide evidence for blister pearls in ammonoids. He documented specimens of Dactylioceras where the depression in the internal mould coincides with a blister pearl, which contained shell material overgrowing a largely hollow (now sparitic) centre which contains a structure reminiscent of a bivalve shell (Fig.  7.2a–d). Blister pearls have also been reported from extant (Landman et  al. 2001; Fig.  7.1b) and extinct nautiloids (Kieslinger 1926; Mironenko 2018; Fig. 7.4). These can, however, only be confidently identified when shell material is preserved. There are additional instances of pits with similar shape and dimensions in internal moulds of externally shelled cephalopods, which have traditionally been suspected to correspond to blister pearls (Kieslinger 1926; Kirchner 1927; House 1960; Chlupáč and Turek 1983; Stridsberg and Turek 1997; Manda and Turek 2009; Turek and Manda 2010; De Baets et al. 2011; Mironenko 2016). Particularly deep isolated pits in ammonoids and nautiloids have been suggested to correspond to imprints of blister pearls (Kirchner 1927; Mironenko 2016, 2018; Turek and Manda 2016). Such pits can be traced back to the Silurian (Turek and Manda 2016), but it is probably only a matter of time until they are also reported in older cephalopods. In addition to a deeper pit in one specimen of Kachpurites fulgens, Mironenko (2016) reported groups of smaller elongated pits in various specimens of this ammonoid species (Fig. 7.2e, f). These pits correspond with deflections of shell material and growth lines (e.g. actual depressions in the shell) and therefore not blister pearls. However, in the absence of preserved shell layers, these pits can be easily confused with imprints of blister pearls on the internal mould. Mironenko (2016) attributed them to parasitic epizoans located at a flexible unmineralized part of the periostracum in the apertural region of the growing ammonite shell. Turek and Manda (2016) suggested that both pit types were also present in Ophioceras and potentially other externally shelled nautiloids (Fig. 7.4). As the blister pearl (or in multiple their putative imprints) is not associated with remains of parasitic organisms, their parasitic nature cannot be proven. These structures are therefore assigned to category 3 as parasites (in the absence of external injuries) represent the most plausible explanation. Nevertheless, it should be noted that in modern bivalves not all blister pearls are a sign of parasitic infestation, since they can form around inorganic particles, such as grains of sand, which are accidentally caught between the mantle and the shell wall (Newell 1969). It cannot be ruled out that inorganic particles or organic debris, accidentally got into the body chamber, could have been a reason for blister pearl formation in externally shelled cephalopods. An anecdotical example is a recently discovered macroconch of Kepplerites galilaeii with a blister pearl in the body chamber recovered from the Lower Callovian deposits of Znamenka locality (Central Russia: Keupp and Mitta 2013). This blister pearl contains a bivalve shell (Fig. 7.3a–c). Although the blister pearl accidentally opened during excavation and only one valve of the bivalve partially survived, the shape of the cavity in the blister pearl suggests that initially there was a whole bivalve shell inside it. Whereas the shell has not been fully preserved and quite small, it can be tentatively identified as representative of the Astartidae. Astartidae are facultatively mobile, infaunal

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Fig. 7.2  Blister pearls in ammonites. (a, b) Blister pearls on internal moulds of Dactylioceras anguinum, Toarcian (Jurassic), Altdorf near Nürnberg (Germany), SHK PA-643, dm 59 mm (a), SHK PA-1696, dm  =  60  mm (b). (c) Polished surface through the 1.5  mm blister of specimen A. (d) Thin section through the 3 mm large blister of specimen B - note the structure reminiscent of a bivalved fossil. (e) Concave areas (pits) on the shell surface of the ammonite Kachpurites fulgens, specimen MSU 118/1 (see Mironenko 2016). Upper Jurassic (Upper Volgian), Central Russia, Moscow region, Eganovo locality. These pits are not related with blister pearls, but may be confused with them, especially on the internal moulds (MSU = Moscow State University Museum). (f) Ventral view of the body chamber of Upper Jurassic (Upper Volgian) ammonite Kachpurites fulgens with a large imprint of a blister pearl, specimen MSU 118/6. Scale bar = 1 cm

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Fig. 7.3  Kepplerites galilaeii with blister pearl, Lower Callovian (Jurassic), Kostroma region (Russia), Znamenka locality: (a) Overview of the specimen showing the position of the blister pearl. (b) Close-up of the astartid contained with the pearl. (c) Counter part of the specimen with arrow showing the position of the blister pearl

suspension feeders (Zakharov 1970) and there are no parasitic forms among them today (Skawina 2021) but this might have been different in the past. This suggests that the bivalve shell could have accidentally ended up in the ammonoid body chamber during feeding at the seabottom—although the reason for it is not clear at the moment. Thus, this case highlights that some of cephalopod blister pearls are potentially not associated with parasitism and could be related to a variety of other causes. A peculiar type of serially arranged pits was first described by House (1960). In his honour, Davis and Mapes (1999) dubbed them Housean pits. These pits on internal moulds have been studied in detail by De Baets et  al. (2011, 2013a, 2013b, 2015b) and are commonly repeated episodically and/or arranged in pairs or series and were reported from multiple ammonoid taxa (Chlupáč and Turek 1983; Klug 2002a; Ebbighausen et al. 2011; Rakociński 2012; De Baets et al. 2015b; Pohle and Klug 2018; Fig. 7.5). Interestingly, they are absent from other similarly preserved specimens belonging to the same species from the same locality or entirely absent in those deriving from other localities (e.g. Ivoites schindewolfi in the Eifel mountains as opposed to the Hunsrück: De Baets et al. 2013a). The fact that they are also absent from other common taxa from the same localities or time intervals suggests a certain amount of host specificity in addition to local environmental controls (De

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Fig. 7.4  Nautiloids with blister pearls. (a) Ophioceras with deep ventral pit. (b, c) Ophioceras with anomalous suture and rib pattern linked with pits (A–C from Turek and Manda 2016). (d) Peismoceras pulchrum with lateral pit (from Turek and Manda 2010). (e) Pomerantsoceras pollux anomalous suture linked with pits (Manda and Turek 2009). (f) Cyclopoceras with single deep pit just below the muscle attachment area (from Mironenko 2018). Scale bar = 1 mm

Baets et al. 2011, 2015b). Most types of pits lie at the back of the body chamber—a position deep in the soft tissues consistent with a parasitic infestation and therefore assigned to category 3. In some species, it has been evidenced that these correspond with blister pearls and overgrown organic tubes (De Baets et al. 2011) which are here assigned to category 2. The identity of the parasitic organisms is unknown, but likely these do not belong to flatworms (De Baets et al. 2015a; Leung 2017, 2021), which have commonly been identified and implicated in superficially similar structures in bivalves (Lauckner 1983; Huntley and De Baets 2015). The fact that these pits are serially arranged might suggest a repeated infestation with parasite life stages and/or repeated encapsulation of parasite material. However, in early ammonoids, similar paired and serially repeated pits are found near the aperture of completely preserved body chambers suggesting that they formed at the anterior part of the body chamber (De Baets et al. 2011). The structures (named Opitzian pits by De

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Fig. 7.5  Morphology and distribution of Opitzian (type 4) and Housean (types 1–3) pits known from Devonian ammonoids (modified from De Baets et al. 2011). (C) Ivoites opitzi, HS 371, early Emsian, middle Kaub Formation (Hunsrück Slate), Bundenbach, Germany. (D) Sobolewia nuciformis, R.08459, Givetian, Redjel Iamrad, Algeria. (E) Subanarcestes sp., Eifelian, Erg El Djemel, Algeria (after House 1960). (F) Afromaenioceras sulcatostriatum, PIMUZ 28592, Givetian, Jebel Ouaoufilal, Morocco. (G) Sobolewia aff. nuciformis, R.08459, Givetian, Pentonwarra Rd., Trevone, UK (after House 1960). (H) Anarcestes sp., L19725, late Emsian, Koněprusy, Czech Republic (after Chlupáč and Turek 1983). (I) Crispoceras tureki, PIMUZ 28591, Eifelian, Jebel Ouaoufilal (Morocco). (J) Anarcestes sp., Eifelian, Wissenbacher Schiefer, Germany (after House 1960). (K) Anarcestes sp., PIMUZ 28581, late Emsian, Jebel Mech Agrou, Morocco. (L) Anarcestes latissimus, PIMUZ 1971-293, late Emsian, Hassi Moudaras, Morocco. (M) Sellanarcestes cf. ebbig hauseni, PIMUZ 28582, Emsian, Jebel Ouaoufilal, Morocco. (N) Sellanarcestes ebbighauseni, GPIT 1871-171, Emsian, northern Jebel Amessoui, Morocco, from Klug (2002a). (O) Sellanarcestes neglectus, GPIT 1871-285, Emsian, southern Jebel Mech Agrou, Morocco (from Klug 2002a)

Baets et al. 2013a, 2013b) are not comparable to inorganic conellae (diagenetic calcitic structures) in size and shape with apices pointing inward instead of outward (House 1960, see also Hoffmann et al. 2019). Similarities in spacing and host specificity as well as their association with mantle damage suggest that Opitzian pits (Fig. 7.5) might have similar causes like Housean pits sensu stricto (De Baets et  al. 2013b). So far, they have not been recovered from other localities or from specimens showing shell preservation, so that further research is necessary to confirm their putative parasitic nature and association with blister pearls rather than shell deflections or other structures. The occurrence of such pits also in the phragmocone chambers excludes a simple post-mortem infestation as explanation. Kidney-shaped pits in the middle of the venter associated with the most posterior point of the hyponomic sinus of their growth (Klug 2001; De Baets et al. 2011) are probably not of parasitic origin and are not further considered herein. Some pearls overgrow an organic tube which warrants their assignment to category 2, but in most cases their parasitic nature is plausible but not proven and therefore they are assigned to category 3.

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Fig. 7.6  Examples of different pathologies attributed to parasitic infestations with various degrees of certainty from the Devonian to Cretaceous (modified from Keupp 2012; unless stated otherwise):

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7.3.2  Volume-Enlarging Pathologies Temporarily increased shell volume and changes in ornamentation have been linked with parasitism by Keupp (1976). Initially, such cases in ammonoids were described as forma aegra inflata by Keupp (1976). Since the work of Kröger (2000), at least two main types have been distinguished: shell volume-enlarging pathologies (forma aegra inflata) and ornamentation-enlarging pathologies (forma aegra augata Kröger 2000; Fig. 7.6a, b). Most authors have reasonably attributed these to temporary swellings to mantle tissue infections and infestations caused by parasites (Keupp 1976, 2000, 1976, 2000; Hengsbach 1979, 1991a, 1996; Kröger 2000). Further comparative studies on extant bivalves, gastropods or other shelled molluscs are necessary to corroborate this interpretation. Keupp (1976, 2000) documented a specimen of Amoeboceras in which the crenulated keel temporally and progressively developed several large protuberances, which he attributed to a short-term infestation of the ventral apertural mantle tissue by parasites. Keupp (1984, 1997, 2000) suggested that this could also explain a similar phenomenon in a Dactylioceras in which the ribs suddenly and progressively developed into large shovel-like bands on the venter, which subsequently returned back to normal ribs (f.a. augata). Fernández-López (1987, pl. 1, Fig. 1) figured a specimen of Bajocisphinctes with a similar pathology, which can be attributed to the struggle between ammonoid and parasite (Hengsbach 1996). The Fig. 7.6 (continued) (a) Amoeboceras alternans with progressive enlargement of the ventral ornamentation (forma aegra augata Kröger 2000), Oxfordian (Jurassic), Kucha near Hersbruck (Germany), SHK PA-785, dm 12 mm. (b) Quenstedtoceras leachi with a conspicuous, temporary bulbous swelling of the ventral shell and ornamentation (forma aegra augata, Kröger 2000), Callovian (Jurassic), Dubki near Saratov (Russia), SHK PA-20114, dm 58 mm. (c) Upper Callovian (Middle Jurassic) ammonite Quenstedtoceras lamberti with a large bulbous swelling of the shell (forma aegra inflata). Saratov region (Russia), Dubki locality. Collection of the Geological institute of RAS, AM-D 34. (d) Dactylioceras athleticum with a progressive development of shovel-like ribs (forma aegra augata, Kröger 2000), Kimmeridgian (Jurassic), Hartmannshof (Germany), SHK PA-1871, dm 60 mm. (e, f) Pleuroceras spinatum with a unilateral thickening of the body chamber resulting in a significant left-right asymmetry of the whorl section, SHK PA-5170, Pliensbachian (Jurassic), Unterstürmig (Germany), dm 41 mm. (g, h) Hildoceras bifrons showing multiple oscillations of the keel around its normal ventral position (forma aegra undaticarinata), SHK PA-6245, Toarcian (Jurassic), Grand Causses (France), dm 23 mm. (i, j) Cleviceras elegans with Morton’s syndrome (sensu Landman and Waage 1986), SHK PA-543, Toarcian (Jurassic), Altdorf near Nürnberg (Germany), dm 55 mm. (k) Pseudosageceras multilobatum with Morton’s syndrome (sensu Landman and Waage 1986), SHK PA-9204, Early Triassic, Vikinghøgda south of Sassendalen (Spitzbergen), dm 34  mm. (l) Upper Oxfordian (Upper Jurassic) ammonite Amoeboceras alternoides with an oscillated keel (forma aegra undaticarinata). Moscow region (Russia), Markovo locality. Collection of the geological institute of RAS, AM-Ma 18. (m) Amoeboceras sp. with a progressive asymmetric shift of the keel (forma aegra juxtacarinata, Hölder 1956; similar to the case described by Rieber (1963)), SHK PA-786, Oxfordian (Jurassic), Scarborough (United Kingdom), dm 20 mm. (n) Latanarcestes noeggerathi with an eccentrical position of the external lobe (forma aegra juxtalobata, Hölder 1956), Emsian (Devonian), Tafilalt (Morocco), dm 27 mm. Scale bar = 1 cm

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increase in development of ornamentation can lead to a polygonal outline in rare specimens (Keupp 2012). However, it should not be confused with other types of pathologies resulting in a polygonal shape linked to possible endogenic causes (forma aegra polygonia sensu Hüne and Hüne 2006) or taxa where a polygonal whorl is normal and all specimens have it (e.g. triangular Soliclymenia from the Late Devonian: Korn et  al. (2005b) or the tetrangular Entogonites from the Carboniferous: Korn et al. (2005a)). Single swellings reminiscent of forma aegra augata have in the meantime been described from the Triassic (Arcestes) and Jurassic (Pleuroceras, Quenstedtoceras, Orthosphinctes). Keupp (2012) suggested that the normal ornamentation surrounding these structures indicates that the mantle tissue at the apertural margin was probably not infected. The forma aegra inflata should be restricted to conspicuous, temporary bulbous swellings of the shell behind the aperture, which are typically associated with the regeneration of external injuries (Kröger 2000; Keupp 1995, 2006; Keupp 2012; Fig. 7.6). They have become known from a wide variety of taxa (Lehmann 1975; Keupp 1976, 1995, 2000, 2006; Kröger 2000; Hengsbach 1996) from the Early to Late Jurassic (e.g. Dactylioceras, Pleuroceras, Rehmannia, Divisosphinctes, Orthosphinctes) and the Early to Late Cretaceous (e.g. Baculites, Discoscaphites, including Jeletzkytes according to Landman et  al. 2010, Hoploscaphites and Ptychoceras). The swellings are mostly smooth indicating that the mantle tissue at the aperture was not involved in their formation, although in rare cases, damages to the apertural mantle tissue might have resulted in phenomena similar to forma aegra augata during further growth. Such temporary swellings were first figured in a Dactylioceras by Lehmann (1975), which he related to the mantle protruding considerably outside of the shell after some injuries behind the aperture. Keupp (2012) pointed out that Lehmann’s explanation would be rather unlikely because of the consistency of the mantle musculature as well as the offset between the injuries and the bulbous swellings. According to Keupp (1976, 1995, 2000, 2006, 2012), the temporarily exposed mantle tissue (as a consequence of an injury) was more prone to infection and infestation by parasites, thus resulting in the temporary swelling. Keupp (1995, 2012) described additional volume-increasing phenomena in ammonoids. They correspond to a gradual “thickening” of one side of the whorl resulting in a significant left-right asymmetry of the whorl section, which has so far only been reported in Pleuroceras (Early Jurassic) and Hoploscaphites (Late Cretaceous). Keupp (1995, 2012) interpreted these as the temporary volume enlargement of the soft tissue along one side of the body in response to a parasitic infestation rather than a tumour-like swelling. This is consistent with the fact that true tumours or neoplasia are considered rare in extant cephalopods (Sparks 1972; Scimeca 2012; Gestal et al. 2019a). Neoplasia in cephalopods (Gestal et al. 2019a) has been attributed to a variety of causes including aquarium maintenance, xenobiotics, infectious viruses, bacteria or parasites. Infestation with a pathogen is most plausible to explain the volume-enlarging pathologies and the negative effect on their host is clearly documented; they merit assignment to our category 3.

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7.3.3  Disturbances in Apertural Shell Growth Kröger (2000) introduced the term forma aegra umbilicata for pathologies, where the shell formation is delayed leading to the progressive development of a deep slit-­ shaped recess (and ribbing vertices) in the apertural margin of rare specimens in the absence of external injuries. Such pathologies were first described in Dactylioceras where the shell formation is delayed near the umbilicus (Keupp 1979), but is more variable or develops in other positions in Epivirgatites and Quenstedtoceras (Keupp 2012). These should not be confused with muscle scars, which are usually restricted to the back of the body chamber (whereas some of soft-tissue attachment areas are located not far from the aperture: see Mironenko 2014) or similar structures developing in association with external injuries (forma aegra verticata, forma aegra semiverticata) in similar positions (Keupp and Hoffmann 2015; De Baets et al. 2015b). As slit-shaped recesses similar to those in ammonoids have been attributed to parasitic infestations by intermediate stages of parasitic flatworms in extant gastropods (Pila sp.: Keupp 2000, Keupp 2012; De Baets et al. 2015b; Fig. 7.1a), these structures can therefore be confidentially assigned to our category 2. The pathologies are best known from the Early Toarcian of Altdorf (southern Germany) where up to 5% of Dactylioceras display these structures, but they are absent from all other ammonoid taxa (Harpoceratidae, Hildoceratidae, Phylloceratidae, Lytoceratidae). This indicates that these pathologies and also their culprits are host specific. In addition, Keupp (2012) attributed their high prevalence to a regionally limited population of these parasites. As these structures are rare in dactylioceratids in other regions, their ecology (mode of life, predator-prey relationships) or particular environmental factors in this region might also have augmented their infection risk. Mironenko (2016) described another type of disturbance in apertural shell growth, probably caused by parasitism. This new type of shell malformation consists of small (less than 1 mm) elongated pits, arranged in groups on the surface of the shells and concentrated near the terminal aperture of Late Jurassic ammonites Kachpurites fulgens (Fig. 7.2e, f). The examination of the pits revealed no signs of drillings or healing of punctures. The shell layers in the pits are bent downward without changing their thickness. Deformed growth lines on the shell surface are often associated with these pits suggesting the presence of epibionts, likely parasites at the aperture. They may have colonized the surface of a flexible unmineralized part of the periostracum in the apertural region. This could explain the deformation of the growing shell edge. Although phosphatized remnants of some tissues are preserved in some pits, their poor preservation did not allow the identification of its producers. Some clusters of pits on the surface of the same shell are very similar to each other and probably their formation could have been provoked by the same animals, which might have been able to follow the growing shell edge (see Mironenko 2016: Fig. 12). If this conclusion is correct, this is the first fossil example of ectoparasites that live on the exterior surface of their externally shelled cephalopod hosts (as opposed to endoparasites, which live in internal organs or tissues of cephalopods). The prevalence of pits on Kachpurites is low: they were found on 15 shells of 1133

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studied specimens (1.23%), but in all infected specimens, the pits are very numerous. The negative effect on the host is clearly established, but the lack of modern analogues or clearly identifiable parasitic remains places these in our category 3.

7.3.4  Symmetropathologies Hengsbach (1991a) introduced the term “symmetropathy” to refer to pathological asymmetries or deviations from the plane of bilateral symmetry. Several symmetropathologies in both the phragmocone and body chamber in the absence of external injuries or epizoa have been attributed to parasitism with various degrees of certainty (Hengsbach 1991b, 1996; Keupp 2012; De Baets et al. 2015b). These include asymmetry in the position of the keel (forma aegra juxtacarinata: Fig. 7.6m) or the entire shell (Morton’s syndrome: Fig. 7.6h–k) as well as asymmetry of the siphuncle and ventral lobe (forma aegra juxtalobata). Symmetropathologies in the Shell Heller (1958) described a Pleuroceras with an asymmetrical keel that shows multiple oscillations and only normalizes towards the end of the body chamber. Heller (1958) dubbed this phenomenon forma aegra undaticarinata. It can probably be explained by a temporary parasite infestation of the ventral mantle epithelium (Keupp 2012). This is supported by the fact that it can be associated with a flattening and asymmetrical appearance of the keel crenulation, which is reminiscent of pathologies dubbed forma aegra cicatricocarinata (Heller 1964) caused by injuries to the ventral mantle epithelium as well as unilateral temporary disappearance of the groove surrounding the keel (Fig.  7.3). This phenomenon is known from the Amaltheidae and from other groups with keeled or acute venters including the Harpoceratidae and Hildoceratidae (Keupp 2012). The few published quantitative analyses (Keupp 2012) show a ten times higher prevalence of this pathology in Pleuroceras than in Hildoceras (see Table 7.1). A high prevalence of forma aegra undaticarinata (11.6%) was found in Late Oxfordian Amoeboceras alternoides from Central Russia (Mironenko 2017). In these ammonites, multiple keel oscillations, which suddenly appear and also suddenly stop, occurred at different ontogenetic stages, starting from early whorls up to the terminal body chamber. Mironenko (2017) suggests that these oscillations might not necessarily be related with parasitism, but likely were caused by minor mechanical failures during shell growth: the mantle edge and the periostracum on the pointed tip of the ventral rostrum could have slightly shifted due to abrupt movement of an ammonite. The keel can maximally deviate about 90° from the planispiral position and if it exceeds this value, it can result in one or multiple re-establishments of the keel and an associated chaotic, zigzag pattern of the ornamentation (forma aegra chaotica of Keupp 1977).

Anarcestes cf. latissimus Anarcestes crassus

Anarcestes sp.

Anarcestes sp.

Sellanarcestes draensis Sellanarcestes neglectus Sellanarcestes neglectus Sellanarcestes solus

Anarcestes latissimus

Anarcestes ssp.

Housean pits

Housean pits

Housean pits

Housean pits

Housean pits (type 1)

Housean pits (type 1)

Housean pits

Housean pits

Housean pits

Housean pits

Taxon ?Werneroceras sp.

Type Housean pits

2

3

3

22

59%

18

–

–

72%

–

–

–

–

–

–

–

–

Chlupáč and Turek (1983) Klug (2002b), but see Ebbighausen et al. (2011) Klug (2002a), Pohle and Klug (2018) De Baets et al. (2011)

3

3

Ebbighausen – et al. (2011) Klug (2002a) –

–

–

–

–

Devonian

Devonian

Devonian

Devonian

Devonian

Devonian

Devonian

Devonian

Devonian

Devonian

Sample Prevalence size Period – – Devonian

3

Category Reference 3 Chlupáč and Turek (1983) 3 Chlupáč and Turek (1983) 3 Ebbighausen et al. (2011) 3 Chlupáč and Turek (1983) 3 House (1960)

Table 7.1  Compilation of pathologies attributed to parasitism

Upper Emsian

Upper Emsian

Upper Emsian

Upper Emsian

Upper Emsian

Upper Emsian

Upper Emsian

Upper Emsian

Upper Emsian

Upper Emsian

Epoch Eifelian

Morocco

Hamar Laghdad

Morocco

Bohemia

Morocco

Oufrane

Germany

Bohemia

Oufrane

Bohemia

Region Bohemia

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Group Blisters/pits

External (ammonoid) (continued)

External (ammonoid)

Shell External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid)

Type Housean pits (type 1) Housean pits (type 1) Housean pits (type 1) Housean pits (type 1) Housean pits (type 2) Housean pits (type 2) Housean pits (type 2) Housean pits (type 2) Housean pits (type 2) Housean pits (type 2) Housean pits (type 2) Housean pits (type 2) Housean pits (type 2?) 1.5%

De Baets et al. (2011) De Baets et al. (2011) De Baets et al. (2011) Rakociński (2012) House (1960) De Baets – et al. (2011) House (1960) – Göddertz – (1987) Chlupáč and – Turek (1983)

3

3

3

3

Subanarcestes

Subanarcestes cf. marhoumensis Subanarcestes marhoumensis Holzapfeloceras sp. III

2

3

Crispoceras tureki

Felisporadoceras

3

Sobolewia nuciformis 3

3

–

6.3%

–

–

–

–

Sellanarcestes ebbighauseni Afromaenioceras sulcatostriatum Anarcestes

–

–

–

–

–

48

–

–

200

–

ca. 50%

Sellanarcestes

Devonian

Devonian

Devonian

Devonian 

Devonian

Devonian

 Devonian

Devonian

Devonian

Devonian

Devonian

Eifelian

Eifelian

Eifelian

Eifelian

Givetian

Famennian

Eifelian

Emsian

Givetian

Upper Emsian

Emsian

Upper Emsian

101

33%

Sellanarcestes

Devonian

Epoch Upper Emsian

Sample Prevalence size Period 30% 30 Devonian

Taxon Anarcestes ssp.

Category Reference 3 Pohle and Klug (2018) 3 Chlupáč and Turek (1983) 2 De Baets et al. (2011) 3 Klug (2002a)

Table 7.1 (continued)

Bohemia

Algeria

Great Britain

Morocco

Holy Cross Mountains Great Britain

Morocco

Morocco

Morocco

Morocco

Morocco

Region Hamar Laghdad Bohemia

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Group Blisters/pits

Shell External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid)

Keupp (1979, 5% 2012) Keupp (2012) –

3

2

2

Kachpurites fulgens

Dactylioceras

Epivirgatites sp.

1.32%

–

–

1133

14

14%

Pits sensu Mironenko (2016) Forma aegra umbilicata Forma aegra umbilicata

3

Ivoites schindewolfi

Opitzian pits

20

45%

3

Ivoites opitzi

–

– 1133

–

–

0.09%

575

0.2%

Mironenko (2016) De Baets et al. (2013a, 2013b) De Baets et al. (2013a, 2013b) Mironenko (2016)

–

–

3

21

4.8%

Jurassic

Jurassic

Jurassic

Devonian

Devonian

Jurassic

Devonian

Triassic

Upper Devonian Lower Jurassic Cretaceous

Sample Prevalence size Period – – Devonian

Kachpurites fulgens

Taxon Category Reference Sobolewia nuciformis 2 Petter (1959), De Baets et al. (2011) Cyclopoceras 3 Mironenko abundans (2018) Dactylioceras 3 Keupp (1987) anguinum Endemoceras sp. 3 Richter (2002) Ceratites compressus 3 Kirchner (1927) Cheiloceras sp. 3 Keupp (2012)

Isolated blister pearl Isolated blister pearl Isolated blister pearl Isolated blister pearl? Isolated blister pearl? Isolated blister pearl? Opitzian pits

Type Housean pits (type 3)

Moscow

Nehden

Muschelkalk

Hannover

Altdorf

Krutoye

Region Algeria

Tithonian

Toarcian

Tithonian

Moscow

Altdorf

Moscow

Lower Emsian Hunsrück

Lower Emsian Hunsrück

Tithonian

 -

Anisian

Hauterivian

Toarcian

Frasnian

Epoch Givetian

Disturbances in shell growth Disturbances in shell growth

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Blisters/pits

Group Blisters/pits

External (ammonoid) External (ammonoid) (continued)

External (ammonoid)

External (ammonoid)

External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid) External (ammonoid)

Shell External (ammonoid)

4

4

4

Branneroceras branneri

Cancelloceras huntsvillense

Cymoceras cracens

Diaboloceras neumeieri

Diaboloceras varicostatum

?Pathological gigantism

?Pathological gigantism ?Pathological gigantism

?Pathological gigantism

4

4

4

Axinolobus quinni