Comparative Anatomy of the Gastrointestinal Tract in Eutheria I: Taxonomy, Biogeography and Food: Afrotheria, Xenarthra and Euarchontoglires 9783110527735, 9783110526158

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Handbook of Zoology Mammalia Comparative Anatomy of the Gastrointestinal Tract in Eutheria Taxonomy, Biogeography and Food Volume 1: Introduction, Afrotheria, Xenarthra and Eucharchontoglires

Handbook of Zoology Founded by Willy Kükenthal Editor-in-chief Andreas Schmidt-Rhaesa

Mammalia Edited by Frank E. Zachos

DE GRUYTER

Comparative Anatomy of the Gastrointestinal Tract in Eutheria

Taxonomy, Biogeography and Food Volume 1: Introduction, Afrotheria, Xenarthra and Eucharchontoglires Peter Langer

DE GRUYTER

Author Peter Langer Institut für Anatomie & Zellbiologie Justus-Liebig-Universität Aulweg 123 D-35392 Giessen [email protected] Scientific Editor Frank E. Zachos Naturhistorisches Museum Wien Säugetiersammlung Burgring 7 A-1010 Wien, Österreich

ISBN 978-3-11-052615-8 e-ISBN (PDF) 978-3-11-052773-5 e-ISBN (EPUB) 978-3-11-052707-0 ISSN 2193-2824 Library of Congress Cataloging-in-Publication Data A CIP catalogue record for this book is available from the Library of Congress. Bibliografic information published by the Deutsche Nationalbibliothek The Deutsche Nationalbibliothek lists this publication in the Deutsche Nationalbibliografie; detailed bibliographic data are available in the Internet at http://dnb.dnb.de. © 2017 Walter de Gruyter GmbH & Co. KG, Berlin/Boston Typesetting: Compuscript Ltd. Shannon, Ireland Printing and Binding: Hubert & Co. GmbH & Co. KG, Göttingen ∞ Printed on acid-free paper Printed in Germany www.degruyter.com

To the memory of my parents

Motto: “Der derzeitige Wissenschafts- und Universitätsbetrieb leidet nicht nur unter einer bisweilen schon ins Absurde gehenden Spezialisierung, sondern auch unter dem Verlust der historischen Kontinuität” (F. M. Wuketits, 2015).

Comparative Anatomy of the Gastrointestinal Tract in Eutheria Taxonomy, Biogeography and Food Volume 1: Introduction, Afrotheria, Xenarthra and Eucharchontoglires (ISBN 978-3-11-052615-8) Volume 2: Laurasiatheria, General Discussion (ISBN 978-3-11-056047-3)

Preface In an excellent biography, dealing with Alfred Wegener and his theory of continental drift, M. T. Greene1 compares scientific textbooks, lectures and monographs with Handbücher (sic), handbooks, and characterizes these publications as reference volumes that contain “material deemed certain” (page 209). This statement, based on literature from the early twentieth century, is also true today and writing a handbook on the comparative anatomy of the digestive tract in eutherian mammals represents a promising task: It is helpful to compile available information from time to time, to generalize and to present overviews. Gaps in our knowledge can be identified; they can be enumerated and should hopefully stimulate future research. Fruitless extrapolations can thus be avoided, but still unanswered problems will be identified and can represent valuable incentives for future studies. A balanced compilation of modern and old publications will allow new insights. When recent as well as older publications are considered, a handbook becomes a “historical” reference source. The present book will show that half-forgotten publications are often remarkably informative. An extensive list of references will help readers to ask their own “progressive” scientific questions, for example on evolutionary aspects. This book deals with the anatomy of the stomach, small intestine, caecum and colon of most eutherian orders and suborders. In studies of the gastrointestinal tract anatomy and physiology are interwoven. Information on form and function of organs of digestion in eutherians is discussed under comparative-anatomical aspects, as well as information concerning biology, taxonomy, biogeography or food. However, anatomical questions will form the crucial points of this book. The availability and quality of anatomical data on the gastrointestinal tract between eutherian orders are extremely unbalanced, a fact that influenced the production of this text. In many taxa there exists very limited anatomical information, but for species of economic importance a multitude of publications on form and function of the gastrointestinal tract is available. These cases include meat or milk production, work capability, speed (horses, camels and dogs), even aggressiveness (some breeds of dogs) and are enforced during domestication. Detrimental effects on stores of human resources (e.g., rodents in granaries) also represent a centre of interest and are responsible for a great number of publications.

1 M. T. Greene (2015): Alfred Wegener. Science, Exploration and the Theory of Continental Drift. – Johns Hopkins University Press: Baltimore.

Although a general discussion of the entire digestive tract might be useful for functional studies, different sections of the post-oesophageal tract are handled separately in this handbook to enable readers to identify gaps in the availability of data in taxa that have been investigated only superficially. While using this handbook, the reader may criticise that the number of illustrations is unbalanced in different chapters. The present author attempted to obtain permission to use illustrations that were originally published by earlier researchers, but some publishers requested excessive sums to grant permission to use their illustrations. Most of these illustrations, originally integrated into a previous draft of the text, have been deleted from this handbook. It is self-evident that all sources used in this book are cited with complete reference, and the present author fully acknowledges that he uses and discusses the results of other researchers. The high-price-policy of some publishers is, in fact, decidedly anti-scientific. Permissions were granted by Acad. Sci. South Africa, Acta Vet. Beograd, Akadémiai Kiadó, American Medical Assoc., Bill Breed, Cambridge University Press. Canadian Science Pub., Ciéncia Rural, Cornell University, CSIRO Publishing, De Gruyter, Elsevier, Illinois Academy of Sci., Julia Boonzaier, Inst. Cetacean Res., Internat. J. Morphology, Japanese Assoc. of Anatomists, Marcus Clauss, Marlène Razanahoera Rakotomalla, Mammal Soc. of Japan, Nathalie Crevier, Okajimas Folia Anat. Japonica, Oxford University Press, Polish Acad Sci., Rangolf Hoffmann, Robert L. Snipes, Roy. Belgian Soc. of Natural Sci., S. A. Assoc. of Animal Sci., S. A. Wildlife Mgmt. Assoc., Sanet Kotzé, Salomé OettliRahm, Taylor & Francis, University of Michigan, University of Kansas, University of Stellenbosch. The present author hopes that comparative anatomists, mammalogists, physiologists, nutritionists, ecologists, taxonomists and other readers interested in the history of research in digestive systems may find this book useful. The number of people who helped the author to produce this text is innumerable and cannot be listed here. However, three people gave important technical help: the editor of the section on Mammalia of the “Handbook of Zoology”, Privatdozent Dr. Frank Zachos, Naturhistorisches Museum Wien, Austria, made the publication of my text possible. After my retirement Professor Dr. Wolfgang Kummer, Institut für Anatomie & Zellbiologie, Justus-Liebig-Universität Giessen, made a room available, where I could do literature research and

write. Dr. Mariusz A. Bromke of Verlag Walter de Gruyter, Berlin, painstakingly worked on the text I supplied and considerably improved it. He gave technical advice, patiently answered my often rather ignorant questions and always strived to produce an attractive book. My sincere

gratitude has to be expressed to the many unnamed colleagues, but especially, to the three above-mentioned gentlemen. Giessen, 2 August 2017

Contents of volume I Preface

vii

1 I Introduction 1 An appreciation of exemplary investigators – past and present 3 2 Outline of eutherian systematics 3 2.1 Definition and delineation of gut sections 4 2.2 Functional differentiations of gastrointestinal tract sections 5 2.3 General remarks on sections of the gastrointestinal tract 7 2.4 Food index and volume 7 Food quality eaten by eutherian taxa 2.5

9

61 II Afrotheria Description of the post-oesophageal digestive tract in the eutheria 63 1 Afrosoricida, Tenrecomorpha 63 1.1  Geographical distribution and types of food eaten by species of the four tenrecomorph subfamilies 63 1.2  Remarks on gastric and small intestinal, as well as on colon anatomy in Tenrecomorpha 64 2 Afrosoricida, Chrysochloridea 65 2.1  Type of food eaten by species of the two chrysochlorid subfamilies 65 2.2  Remarks on gastric and small intestinal, as well as on colon anatomy in Chrysochliridae 65 3 Macroscelidea 66 3.1  Type of food eaten by Macroscelidea 66 3.2  Remarks on gastric and small intestinal, as well as colon and caecum anatomy in Macroscelidea 67 4 Tubulidentata 68 4.1  Type of food eaten by Tubulidentata 69 4.2  Remarks on gastric and small intestinal, as well as colon and caecum anatomy in Tubulidentata 69 5 Hyracoidea 70 5.1  Types of food eaten by Hyracoidea 70 5.2  Anatomy of the stomach of Hyracoidea 71 Functional considerations related to the 5.3  stomach and other sections of the digestive tract of Hyracoidea 73

5.4  The small intestine, especially the duodenum of Hyracoidea 74 5.5  Colon and caecum of the Hyracoidea 75 5.6  Arterial supply of the caecum and of other parts of the digestive tract in Hyracoidea 77 5.7 Terminology of the digestive tract of Hyracoidea under special consideration of the caecum 77 5.8  Descriptive and functional anatomy of the caecum of Hyracoidea 78 6 Proboscidea 79 6.1  Introductory remarks 79 Food of elephants 6.2  80 6.3  Anatomy of the stomach of the Proboscidea 81 6.4  Functional considerations concerning the stomach of the Proboscidea 81 6.5  Anatomy of the small intestine of Proboscidea 82 6.6  Anatomy of the colon of Proboscidea 82 6.7  Anatomy of the caecum of Proboscidea 82 6.8  Functional considerations concerning the large intestine of Proboscidea 83 7 Sirenia 84 7.1  Introductory remarks 84 7.2  Food of Dugong dugon (living in salt water) 85 7.3  Food of Trichechus manatus (living in variable salinity) 86 7.4  Food of Trichechus inunguis (living in freshwater) 86 7.5  Food of Hydrodamalis gigas (marine and extinct) 86 7.6  Gastric anatomy in the Sirenia 86 7.6.1 Mucosal differentiations of the sirenian stomach 90 7.6.2 Mesenteria of the sirenian stomach 90 7.6.3 Arterial supply of stomach and ampulla duodeni 91 7.6.4 Functional remarks, emphasising the sirenian stomach and ampulla duodeni 92 7.7  Small intestine of the Sirenia 93 7.8  Colon anatomy in the Sirenia 93 Caecum anatomy in the Sirenia, as 7.9 described for Trichechus manatus, by Snipes (1984b) 94

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 Contents of volume I

7.9.1 Vascularisation of the caecum in Trichechus manatus, described by Snipes (1984b) 96 7.9.2 Transmission electron microscopy in Trichechus manatus, described by Snipes (1984b) 97 7.10  Remarks on functional aspects of the total post-oesophageal digestive tract in Sirenia 97 7.11  Final remarks on the Paenungulata (Hyracoidea + Proboscidea + Sirenia) 98 99 III Xenarthra Introductory remarks, Xenarthra in general 101 8 Cingulata 101 8.1  Systematics, phylogeny and physiology 101 8.2  Type of food eaten by Cingulata, Dasypodidae 102 8.3  Gastric anatomy of Cingulata, Dasypodidae 104 8.4  Anatomy of the small intestine of Cingulata, Dasypodidae 105 8.5  Anatomy of the colon of Cingulata, Dasypodidae 105 8.6  Anatomy of the caecum of Cingulata, Dasypodidae 105 9 Pilosa, Folivora 106 9.1  Introductory remarks 106 9.2  Food of the Pilosa, Folivora 107 9.3  Gastric anatomy of Pilosa, Folivora 108 9.3.1  Mesenteries of Pilosa, Folivora 112 9.3.2  Architecture of the gastric tunica muscularis in Bradypus sp. 114 9.3.3  Mucosal lining of the stomach 115 9.3.4  Blood vessels of the gastric area in Bradypus tridactylus 115 9.3.5  Concluding functional remarks on the stomach of the Pilosa, Folivora 116 9.4  Anatomy of the small intestine of the Pilosa, Folivora 117 9.5  Anatomy of the colon of Pilosa, Folivora, including remarks on the absence or presence of a caecum 117 10 Pilosa, Vermilingua 118 10.1  Introductory remarks, also considering fossil forms 118 10.2  Recent species 119 10.3  Food of the Pilosa, Vermilingua 119 10.4  Gastric anatomy of Pilosa, Vermilingua 120 10.5  Anatomy of the small intestine of Pilosa, Vermilingua 121

10.6  Anatomy of the colon of Pilosa, Vermilingua 122 10.7  Anatomy of the caecum of Pilosa, Vermilingua 122 123 IV Euarchontoglires 125 Introductory remarks 11 Scandentia 125 11.1 Food of Scandentia 126 11.2 Gastric anatomy of Scandentia 126 11.3 Anatomy of the small intestine of Scandentia 127 11.4 Anatomy of the colon of Scandentia 127 11.5 Anatomy of the caecum of Scandentia 127 11.6 Short remarks on digesta transit in Scandentia 130 12 Dermoptera 130 12.1 Introductory remarks 130 12.2 Food of Dermoptera 131 12.3 Gastric anatomy of Dermoptera 131 12.3.1 Arterial supply of the stomach in Cynocephalus volans (Schultz, 1972) 131 12.4 Anatomy of the small intestine of Dermoptera 131 12.5 Anatomy of the colon of Dermoptera 132 12.6 Anatomy of the caecum of Dermoptera 133 12.7 Functional remarks on the gastrointestinal tract in Dermoptera 133 13 and 14 Primates 133 General overview 133 13 Strepsirrhini (“wet-nosed” primates) 136 13.1 Introductory remarks 136 13.2 The food of Strepsirrhini 137 13.3 The stomach of Strepsirrhini 139 13.3.1 Gastric anatomy of Strepsirrhini 139 13.3.2 Internal lining of the strepsirrhine stomach 142 13.3.3 Functional remarks concerning the strepsirrhine stomach 142 13.4 General remarks on small and large intestines of Primates 143 13.4.1 Anatomy of the small intestine of Strepsirrhini 146 13.4.2 Anatomy of the colon of Strepsirrhini 147 13.4.3 Concluding remarks to the colon of Strepsirrhini 149 13.5 Anatomy of the caecum of Strepsirrhini 150 14 Haplorrhini (“dry-nosed” primates) 151 14.1 Introductory remarks 151 14.2 General remarks on food 151 14.2.1 Food of the Tarsiiformes, Tarsiidae 152



14.2.2

Food of the Simiiformes, Platyrrhini 152 14.2.3 Food of the Simiiformes, Catarrhini: Cercopithecidae 153 14.2.4 Food of the Simiiformes, Catarrhini: Hylobatidae and Hominidae 153 14.3 Anatomy of the stomach of Haplorrhini 153 14.3.1 Tarsiiformes and Simiiformes: Platyrrhini 153 14.3.2 Simiiformes: Catarrhini 154 14.3.2.1 Cercopithecoidea: Cercopithecinae 154 14.3.2.2 Hominoidea, Hylobatidae and Hominidae. Discussion of the mesogastria 154 14.3.2.3 Musculature of the gastric wall, mainly of the human stomach 156 14.3.2.4 Remarks on the histology of the tunica mucosa in the unilocular, mainly human, stomach 159 14.3.2.5 Remarks on vascularisation and innervation 160 14.4 Small intestine of the Haplorrhini 161 14.5 Colon of the Haplorhini 161 14.6 Caecum of the Haplorrhini 165 14.7 Appendix vermiformis in Primates 167 14.8 Cercopithecoidea: Colobinae (mainly dealing with the stomach) 168 14.8.1 Introductory remarks 168 14.8.2 Food of the Colobinae 168 14.8.3 Short account of previous publications on the macroscopic anatomy of the stomach in Colobinae 170 14.8.3.1 General subdivision and position of the colobine stomach 171 14.8.3.2 Form of the colobine stomach 174 14.8.3.3 Macroscopic and microscopic internal surface differentiations of the colobine stomach 177 14.8.3.4 Volumes of the stomach regions in Colobinae 178 14.8.3.5 Gastric blood vessels in Colobinae 179 14.8.3.6 Gastric mesenteries in Colobinae 180 14.8.3.7 Muscle architecture of the tunica muscularis 180 14.8.3.8 Superficial layer 180 14.8.3.9 Deep layer 180 14.8.3.10 Functional remarks on the stomach of the Colobinae 181 15 to 20 Glires, short overview 182 15 to 19 Rodentia 183 General remarks 183

Contents of volume I 

 xi

15 Sciuromorpha 185 15.1 General remarks 185 15.2 Food of the Sciuromorpha 186 15.3 Gastric anatomy of the Sciuromorpha 188 15.4 Small intestine of Sciuromorpha 189 15.5 Colon of Sciuromorpha 190 15.6 Caecum of Sciuromorpha 191 16 Castorimorpha 194 16.1 Introductory remarks 194 16.2 Food of the Castorimorpha 194 16.3 Gastric anatomy of the genus Castor 195 16.4 A few remarks on the castorimorph families Geomyidae and Heteromyidae 196 16.5 Small intestine of Castorimorpha 197 Colon of Castorimorpha 16.6 198 16.7 Caecum of Castorimorpha 198 17 Myomorpha 199 17.1 General remarks 199 17.2 Food of the Myomorpha 199 17.3 Gastric anatomy in the Myomorpha 201 17.3.1 Terminological remarks 201 17.3.2 General remarks on gastric form, mucosal lining and taxonomic relationships in the Myomorpha 202 17.3.2.1 Remarks on the stomachs of Dipodidae 204 17.3.2.2 Remarks on the stomachs of Nesomyidae 205 17.3.2.3 Remarks on the stomachs of Cricetidae 206 17.3.2.3.1 Subfamily Arvicolinae 206 17.3.2.3.2 Subfamily Sigmodontinae 207 17.3.2.3.3 Subfamily Cricetinae 208 17.3.2.3.4 Subfamily Neotominae 208 17.3.2.3.5 Subfamily Lophiomyinae 209 17.3.2.3.6 Subfamily Tylomyinae 209 17.3.2.4 Remarks on the stomachs of Muridae 210 17.3.2.5 Remarks on the stomach of Spalacidae 213 17.4 Small intestine of Myomorpha 214 17.5 Colon of Myomorpha 215 17.6 Caecum of Myomorpha 220 17.6.1 Muridae 220 17.6.2 Cricetidae, Genus Microtus 222 17.6.3 Cricetidae, Genus Ondatra 223 17.6.4 Caecum of Myomorpha, Cricetidae, Genus Mesocricetus 223 17.6.5 Caecum of Myomorpha, Cricetidae, diverse genera 224

xii 

 Contents of volume I

17.6.6 Caecum of Myomorpha, Spalacidae and Nesomyidae 225 17.6.7 Concluding remarks on caecal digestion 225 18 Anomaluromorpha 226 18.1 General remarks 226 18.2 Gastric anatomy of the Anomaluromorpha 226 18.3 Small intestine of Anomaluromorpha 227 18.4 Colon of Anomaluromorpha 227 18.5 Caecum of Anomaluromorpha 227 19 Hystricomorpha 228 19.1 General remarks 228 19.2 Form and function of the gastric region in Hystricomorpha 228 19.2.1 Infraorder: Ctenodactylomorphi 229 Family: Ctenodactylidae 19.2.1.1 229 19.2.2 Infraorder: Hystricognathi 229 African and Eurasian hystricognath families 229 19.2.2.1 Family: Bathyergidae 229 19.2.2.1.1 Food of some bathyergid species 229 19.2.2.1.2 Remarks on the gastric anatomy of some bathyergid species 229 19.2.2.2 Family: Hystricidae 230 19.2.2.2.1 Remarks on the gastric anatomy of some hystricid species, combined with short notes on food 230 19.2.2.2.2 Arterial supply of the stomach of Hystrix cristata 231 19.2.2.3 Family: Petromuridae 231 19.2.2.4 Family: Thryonomyidae 231 American hystricognath families 232 19.2.2.5 Family: Erethizontidae 232 19.2.2.6 Family: Chinchillidae 233 19.2.2.7 Family: Dinomyidae 233 19.2.2.8 Family: Caviidae 233 19.2.2.9 Families: Dasyproctidae and Cuniculidae 236 19.2.2.10 Family: Ctenomyidae 237 19.2.2.11 Family: Octodontidae 237 19.2.2.12 Family: Abrocomidae 239 19.2.2.13 Family: Echimyidae 239 19.2.2.14 Family: Myocastoridae 239 19.2.2.14.1 Food of the nutria (Myocastor coypus) 239 19.2.2.14.2 Anatomy of the nutria stomach 239 Caribbean hystricognath families 240 19.2.2.15 Family: Capromyidae 240 19.3 Hystricomorpha, small intestine 241 19.4 The colon of Hystricomorpha 241

247 Compilation of colonic differentiations Mesenteries of the rodent colon 248 Arterial supply of the rodent colon 250 Macroscopic configuration of the rodent colon 254 19.4.5 Differentiations of the colon wall in rodents 256 19.4.6 Macroscopically visible internal differentiations of the colon 260 19.4.7 Histological differentiations of the colonic internal lining 264 19.4.8 The colonic separation mechanism and colonic anatomy 266 19.5 Caecum of Hystricomorpha 268 19.5.1 The caecum of Bathyergidae 268 19.5.2 The caecum of Hystricidae and Erethizontidae 270 19.5.3 The caecum of Thryonomyidae 271 19.5.4 The caecum of Chinchillidae 271 19.5.5 The caecum of Caviidae 272 19.5.6 The caecum of Octodontidae 275 19.5.7 The caecum of Echimyidae 275 19.5.8 The caecum of Myocastoridae 275 20 Lagomorpha 276 20.1 Leporidae 278 20.1.1 General remarks 278 20.1.2 Food of the Leporidae 278 20.1.3 Coprophagy and caecotrophy, general remarks 280 20.1.3.1  Coprophagy and caecotrophy in Lagomorpha 280 20.1.3.2 Microbial population in the stomach of Oryctolagus cuniculus and its ontogenetic differentiation 281 20.1.4 Anatomy of the stomach of the genus Oryctolagus 281 20.1.4.1 Short remark on the arterial supply of the rabbit stomach 283 20.1.5 Anatomy of the stomach of the genus Lepus 283 20.2 Ochotonidae, general considerations 284 20.2.1 Food of the Ochotonidae 284 20.2.2 Gastric anatomy of the Ochotonidae 285 20.3 The small intestine in Lagomorpha 285 20.4 Colon configuration and arterial supply in Lagomorpha 285 20.4.1 Taeniae in the colon wall 292 20.4.2 Macroscopically visible internal differentiations of the colon in Lagomorpha 292 19.4.1 19.4.2 19.4.3 19.4.4

Contents of volume I 



20.4.3

Histology of the tunica mucosa in the colon of Lagomorpha 293 20.4.4 Functional differentiations in the colon of the rabbit 293 20.4.5 Mesenteries of the colon of the rabbit 294 20.5 Anatomy of the caecum of the Lagomorpha, especially the rabbit 294 20.5.1 Microbes in the caecum of lagomorphs 298 20.5.1.1 Hard and soft faeces, refection and caecotrophy in rabbits 298

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20.6 Anatomy of the caecum in hares and jackrabbits 301 20.6.1 Hard and soft faeces, refection and caecotrophy in hares 302 20.7 The caecum in Ochotonidae 302 20.7.1 General remarks 302 20.7.2 Anatomy of the caecum in pikas 302 Index

305

Contents of volume II V Laurasiatheria xix 21 to 23 General remarks on Erinaceomorpha, Soricomorpha and Pholidota 309 309 21 Erinaceomorpha 21.1  Introductory remarks and notes on food of Erinaceomorpha 309 21.2  Anatomy of the stomach of the Erinaceomorpha, including arterial supply 310 21.3  Small intestine and colon in Erinaceomorpha 311 21.4  Blood vessels supplying or draining the colon of Erinaceomorpha 311 22 Soricomorpha 312 22.1  General remarks 312 22.2  Short remarks on the digestive physiology of Soricomorpha 312 22.2.1 Family Soricidae, Subfamily Crocidurinae and Myosoricinae 313 22.2.1.1 Food of Crocidurinae and Myosoricinae 313 22.2.1.2 Gastric anatomy and remarks on digestion 313 22.2.2 Family Soricidae, Subfamily Soricinae 315 22.2.2.1 General remarks 315 22.2.2.2 Food of Soricinae 315 22.2.2.3 Gastric anatomy and remarks on digestion 315 22.2.2.4 Rectum-licking 316 22.2.3 Family Talpidae, short overview 316 22.2.4 Concluding remarks on gastric elongation in the Soricomorpha 317 22.2.5 Blood vessels of the digestive tract in Soricomorpha 317 22.2.6 Colon of the Soricomorpha 318 22.2.6.1 Colonic villi in Soricomorpha 318 318 23 Pholidota 23.1  General remarks 318 23.2  Remarks on systematics, biogeography and food in Pholidota 319 23.3  Gastric anatomy of Pholidota 319 23.4  Form of the small and large intestines in Pholidota 321 23.5  Arteries of the gut in Pholidota 321 23.6  Concluding remarks on the colon of Erinaceomorpha, Soricomorpha and Pholidota 321

322 24 Chiroptera 24.1  Introductory remarks 322 24.2  Systematics, phylogeny, zoogeography of Chiroptera 323 24.3  Food of Chiroptera in general 325 24.4  General remarks on the gastric anatomy of Chiroptera 327 24.5  Chiroptera, Pteropodidae 328 24.5.1 General remarks on Pteropodidae 328 24.5.2 Gastric anatomy of Pteropodidae 328 24.5.2.1  Pteropus sp. 329 24.5.2.2  Harpyionycteris sp. 329 24.5.2.3 Scotonycteris sp. 331 24.5.2.4 Eonycteris sp. 331 24.5.2.5 Rousettus sp. 331 24.5.2.6 Megaloglossus sp. 331 24.5.2.7 Epomophorus sp. 332 24.5.2.8 Concluding remarks on pteropodid stomach anatomy 332 24.5.2.9 Gastric digestion in Pteropodidae 332 24.5.3 Small intestine of the Pteropodidae, form and function 332 24.5.4 Large intestine in the Pteropodidae 333 24.6  Chiroptera, Microchiroptera 333 24.6.1 Gastric anatomy 333 24.6.1.1 Gastric anatomy of the Megadermatidae 333 24.6.1.2 Gastric anatomy of the Rhinopomatidae 334 24.6.1.3 Gastric anatomy of the Hipposideridae 334 24.6.1.4 Gastric anatomy of the Rhinolophidae 334 24.6.1.5 Concluding remarks on the gastric form of Megadermatidae, Rhinopomatidae, Hipposideridae and Rhinolophidae 334 24.6.2 Gastric anatomy of the Noctilionidae and Mormoopidae 334 24.6.3 Gastric anatomy of the Thyropteridae 335 24.7  Chiroptera, Phyllostomidae 336 24.7.1 General remarks 336 24.7.2 Feeding types within the Phyllostomidae 336 24.7.3 Gastric anatomy of the Phyllostominae 337 24.7.4 Gastric anatomy of the Carollinae 338



24.7.5 Gastric anatomy of the Stenodermatinae 338 24.7.6 Gastric anatomy of the Glossophaginae 339 24.7.7 Gastric anatomy of the Brachyphyllinae and Phyllonycterinae 341 24.7.8 Gastric anatomy of the Desmodontinae 341 24.8  Chiroptera, Molossidae 342 24.8.1 Introductory remarks 342 24.8.2 Gastric anatomy of the Molossidae 342 24.9  Chiroptera, Emballonuridae 343 24.9.1 Introductory remarks 343 24.9.2 Gastric anatomy of the Emballonuridae 343 24.10  Chiroptera, Natalidae 344 24.11  Chiroptera, Vespertilionidae 345 24.11.1 Introductory remarks 345 24.11.2 Gastric anatomy in the subfamily Vespertilioninae 345 24.11.3 Gastric anatomy in the subfamily Antrozoinae 346 24.11.4 Gastric anatomy in the subfamily Myotinae 347 24.11.5 Gastric anatomy in the subfamily Miniopterinae 348 24.11.6 Gastric anatomy in the subfamily Kerivoulinae 348 24.12  Small intestine of Chiroptera 349 24.12.1 Villi in the chiropteran small intestine 349 24.13  The caecum in Chiroptera 349 24.13.1 Distribution and anatomy of the chiropteran caecum 349 24.13.2 Digestive physiology of chiropterans under special consideration of the caecum 351 24.14  Colon of Chiroptera 352 24.15  Arterial supply of the gastrointestinal tract of Chiroptera 352 24.16  Concluding remarks on the digestive tract of Chiroptera 353 355 25 and 26 Carnivora General remarks on Carnivora 355 Types of food in Carnivora 356 25 Feliformia 356 25.1  General remarks on Feliformia 356 25.2  Gastric anatomy of Feliformia 356 25.3  Small intestine of the Carnivora 359 25.4  General remarks on the caecum of the Carnivora 359 25.5  Anatomy of the carnivoran caecum 359

Contents of volume II 

 xv

361 25.5.1 Caecum of the Carnivora, Feliformia 361 26 Caniformia 26.1  Fissipeds, land-living Caniformia 361 26.1.1 General remarks on fissipeds 361 26.1.2 The food of fissipeds 362 26.1.3 Gastric anatomy of fissipeds 362 26.2  Pinnipeds, aquatic Caniformia 364 26.2.1 General remarks on pinnipeds 364 26.2.2 Gastric anatomy of pinnipeds 365 26.2.3 The small intestine of Pinnipedia 366 26.2.4 Caecum of the Carnivora, Caniformia 366 26.2.4.1 Caecum of the Canidae 366 26.2.4.2 Regio ileocolica of the Mustelidae 366 26.2.4.3 Regio ileocolica of the Ursidae (including Ailuropoda melanoleuca and Ailurus fulgens) 367 26.3  Caecum of the Pinnipedia 369 26.4  Colon of the Carnivora 369 26.4.1 Topography and morphology of the colon in Carnivora 369 26.4.2 Notes on the wall of the colon 372 26.4.3 Functional characteristics of the carnivoran colon 373 26.4.4 Blood vessels supplying or draining the carnivoran colon 375 26.4.5 Concluding remarks on the colon of Carnivora 376 378 27 Perissodactyla 27.1  General remarks on the Perissodactyla 378 27.2  Food of Perissodactyla in general 378 27.3  Form and function of the post-oesophageal digestive tract in the Perissodactyla 380 27.4  Equidae 380 27.4.1 Considerations on the Phylogeny of horses 380 27.4.2 Food of the genus Equus 381 27.4.3 Wild asses 382 27.4.4 Gastric anatomy of the Equidae 382 27.4.4.1 Internal mucosal lining of the equine stomach 384 27.4.4.2 Gastric digestion in the horse 385 27.5  Rhinocerotidae 385 27.5.1 Food of the Rhinocerotidae 386 27.5.2 Anatomy of the stomach of Rhinocerotidae 387 27.6  Tapiridae 388 27.6.1 Food of the Tapiridae 388 27.6.1.1 Food of Tapirus bairdii 388 27.6.1.2 Food of Tapirus pinchaque 389

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 Contents of volume II

27.6.1.3 Food of Tapirus terrestris 389 27.6.1.4 Food of Tapirus indicus 390 27.6.1.5 Summing up the information on tapir food 390 27.6.2 Anatomy of the stomach of Tapiridae 390 27.7  The small intestine of Perissodactyla 391 27.8  Caecum of the Equidae – recent horses, donkeys and asses 391 27.8.1 Functional remarks on the equine caecum 393 27.8.2 General remarks on the caecum of the Tapiridae 396 27.8.2.1 Anatomy of the caecum of the Tapiridae 396 27.8.3 General remarks on the caecum of Rhinocerotidae 397 27.8.4 Anatomy of the caecum of the Rhinocerotidae 397 27.9  Topography and morphology of the colon in Perissodactyla 399 27.9.1 Notes on the wall of the colon in Perissodactyla 402 27.9.2 Blood vessels supplying or draining the colon 403 27.9.3 Functional characteristics of the colon in Perissodactyla 404 27.10  Remarks on the digestive tract of Perissodactyla, with anatomical and functional considerations 405 27.11  Concluding remarks on Perissodactyla 409 28 to 30 Cetartiodactyla 410 410 28 Cetartiodactyla, Artiodactyls 28.1  General remarks 410 28.1.1 Systematics and types of food 412 28.2  Camelidae 415 28.2.1 General remarks 415 28.2.2 Food of the Camelidae 416 28.2.3 Anatomy of the stomach of Camelidae 416 28.2.3.1 Terminological questions 416 28.2.3.2 Descriptive anatomy of the camelid stomach 418 28.2.3.2.1 General gastric anatomy and topography 418 28.2.3.2.2 Specific remarks on the rumen of Camelidae 420 28.2.3.2.3 Specific remarks on the reticulum of Camelidae 422 28.2.3.2.4 Specific remarks on the gastric tube and hindstomach of Camelidae 422

423 28.2.3.2.5 Gastric mesenteries of Camelidae 28.2.3.2.6 Architecture of the tunica muscularis in Camelidae 423 28.2.3.2.7 Histology of the tunica mucosa in Camelidae 425 28.2.3.2.8 Gastric blood vessels in Camelidae 426 28.2.3.2.9 Functional overview of the stomach in Camelidae 426 28.2.3.2.10 Concluding remarks on the camelid stomach 429 28.2.4 Small intestine of Camelidae 429 28.2.5 Colon of Camelidae 430 28.2.6 Functional anatomy of the caecum in Camelidae 430 28.3  Suidae 431 28.3.1 Introductory remarks 431 28.3.2 Food of Suidae 433 28.3.3 Gastric anatomy of the Suidae (Babirusa follows separately) 433 28.3.3.1 Mucosal lining of the suid stomach (Babirusa follows separately) 435 28.3.3.2 Gastric mesenteries (Babirusa follows separately) 436 28.3.3.3 Architecture of the tunica muscularis (Babirusa follows separately) 437 28.3.3.4 Blood vessels of the porcine stomach (Babirusa follows separately) 438 28.3.3.5 Ontogenetic development of the porcine stomach 439 28.3.3.6 Short functional remarks on the porcine stomach 440 28.3.4 Small intestine of Suidae 440 28.3.4.1 Glands and villi in the small intestine of Suidae 440 28.3.5 Topography and morphology of the colon in Suidae 440 28.3.5.1 Blood vessels of the colon in Suidae 441 28.3.6 The caecum of the Suidae, general remarks 442 28.3.6.1 Anatomy of the porcine caecum 442 28.3.6.2 Remarks on the functions of the porcine caecum 443 28.4 Babyrousa sp. 444 28.4.1 Introductory remarks 444 28.4.2 Food eaten by the babirusa 444 28.4.3 Anatomy and mucosal lining of the stomach  445 28.4.3.1 Gastric mesenteries of the babirusa 447 28.4.3.2 Blood vessels of the babirusa stomach 448



28.4.4 Small intestine of babirusa 448 28.4.5 Colon of babirusa 448 28.4.6 Remarks on the caecum of babirusa 449 28.5  Tayassuidae 449 28.5.1 Introductory remarks 449 28.5.2 Remarks on the biology of peccaries 450 28.5.3 Food of the peccaries 451 28.5.4 Anatomy of gastric compartments 451 28.5.4.1 Internal mucosal lining 455 28.5.4.2 Muscle architecture of the tunica muscularis 456 28.5.4.3 Arteries of the gastric region 457 28.5.4.4 Mesenteries of the peccary stomach 457 28.5.4.5 Functional remarks on the peccary stomach 459 28.5.5 Small intestine of Tayassuidae 460 28.5.6 Colon of the Tayassuidae 460 28.5.7 Caecum in Tayassuidae 460 28.5.8 Remarks on digestion the Tayassuidae 461 28.5.9 Comparative remarks on digestion in Suidae and Tayassuidae 462 28.6  Tragulidae 463 28.6.1 Introductory remarks 463 28.6.2 Fossil and surviving Tragulidae 464 28.6.3 The food of Tragulidae 464 28.6.4 Anatomy of gastric compartments 465 28.6.4.1 Rumen 465 28.6.4.2 Reticulum 466 28.6.4.3 Isthmus reticuloabomasicus 466 28.6.4.4 Abomasum 468 28.6.4.5 Mucosal lining of the tragulid stomach 468 28.6.4.6 Blood vessels of the tragulid stomach 469 28.6.4.7 Muscle architecture of the tunica muscularis 469 28.6.4.8 Mesenteries 469 28.6.4.9 Digestion and functional remarks on the stomach of the Tragulidae 470 28.6.5 Small intestine of the Tragulidae 471 28.6.6 Colon of the Tragulidae 472 28.6.7 Caecum of the Tragulidae 472 28.6.8 Remarks on digestion in Tragulidae 473 28.7  Pecora 473 28.7.1 Introductory remarks on Pecora 473 28.7.2 General considerations of gastric digestion in the Pecora 474 28.7.3 Remarks on food and general gastric function in Pecora 475

Contents of volume II 

 xvii

28.7.4 Gastric anatomy in the Pecora 476 28.7.4.1 The ruminoreticulum in Pecora 476 28.7.4.2 Anatomy of the rumen in Pecora 476 28.7.4.3 Internal macroscopic surface differentiations in the pecoran rumen 477 28.7.4.4 Anatomy of the reticulum in Pecora 479 28.7.4.5 Internal macroscopic surface differentiations in the pecoran reticulum 479 28.7.4.6 Functional remarks on the whole ruminoreticulum in Pecora 480 28.7.4.7 Anatomy of the omasum in the Pecora 480 28.7.4.8 Internal macroscopic surface differentiations in the pecoran omasum 480 28.7.4.9 Functional remarks on the omasum in Pecora 481 28.7.4.10 Anatomy of the abomasum in Pecora 482 28.7.4.11 Internal macroscopic surface differentiations in the pecoran abomasum 482 28.7.4.12 Functional remarks on the abomasum of Pecora 482 28.7.4.13 Relative volumes of gastric compartments in Pecora 482 28.7.4.14 Blood vessels of the stomach in Pecora 482 28.7.4.15 Gastric mesenteries in Pecora 483 28.7.4.16 Muscle architecture of the gastric tunica muscularis in Pecora 483 28.7.4.17 Functional remarks on the total stomach of Pecora 485 28.7.5 Small intestine of Pecora 486 28.7.5.1 Glands and villi in the small intestine of Pecora 487 28.7.6 Colon of Pecora 488 28.7.6.1 The tunica mucosa in the colon of Pecora 489 28.7.7 Caecum of Pecora 490 28.7.7.1 Anatomy and topography of the pecoran caecum 490 28.7.7.2 The caecum in Bovidae 491 28.7.7.3 The caecum in Cervidae 492 28.7.7.4 The caecum in Giraffidae 492 28.7.7.5 Remarks on the histology of the pecoran caecum 493 28.7.7.6 Embryology of the pecoran caecum 493 28.7.7.7 Microbiology of the pecoran caecum 494 28.7.7.8 Remarks on the physiology of the pecoran caecum 494

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 Contents of volume II

28.7.7.9 Remarks on the arterial supply, venous drainage and innervation of the pecoran caecum 495 28.8  Hippopotamidae 496 28.8.1 General remarks 496 28.8.2 Fossil Hippopotamidae 497 28.8.3 Food of the Hippopotamidae 497 28.8.4 Gastric anatomy in Hippopotamidae 498 28.8.4.1 General subdivision and position of the stomach in Hippopotamidae 498 28.8.4.2 Visceral blindsac in Hippopotamidae 499 28.8.4.3 Parietal blindsac in Hippopotamidae 500 28.8.4.4 Connecting compartment in Hippopotamidae 500 28.8.4.5 Glandular stomach in Hippopotamidae 500 28.8.4.6 Volumes of gastric compartments in Hippopotamidae 500 28.8.4.7 Macroscopic internal surface differentiations in hippopotamid forestomachs 502 28.8.4.8 The mucosa of the glandular stomach in Hippopotamidae 504 28.8.4.9 Mesenteries of the stomach in Hippopotamidae 504 28.8.4.10 Muscle architecture of the hippopotamid gastric tunica muscularis 504 28.8.4.11 Blood vessels of the gastric region in Hippopotamidae 506 28.8.4.12 Remarks on gastric digestion in Hippopotamidae 507 28.8.5 Small intestine of Hippopotamidae 509 28.8.6 Colon of Hippopotamidae 509 28.9  Concluding remarks on functional characteristics of the colon in different Artiodactyla 510 28.9.1 Microbial population 510 28.9.2 Alloenzymatic digestion (fermentation) 511 28.9.3 Importance of fermentation in the colon of Artiodactyla 511 28.9.4 The colon as fermentation volume 511 28.9.5 Colonic spirals 512 28.9.6 Taeniae, haustra and semilunar folds as differentiation of the colonic wall 512 28.9.7 Differentiation of the colonic tunica mucosa 512 28.9.8 Lymphoid tissue and innervation of the colon in Artiodactyla 513

514 29 and 30 Cetartiodactyla, Cetacea 29 Mysticeti 514 29.1  Introductory remarks 514 29.2  Systematics and Phylogeny of the Whippomorpha (Hippopotamidae plus Cetacea) 514 29.3  Types of food in Mysticeti 518 29.4  Types of food in Odontoceti 519 29.5  Anatomy of the stomach of Cetacea 521 29.5.1 General remarks 521 29.5.2 Stomach of Mysticeti 522 29.5.2.1 Stomach of Balaenidae, right whales 522 29.5.2.2 Stomach of the Balaenopteridae, rorquals 522 29.5.2.3 Stomach of Neobalaenidae 526 29.5.2.4 Stomach of Eschrichtidae 526 527 30 Odontoceti 30.1  Stomach 527 30.1.1 Stomach of Odontoceti 527 30.1.2 Stomach of Delphinidae 527 30.1.3 Stomach of Monodontidae 530 30.1.4 Stomach of Phocoenidae 531 30.1.5 Stomach of Physeteridae 533 30.1.6 Stomach of Platanistidae 535 30.1.7 Stomach of Iniidae 537 30.1.8 Stomach of Inia geoffrensis 538 30.1.9 Stomach of Pontoporia blainvillei 538 30.1.10 Stomach of Lipotes vexillifer 538 30.1.11 Comparative remarks on the stomach of the Iniidae and Platanista 539 30.1.12 Stomach of Ziphiidae, general remarks 540 30.1.13 Stomach of Hyperoodon 540 30.1.14 Stomach of Mesoplodon 541 30.1.15 Concluding and comparative remarks on the cetacean stomach 542 30.2  Small intestine 545 30.2.1 Small intestine of Mysticeti 545 30.2.2 Small intestine of Odontoceti 546 30.3  Morphology and topography of the colon in  546 Cetacea, introductory remarks 30.3.1 Colon of Mysticeti 546 30.3.2 Colon of Odontoceti 547 30.3.3 Notes on the wall of the cetacean colon 551 30.3.4 Concluding remarks on the colon of Cetacea 553

Contents of volume II 



30.4  The cetacean Caecum 553 30.4.1 Caecum in Mysticeti 553 30.4.2 Caecum in Odontoceti 555 30.5  Functional considerations concerning the cetacean gut 555 VI 1 1.1 1.2

557 General discussion 559 The digestive tube of Eutheria Reactor models 560 Form, size and function in the digestive tract in Eutheria 560 1.3 General remarks on fermentation and alloenzymatic digestion 561 1.4 Functional differentiation within the gut 562 2 Some criteria that are used to define anatomical sections of the gut 562 2.1 Blood vessels 563 2.2 Intraperitoneal and retroperitoneal positions 563 2.3 Tunica mucosa 564 2.4 Tela submucosa 565 2.5 Tunica muscularis 565 2.5.1 Taeniae, haustra and semilunar folds 565 2.5.2 Architecture of the gastric tunica muscularis 566 2.6 Anatomy of the gastrointestinal tract, comparative aspects 566

2.7

 xix

Food quality and regional differentiations of compartments of the post-oesophageal digestive tract 569 2.8 Combinations of morphological differentiations 573 577 3 Stomach 3.1 Separate glands in the stomach of some Eutheria 578 4 Small intestine 579 4.1 Duodenum 580 4.2 Jejuno-ileum with remarks on their differentiation and on their mesentery 582 583 5 Colon 5.1 Terminological aspects 584 5.2 Sections of the colon 584 5.3 Colonic spirals and loops 586 D  igestive function of the colon – 5.4 comparative aspects 587 589 6 Caecum 6.1 Comparative remarks 589 6.2 The appendix vermiformis, a differentiation of the caecum in some eutherian mammals 591 6.3 Functional remarks on the Appendix vermiformis 593 595

Literature Index

683

I Introduction

Introduction: The purpose of this text is to compile anatomical data for a handbook that deals with the post-oesophageal digestive tract of eutherian mammals. Over-specialisation should be avoided. Consideration of older scientific literature is not obsolete, but it should inform about the long tradition of often surprisingly exact anatomical studies, which have been partly forgotten and are therefore often not taken into account by modern researchers. Presentday knowledge of form and function of organ systems should keep in mind that insights are the product of a continuous evolutionary diversification. Therefore, it is necessary not only to describe anatomical complexity, but also to consider – if possible – morphological and functional developments.

1 An appreciation of exemplary investigators – past and present An effort like the present treatise is based on the cumulative scientific production of many investigators, who are listed in the table of references. In addition, a small group of investigators has made extraordinary contributions to our knowledge of the anatomy of the gastrointestinal tract of different eutherian taxa; others studied the function of the tract or supplied stimulating overviews. The present author had the pleasure to meet personally some of these researchers; for him, they represent examples of scientific excellence (in alphabetical order): H. Behmann (gut of Rodentia: Myomorpha), M. Clauss (functional and formal differentiations of the gastrointestinal tract), G. L. Forman (digestive tract of Chiroptera), M. Gorgas (gut of Rodentia: Sciuromorpha, Hystricomorpha), R. R. Hofmann (Ruminantia, especially stomach), C. M. Janis (equids and ruminants, comparison of digestive strategies; palaeontology), K. Kostanecki (comparative anatomy of the caecum), R. Moir (“ruminant-like” herbivores), R. Parra (foregut and hindgut fermentation), R. A. Prins (physiology of digestion, microbiology), W. Schultz (gut of Chiroptera and Dermoptera), R. L. Snipes (caecum and internal surface of the digestive tract), N. N. Vorontsov (or Woronzow) (gastrointestinal tract of Rodentia: Myomorpha). Finally, I want to express my gratitude and respect to H.-R. Duncker, Professor Emeritus in Giessen,

DOI 10.1515/9783110527735-001

who benevolently stimulated my interest in comparative anatomy. Outline of the following text The text will cover 30 eutherian taxa – orders and suborders – that are listed in Tab. 1.1. The system of numbering is as follow: Illustrations and tables of the “Introductory remarks” start with “1”, the superorder Afrotheria with “2”, and those referring to the superorders Xenarthra, Euarchontoglires and Laurasiatheria with “3”, “4” and “5”; the number “6” can be found at the beginning of numbers illustrating the “General discussion”. The following numbers identify the consecutive sequence of figures within the superorders. In chapters that deal with the anatomy of the gastrointestinal tract of different eutherian orders, the taxonomy and phylogeny together with accounts of biogeography, as well as food characteristics, are discussed. Scientific names of genera and species, as well as their common English names, will be taken from Wilson and Reeder (2005). Often, the original authors use a nomenclature that is now obsolete and will be avoided in this text. Artiodactyla and Cetacea are now grouped together as Cetartiodactyla. The two “historical” terms are still well established in the literature. The text will deal with the anatomy of the postoesophageal digestive tract, starting at the cardia, the stomach follows, as well as small intestine (according to the terminology in human [Terminologia Anatomica (TA, 1998), 1998] and veterinary [Schaller, 1992] anatomy), and the colon (consisting, according to human anatomy, of the colon ascendens, transversum, descendens, sigmoideum and rectum). At the regio ileocolica, the border between the small intestine and the colon, a caecum can be differentiated in some taxa. Especially in species belonging to the Euarchontoglires, an appendix vermiformis branches off from the apex of the caecum.

2 Outline of eutherian systematics Taxonomic studies, based on molecular investigations, group orders into four superorders (Murphy et al., 2001a, b, Madsen et al., 2001): Afrotheria, Xenarthra, Euarchontoglires and Laurasiatheria. The Afrotheria comprise

4 

 I Introduction

Tab. 1.1: Compilation of four eutherian superorders, thirty orders and some suborders that are dealt with in this book, together with introductory remarks and general discussion. Superorder

Order

Suborder

I Introductory remarks II Afrotheria II Afrotheria II Afrotheria II Afrotheria II Afrotheria II Afrotheria II Afrotheria III Xenarthra III Xenarthra III Xenarthra IV Euarchontoglires IV Euarchontoglires IV Euarchontoglires IV Euarchontoglires IV Euarchontoglires IV Euarchontoglires IV Euarchontoglires IV Euarchontoglires IV Euarchontoglires IV Euarchontoglires V Laurasiatheria V Laurasiatheria V Laurasiatheria V Laurasiatheria V Laurasiatheria V Laurasiatheria V Laurasiatheria V Laurasiatheria V Laurasiatheria V Laurasiatheria VI General discussion

1 Afrosoricida 2 Afrosoricida 3 Macroscelidea 4 Tubulidentata 5 Hyracoidea 6 Proboscidea 7 Sirenia 8 Cingulata 9 Pilosa 10 Pilosa 11 Scandentia 12 Dermoptera 13 Primates 14 Primates 15 Rodentia 16 Rodentia 17 Rodentia 18 Rodentia 19 Rodentia 20 Lagomorpha 21 Erinaceomorpha 22 Soricomorpha 23 Pholidota 24 Chiroptera 25 Carnivora 26 Carnivora 27 Perissodactyla 28 Artiodactyla 29 Cetacea 30 Cetacea

Tenrecomorpha Chrysochloridea

Folivora Vermilingua

Strepsirrhini Haplorrhini Sciuromorpha Castorimorpha Myomorpha Anomaluromorpha Hystricomorpha

Feliformia Caniformia

Mysticeti Odontoceti

Afrisoricida with Tenrecs and Chrysochloridae, Macroscelidae (Elephant shrews), Tubulidentata (Orycteropus, the aardvark), Hyracoidea (hyraxes), Proboscidea (elephants) and Sirenia (manatees and dugongs). Xenarthra consist of the orders Cingulata (armadillos) and Pilosa (Folivora, sloths, and Vermilingua, anteaters and tamanduas). The Euarchontoglires, as characterised by Murphy et al. (2001b), comprise the Glires, consisting of rodents and lagomorphs, as well as the Euarchonta, which include flying lemurs (Dermoptera), tree shrews (Scandentia) and primates. The order of truely flying mammals, the Chiroptera (bats), belongs to the superoder Laurasiatheria (Murphy et al., 2001b) and is genealogically distant from dermopterans (Adkins and Honeycutt, 1991). Together with chiropterans, Laurasiatheria are represented by

Eulipotyphla (Erinaceomorpha plus Soricomorpha, i.e. hedgehogs and shrews and their kin). Pholidota (Pangolins), Carnivora and Perissodactyla (odd-toed ungulates) are also representatives of the Laurasiatheria together with the Cetartiodactyla, which consist of Artiodactyla, even-toed ungulates, and Cetacea, whales (Murphy et al., 2001a).

2.1 Definition and delineation of gut sections The entrance into the stomach lies at the cardia; the exit is called pylorus. There are generally three main sections of the organ, as defined, for example, in human anatomy

I Introduction  

(TA, 1998): The fundus or fornix gastricus, a more or less pronounced outpocketing of the second gastric section, the corpus gastricum, as well as the final setion, the pars pylorica. The following small intestine (intestinum tenue) consists of three sections, the duodenum, the jejunum and the ileum. In many mammals, the latter two are difficult to separate from each other morphologically. The intestinum crassum or large intestine can be subdivided into the caecum, the colon ascendens, transversum, descendens and sigmoideum, as well as the rectum. This terminology is used in human anatomy, but cannot always be used in other Eutheria. It is necessary to consider the criteria applicable to define gut sections anatomically. This is a question difficult to solve, as, for example, in those species where a caecum is missing, such as in Insectivora Lipotyphla, as well as in many chiropterans (bats), Pholidota (scaly anteaters), some carnivores and most odontocete cetaceans (toothed whales). In these cases, no clear line of demarcation between the small and the large intestines exists. Different researchers studying different problems have separated sections of the digestive tract according to different criteria with considerable overlap, thus making

 5

pragmatic work possible, but also making definitions ambiguous.

2.2 Functional differentiations of gastrointestinal tract sections It is the aim of this compilation of published data on functional differentiations (Tab. 1.2) to produce a basis for comparison of the post-oesophageal digestive tract in all eutherian orders (Murphy et al., 2001a, b; Madsen et al., 2001; Wilson and Reeder, 2005). Stomach, small intestine and large intestine will be dealt with, as well as the caecum and the appendix vermiformis, which is an annex to the caecum of primates, rodents and lagomorphs within the Euarchontoglires. Although Tab. 1.2 demonstrates a remarkable overlap of functions between regions of the tract, the functional “compositions” differ between regions. A prominent example is emulgation, which takes place in the small intestine after bile has been “injected” via the choledochic duct. The stomach is the area with the widest range of functions (Tab. 1.2). The following numbers in square brackets

Tab. 1.2: Functional differentiations in five sections of the gastrointestinal tract Functions 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

Storage Retention Transport Kneading Mixing Separation particles – liquids Separation fine – coarse Division into portions Secretion Absorption Digestion, autoenzymatic Fermentation, alloenzymatic Emulgation (bile) BR CSTR PFR Biofilm formation “Safe house” for microbes Re-inoculation after loss

Stomach X X X X X X X X X X X (X)

X (X) (X) (X) (X)

Small intestine (X) X X X X X X X X X X

X

Colon and Rectum

Caecum Corpus

(X) X X X X X X X X X (X) X

X X (X) X

(X) X (X)

(X) (X) (X) (X)

Appendix

X X X X X X X

X X X

Symbols: X, this function is characteristic for the respective section of the gastrointestinal tract; (X), this is a function that cannot be found in all species or plays only a limited functional role. Abbreviations of reactor types as discussed by Penry and Jumars (1987) and Caton and Hume (2000): BR, batch reactor; CSTR, continuous stirred tank reactor; PFR, plug flow reactor.

6 

 I Introduction

can be found in the first column of the table. Storage of digesta [1], their retention [2] to interrupt continuous transport [3], may have a kneading [4] and mixing [5] effect. Particles can be separated from liquids [6] or fine from coarse particles [7]. The pylorus subdivides the digesta into portions [8] that are forwarded into the small intestine. The tunica mucosa secretes into the lumen [9] and absorbs [10] from it. Of course, the stomach is an organ for digestion of food with enzymes that are secreted by the mammalian host [11] (autoenzymatic digestion, Langer, 1988). In some taxa, the ingestion of difficult to digest plant material (herbivory) is enabled by the activity of symbiotic microbes – fermentation of plant matter [12]. However, this alloenzymatic digestion cannot be found in all eutherians because acid digestion makes fermentative processes impossible. The gastric lumen forms a continuous stirred tank reactor [15], but there are also gastric differentiations that make the organ a plug-flow reactor [16] (Penry and Jumars, 1987; Alexander et al., 1991; Hume and Sakaguchi, 1991; Caton and Hume, 2000; Karasov and Martínez del Rio, 2007). When influx and efflux take place at opposite extremities of the lumen, this means that this is not a batch reactor [14], where influx and efflux into and from the same opening can be observed, as, for example, in the caecum. Microbes and mucus can form a biofilm [17]. It is questionable whether beneficial microbes can be preserved in a “safe house” [18] formed by parts of the stomach. In this case, re-inoculation [19] of the gastric contents with “helpful” microbes would be possible. Because of effective separation of the gastric lumen from the small intestine, the emulgation of gastric contents [13] with the help of bile, which is produced by the liver, cannot be observed. The small intestine is not necessarily a storage organ [1], but digesta are retained a certain time [2] and later transported [3], kneaded [4] and mixed [5]. Separation of particulate digesta from liquids [6] or of coarse from fine particles [7] can be observed, but subdivision of small intestinal contents into separate portions [8] does not take place. By peristaltic movement, the plug flow transports digesta more or less continuously in aborad direction [16]. Secretory [9] and absorptive [10] processes enable autoenzymatic digestion [11], especially proteolysis and lipolysis can be observed, for the latter process emulgation [13] of fat with the help of bile takes place in the duodenum, which represents the proximal section of the small intestine. Microbial alloenzymatic digestion of plant matter [12] does not play a role in the small intestine. The tube of the small intestine represents a plug-flow reactor (PFR)[16], but it is not a continuous stirred tank reactor (CSTR)[15]. The tubiform colon is not an effective structure for storing digesta [1], although retention [2] is combined with transport [3]. Peristaltic movements, as well

as haustrations and contractions knead [4] and mix [5] digesta and transport them aborally in this plugflow reactor [16]. Separation of particles from liquids [6] and of fine from coarse particles [7] can be observed. The rectum and the anal sphincters subdivide digesta flow into portions [8] that are voided during defecation. Secretion [9] of mucus with SIgA (secretory immunoglobulin A) and absorption [10] of water and solutes is of importance and enables alloenzymatic fermentation of plant matter [12]. In humans, it is estimated that 5 to 10% of energy requirements are supplied by this process (McNeil, 1984). On the other hand, autoenzymatic digestion [11] of animal or microbial food material plays a less important role in the colon. Function as a continuous stirred tank reactor [15] can only be of very limited importance to the colon. Secretory immunoglobulin A and mucus may be involved in the growth of bacterial biofilms [17] (Everett et al., 2004). Functional differentiations of the caecum and colon are similar. The caecum stores material [1], retains [2], transports [3], kneads [4] and mixes [5] it. Digesta particles are separated from liquids [6] or coarse particles from fine ones [7]. The caecum does not necessarily subdivide digesta into different portions [8] and fat digestion of the emulgated contents [13] has already taken place in the duodenum as part of the small intestine. Secretion [9] and absorption [10] is a characteristic activity of the tunica mucosa. Digesta of plant origin or otherwise undigestible structural carbohydrates are very often submitted to fermentation [12] (Vonk and Western, 1984), but degradation of materials of animal or microbial origin via autoenzymatic digestion [11] plays a less important role. The aboral section of the small intestine, the ileum, enters the large intestine at the ostium ileocaecale close to the border between colon and caecum, and the ostium caecocolicum is generally a wide aperture between both sections of the large intestine. However, the caecum is set-off from the direct oral-aboral digesta flow. As the morphology of the caecum can vary considerably, all three types of reactors can be differentiated in different combinations. Referring to the diversity of eutherian caecum forms, none of the reactor types has a monopoly and is therefore plays a “limited functional role” in placental mammals. The influx and efflux into and from the caecum can be discontinuous via the same opening, the ostium caecocolicum, and contents are well mixed [5] (Hume and Sakaguchi, 1991) so that the organ can be classified as batch reactor (BR) [14] (Caton and Hume, 2000). In long, stretched caeca characteristics of a continuous stirred tank reactor [15] can be found and in some cases movement of digesta resembles the situation in a plugflow reactor [16].

I Introduction  

When beneficial microbes are purged from the colon, for example, during diarrhoea, the appendix vermiformis acts as a “safe house” [18], where microbes survive, forming a biofilm [17] (Everett et al., 2004). Their attachment to the gut wall is mediated by carbohydrates (Savage, 1977). After the colon has been exposed to pathogens and was purged of microbes (Bollinger et al., 2007), re-inoculation of with viable microbes [19] is made possible by the “safe-house” from the biofilm.

2.3 General remarks on sections of the gastrointestinal tract The relationship between the volumes of the stomach, small intestine and large intestine and the type of food will be considered. The volume of the small and large intestines are influenced by the differentiation of the stomach. To characterise the anatomy of the gastrointestinal tract 11 parameters of the stomach, five of the caecum and two of the colon are considered (Tab. 1.3). Plesiomorphic characters are classified as “1”, and apomorphic characters as “2”. For example, the glandular stomach, lined exclusively with a secreting epithelium, is considered as plesiomorphic character and can be found in 62.5% of the considered 601 species. It is classified as “1”. Aglandular stomachs with no secreting epithelium (4.8%), as well as the combination of glandular and non-glandular epithelium, forming a “composite” organ (32.7%), are both considered as apomorphies. These two apomorphies are each classified “2” in Tab. 1.3. Transformation of anatomical differentiations into a numerical system evaluates all differentiations identically – with the exception of the above-mentioned apomorphies of gastric mucosal lining. Later, the discussion will come back to the information given above.

 7

Tab. 1.3: Differentiations of different sections in the gastrointestinal tract Stomach is glandular Stomach is aglandular Stomach is composite Stomach with setoff region Stomach is plurilocular Forestomach is part of oesophagus Forestomach is setoff Forestomach is haustrated Reticulum is present and sacculated Reticulum is present and cellular Omasum is present Caecum is present Caecum is present and haustrated Appendix vermiformis is present Spiral fold in ceacum is present Caecum is paired Colon is haustrated Colon is diverticulated

(1) (2) (2) (1) (1) (1) (1) (1) (1) (1) (1) (1) (1) (1) (1) (1) (1) (1)

The numbers indicate plesiomorphy (1) or apomorphy (2).

2.4 Food index and volume The taxonomy of eutherian species applied here follows a checklist of mammalian names, supplied via the net by the Division of Mammals of the Department of Systematic Biology of the National Museum of Natural History, Washington, DC. This list is based on the taxonomic and geographic reference published by Wilson and Reeder (2005). It is of interest to characterise different taxa according to their average food quality, which is expressed as grams crude fibre per kilogramme dry matter eaten. Langer (2008) used data from tables characterising nutrient compositions of domestic animal feeds (Tab. 1.4) to produce

Tab. 1.4: Food index determined from data from the literature on domestic mammals Feeding typesa

Feeds as listed in feeding value tablesb

Food classificationc (means of grams crude fibre per kg DM)

Sanguinivory, nectarivory, gumivory Carnivory, ichthyophagy Insectivory, myrmecophagy, crustacivory Granivory Frugivory, eaters of tubers and bulbs Herbivory, folivory Graminivory

Blood, milk, egg Fish, meat, offals of poultry and mammals Crustacea Grains and seeds Tubers, beets and roots, fruits Green fodder, leaves Grass, straw

0 4 26 64 98 207 343

aMost

of the terms were taken from Eisenberg (1981) and Starck (1995). data are from the following feeding value tables published for domestic mammals: DLG (1982), Futterwerttabellen für Wiederkäuer; DLG (1984a), Futterwerttabellen für Pferde; DLG (1984b), Futterwerttabellen für Schweine; Meyer and Heckötter (1986), Futterwerttabellen für Hunde und Katzen. cThese values are the means from feeds listed in the above feeding value tables in column “b”. bRaw

8 

 I Introduction

a numerical food classification; low values characterise material of animal origin. The data are based on the content of crude fibre (CF) per kilogramme of dry matter (DM) of the respective food, as published in the agricultural and veterinary literature (DLG, 1982, 1984a, b; Meyer and Heckötter, 1986). The following classification (“Food index”) will be used in this chapter: 250 g CF/kg DM: food of florivores, very low quality. For a general consideration of the relevance of small intestine, caecum and colon volumes (or weights of contents) for small intestine, caecum and colon, as well as food, classified as contents in grams of crude fibre per kilogramme dry matter, were compiled in Tab. 1.5. A second list, representing a data set for anatomical differentiations according to the factors of morphological differentiations as given in Tab. 1.3, was compiled in Tab. 1.6 for the gastrointestinal tract of 601 eutherian species. To characterise the complexity of a section, the values are summarised. An example for two species will be given and reference to Tab. 1.6 should be made: The chimpanzee (Pan troglodytes) has a glandular stomach (1) without any other differentiation, but a caecum is differentiated (1), it is haustrated (1) and has an appendix vermiformis (1). In addition, the colon is haustrated (1). The complexity of this digestive tract under consideration of the three sections sums up: stomach (1) + caecum (3) + colon (1) = 5. On the other hand, the digestive tract of the fat sand rat (Psammomys obesus) sums up as follows: It has a composite stomach (2) with a setoff glandular region (1). This plurilocular stomach (1) also has a setoff forestomach (1). A caecum is present (1), which does not show any further differentiations. The colon is neither haustrated nor diverticulated. The total differentiation amounts to: stomach (5) + caecum (1) + colon (0) = 6. Transformation of anatomical differentiations into a numerical system evaluates all differentiations identically – with the exception of the above-mentioned apomorphies of gastric mucosal lining. Separate ternary diagrams were drawn for the abovementioned six groups of food index (Fig. 1.1). The trian­ gular diagrams are based on Tab. 1.5 and show the relative volumes of small intestine, caecum and colon for a total of 206 specimens in 100 eutherian species. On the other hand, the following three illustrations show the

relative volumes for six groups of food classification in different taxa. For example, Fig. 1.2 informs about carnivores, artiodactyls and Glires. Comparable information on strepsirrhine and haplorrhine primates is given in Fig. 1.3, and in Fig. 1.4, a wide range of taxa with different degrees of food classification are depicted in a triangular diagram. In a purely faunivorous diet (food index 65 million years ago). There is, however, considerable opposition against this view. Eurotamandua might be a sister taxon to the Palaeanodonta (Rose, 1999), which were present in the lower Oligocene of Bavaria (Heißig, 1982). According to Carroll (1988) and Emry (1970), palaeanodonts were closely related to the pangolins (scaly anteaters or Pholidota of Asia and Africa); they were neither related nor ancestral to the Xenarthra (Redford and Eisenberg, 1992). The abovementioned Eurotamandua joresi may be a genus belonging to the palaeanodonts (Rose and Emry, 1993). Gaudin and Branham (1998) write that results of their investigations strongly contradict the hypothesis that Eurotamandua is a vermilinguan. However, their analysis cannot conclusively answer the question of Eurotamandua’s affinities. These facts cast doubt on the close connection between Eurotamandua and Vermilingua (Delsuc et al., 2001). Szalay and Schrenk (1998) and Gaudin (2003) prefer to consider Eurotamandua a distinct clade. The striking morphological resemblance between this fossil and anteaters might be the result of an outstanding adaptative convergence because of “ant-eating” (McDonald et al., 2008). The Vermilingua show great variation in size between genera (Barros et al., 2008). They range from 16 to 23 kg for the strictly terrestrial giant anteaters, Myrmecophaga tridactyla, to 3.8 to 8.5 kg for the medium-sized semi-arboreal southern tamandua, Tamandua tetradytyla, and only 0.155 to 0.275 kg for the arboreal silky anteater, Cyclopes didactylus.



Following Hirschfeld (1976), the living genera of anteaters are not as closely related as previously thought and Cyclopes didactylus, the silky anteater, should be placed separately from the Myremecophagidae in the family Cyclopedidae (Barros et al., 2008; McDonald et al., 2008). The genera Myrmecophaga and Tamandua, on the other hand, had a common ancestor, Prototamandua, which did not belong to the ancestry of Cyclopes. The genus responsible for the name of the eutherian family comprises just one species, Myrmecophaga tridactyla, giant anteater. The two species of Tamandua are geographically separated: T. mexicana is the northern, T. tetradytyla the southern tamandua.

10.2 Recent species The geographical range of the species of Vermilingua is depicted on maps by Wetzel (1982) and Aguiar and da Fonseca (2008). Cyclopes didactylus (Family Cyclopedidae) ranges from tropical Mexico via Nicaragua and the Central American isthmus (Genoways and Timm, 2003) well into the northern part of South America to the northeastern Atlantic coast of Brazil. According to Superina et al. (2010), the area inhabited by this species is separated into two ­sections, one in the west around the Andes and a second one in the Brazilian northeast. Both populations probably remained separated since the Pleistocene, when the Atlantic and Amazonian forests retracted and were separated from each other by the xeric Caatinga (Miranda and Superina, 2010), a “savanna-type” biome with succulent and thorny trees and bushes (Schmithüsen, 1968; Bucher, 1982). The three remaining species belong to the Myrmecophagidae. Myrmecophaga tridactyla, the giant anteater, inhabits the area between Belize and Guatemala far into South America, reaching Uruguay. In the Pleistocene, Myrmecophaga tridactyla even extended its range into northernmost Mexico (Shaw and McDonald, 1984). The genus Tamandua mexicana (northern tamandua) has a range from the Mexican plateau through Central America into South America and it reaches Peru. Finally, the fourth species, T.  tetradactyla, the southern tamandua, can be found in South America east of the Andes, reaching northern Argentina and northern Uruguay.

10.3 Food of the Pilosa, Vermilingua As the anteaters ingest a highly specialised food, it is difficult for zoo operators to supply the animals with a palatable, appealing, high protein diet (Meritt, 1976, 1977). However, information on vermilinguan zoo food can be

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far away from what the animals select for themselves in the wild (Luppi et al., 2008). An artificial food for zoo animals of the northern tamandua, Tamandua mexicana, covers, as Morales-Sandoval (2010) writes, the protein and energetic needs, but fibre contents are low. Tamandua mexicana is an obligate predator of ants and termites, but on Barro Colorado Island, Panama, it was observed that animals eat ripe fruit (Brown, 2011) and consumption of fruit is not the accidental consequence of the anteater seeking insect larvae in the fruit. As the English name, “anteaters” already implies, ants are eaten, but termites are also ingested by the Vermilingua. Redford and Dorea (1984) write that termite workers and soldiers, in comparison with most other invertebrates, tend to be high in ash, low in fat and about equal in water and nitrogen. In contrast, winged ants and termites and most larval or pupal insects have much higher percentages of fat. According to Lubin (1983), some vermilinguans prefer mainly ants, others only termites. On the other hand, tamanduas eat termites regularly. Silky anteaters, the smallest of the Vermilingua, eat a much more specific diet than Tamandua and Myrmecophaga. Food consisting of social insects, such as ants and termites, is abundant and easily found. However, the defence mechanisms of the insects, such as powerful mandibles or stinging processes of the exoskeleton, as well as chemical defences, may be the reason why relatively few mammalian species have specialised on ants and termites as food (Rodrigues et al., 2008). Redford (1986) calls Myrmecophaga tridactyla, the giant anteater, an obligate myrmecophage. In any given habitat, this species will prefer those ants or termites that are most available. According to Möcklinghoff (2008), Myrmecophaga tridactyla feeds not only on ants and termites, but also eats small reptile eggs (diameter = 1 cm). Edwards and Lewandowski (1996) remark that the food of giant anteaters (M.  tridactyla) in zoos had to be supplemented by cellulose to mimic dietary chitin. Like cellulose, chitin is a structural polysaccharide. The chitinous exoskeletons of insects consumed by free-ranging giant anteaters may perform a role similar to that of cellulose in the digestive tract of herbivores by providing gut fill and maintaining faecal consistency. According to Vaz et al. (2012), insects were the main food of wild M. tridactyla, but they also eat seeds. The bulk in the food of adults is difficult to handle, and because of this, it affords approximately 7 months before the young giant anteater is nutritionally independent of its mother (Kühne et al., 2011). Another species, the silky anteater (Cyclopes didactylus), is an ant-eating specialist, it consumes 14,000 ants per day and was never observed by Lubin (1983) to eat termites. Only formicid ants and no termites could be

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found in the gastrointestinal tract of Cyclopes didactylus (Miranda et al., 2009), but Wetzel (1982) mentions that on Trinidad beetles were eaten by this species. Best and Harada (1985) assumed that this species does not posses either chitinase or chitobiase, as it is known from insectivorous bats (Jeuniaux, 1961). Nagy and Montgomery (2012) determined the daily requirements of Cyclopes didactylus for energy, food and water of free-living individuals of this species, which were low, amounting to only one-third to two-thirds of the values found in other eutherians with the same body size. Xenarthra, in general, may have unusually low metabolic intensities and nutritional needs. Tamandua sp. lives in the same area, but eats termites regularly. Oyarzun et al. (1996) analysed the nutrient composition of Nasutitermes termites from Venezuela, which represent the food of Tamandua tetradactyla, the southern tamandua (Gardner, 2005b). Differences in composition were seen between the various termite castes, particularly between adult workers and soldiers, and the alates, the sexually mature winged swarming termites. Alates develop in the colony from immature stages prior to the flight season. The investigations of Oyarzun et al. (1996) revealed this food to be rich in protein, moderate in fat and low in ash content, i.e. low mineral resources (Fig. 3.23). The diagram, which presents just three food constituents (Oyarzun et al., 1996, lists many more), shows that the alates represent a preferable food with a relatively high fat content and a high percentage of protein. Perhaps, a relatively high-fibre fraction, which was measured in total termites, reflects the complex carbohydrate content, including chitin, of the exoskeletons. Wetzel (1982) mentions that the northern tamandua, Tamandua mexicana, eats ants and termites. In that species,

Fig. 3.23: Contents of three nutrients (crude protein, crude fat and ash) in the food of Tamandua tetradactyla, expressed as percentages that are supplied by three castes of the termite Nasutitermes sp. Adapted from Oyarzun et al. (1996).

Sandoval-Gomez et al. (2012) identified 27 ant species, but only 2 termite species. On Barro Colorado Island in Panama, this vermilinguan species was seen to consume ripe fruit of the palm Attalea butyracea (Brown, 2011). Apart from insects, Vaz et al. (2012) found seeds of Poaceae, Cyperaceae and Euphorbiaceae in the gut of the southern tamandua (Tamandua tetradactyla). This semi-arboreal species (Smith, 2007) exploits arboreal termites, as well as wasps and bees; it also takes larvae, adults, eggs, honey and beeswax.

10.4 Gastric anatomy of Pilosa, Vermilingua The anatomy of the stomach of anteaters did not find much interest in published studies. More detailed accounts are from the 19th century and from the first half of the 20th  century. In modern studies, such as the species accounts of Navarrete and Ortega (2011) and Hayssen (2011) on Tamandua mexicana, the digestive tract anatomy was not described. Böker (1937/1967) mentions that the filled stomach of the three-toed sloth, Bradypus tridactylus, represents 11.4% of the body weight, but in the southern tamandua, Tamandua tetradactyla, the filled stomach represents only 1.7% of the total body weight. The stomach of the giant anteater, Myrmecophaga tridactyla, is simple and shows a thickened muscular coat in the pars pylorica (Cuvier, 1854; Flower, 1872). A “taenia” can be found in this region (Rapp, 1843b), which is called “a sheet of tendon” by Owen (1868), which extends from the corpus region of the stomach to the pars pylorica (Fig. 3.24 C). Rapp (1843b) mentions that the stomach of the giant anteater is lined internally with a very soft surface of glandular mucosa. According to Weber (1928/1967), the area of proper gastric glands exceeds that  of pyloric glands; the pylorus has a strong sphincter, so that a thick wall surrounds a narrow lumen, forming a sort of “trituation organ” or “veritable gizzard” that reduces the size of insect exoskeletons (Owen, 1868; Flower, 1872). In M. tridactyla, the stomach consists of a thin-walled and spherical, almost ball-shaped (Klinckowström, 1895), corpus ventriculi (called “cardiac portion” by Owen, 1868) with a diameter of approximately 20 cm and a smaller pars pylorica with a diameter of approximately 7.6 cm (measurements according to Owen, 1868). The oesophagus opens near the middle of the spherical portion (Fig. 3.24) and is situated about 9 cm from the aperture between the corpus ventriculi and the pars pylorica. The gastric cavity is lined with a secreting mucosa, the types of which are not clearly characterised. The mucosal surface shows numerous small wavy folds, of which the larger and apparently more permanent folds converge towards the aperture of the pars pylorica (Fig. 3.24 B). In this latter gastric region, massive,



10 Pilosa, Vermilingua 

 121

mainly longitudinal, folds with a total thickness between 1 and 2.5 cm can be found (Owen, 1868). They are lined by a “horny grinding surface”, which compensates for the absence of teeth in the mouth (Flower, 1872). Flower (1872) also presents information on the gastric anatomy of two other genera of Vermilingua: The stomach of Tamandua sp. resembles that of the giant anteater in having an almost globular thin-walled cardiac portion, and a muscular pyloric “gizzard”, although the latter is not quite so strongly developed. Böker (1937) published an excellent illustration of the stomach of Tamandua tetradactyla (Fig. 3.25). He writes that two pyloric muscular folds are covered with a glandular

mucosa that seems to work against each other like teeth. This can be interpreted as a structure that crushes the insect exoskeletons. The stomach of the silky anteater, Cyclopes didactylus, is pyriform, but the corpus ventriculi is rounded (Klinckowström, 1895). The walls are muscular, especially towards the pylorus, but there is no distinct gizzard-like portion as in the two preceding species. On the other hand, Klinckowström (1895) speaks clearly of two gastric sections in Cyclopes didactylus. Considerable differences have been described by that author when stomachs from different individuals of that species were investigated. In a female, Klinckowström (1895) found a large egg-shaped and thin-walled corpus ventriculi combined with a small and more cone-shaped pars pylorica. The lesser curvature of this stomach is straight. In another stomach, from a male silky anteater, Klinckowström (1895) found a different shape. Although the organ is subdivided into a cardiac and a pyloric part, both are approximately of the same size and the lesser curvature shows a deep concavity. The author could not detect remarkably different types of mucosa in both parts of the stomach of Cyclopes, which are both covered with a soft glandular mucosa with ridges and a pyloric torus on the lesser curvature. Proper gastric glands, which Klinckowström (1895) calls “Labdrüsen”, line the corpus ventriculi and extend into the pars pylorica, which is mainly lined with pyloric gland mucosa, especially along the greater curvature. The border between the proper gastric glands and pyloric glands is difficult to differentiate; even amongst pyloric glands, parietal cells, which are characteristic of proper gastric glands, can be found.

Fig. 3.24: The stomach of the Pilosa, Vermilingua. The pylorus lies between black dots. Adapted from A: Oppel 1896; B: Owen 1868; C: Pernkopf & Lehner 1937.

10.5 Anatomy of the small intestine of Pilosa, Vermilingua

Fig. 3.25: Right side of the opened stomach of Tamandua tetradactyla. Adapted from Böker (1937).

The length of the total small intestine of Tamandua tetradyactyla amounts to 420.5 cm (100%) according to Ferreira et al. (2011). The duodenum is 12.78 cm long (3%), the jejunum 191.42 cm (45.5%), and the ileum 216.28 cm (51.4%). A clear demarcation between the caecum and the colon was not found in T. tetradactyla. In the region of the caecocolic junction, branches of the cranial and caudal mesenteric arteries anastomose. Some remarks on their anatomical findings show that the authors are not accustomed to aspects of comparative anatomy. For example, it is the visceral, not the parietal, peritoneum that surrounds the intestines. Some of the statements made by Ferreira et  al. (2011) are difficult to understand. What does it mean that the cranial mesenteric artery “is ventral to the celiac trunk” (page 493)? It branches off from the

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 III Xenarthra – 10 Pilosa, Vermilingua

­abdominal aorta caudal of the truncus coeliacus. On the same page, another rather enigmatic sentence can be found: “The mesentery of T. tetradactyla is different from that of other vertebrates recently described in the literature. This animal exhibits a basic vascular pattern relative to the ontogeny of vertebrates”.

10.6 Anatomy of the colon of Pilosa, Vermilingua A comparison of the relative length of two vermilinguans has been made possible by different authors: Rezende de Souza et al. (2010) studied the large intestine of Myrmecophaga tridactyla, which weighs approximately 22 kg (Silva and Downing, 1995) and has a total large intestinal length of 132.6 cm (100%). The caecum is 9.6 cm (7.2%), colon descendens 37.6 cm (28.3%) and colon transversum 85.5 cm (64.4%). The Tamandua tetradactyla, with an approximate body weight of only 5 kg (Silva and Downing, 1995), was studied by Rocha Mortoza et al. (2013): the length of the total large intestine is 59.35 cm (100%), caecum 8.21 cm (13.8%), colon descendens 43.5 cm (71.3%), rectum 7.64 cm (12.9%). Information on the transverse colon is not given in this latter publication.

10.7 Anatomy of the caecum of Pilosa, Vermilingua Illustrations and descriptions of the caecum are very limited in the Vermilingua; only the southern tamandua, Tamandua tetradactyla, and the giant anteater, Myrmecophaga tridactyla are depicted. Mitchell (1905) shows the ileocolic region of Tamandua tetradactyla (Fig. 3.26). The vestigial caecum lies on the mesenterial side of the gut. The V.  mesenterica posterior drains the caecum together with the colon. Illustrations of the ileocolic region in Myrmecophaga tridactyla have been published by Huntington (1903) and Rezede de Souza et al. (2010) (Fig. 3.27). According to Huntington (1903), a change in gut calibre can be observed at the site where the ileum enters the colon. A direct funnel-like transition of small into large intestine can be seen, and according to that author, there is no caecum, a statement that is understandable

when looking at Figs. 3.27 A and B. Beyond the ileocolic junction, the calibre of the large intestine increases. The terminal ileum is thus implanted into the apex of a funnel formed by the proximal segment of the colon. Rezede de Souza et al. (2010) are of different opinion. They give an illustration of the ileocolic region and mark the small vestigial caecum with an asterisk. In the paper of these Brazilian authors, the vascularisation is not described systematically, but the arcades are differentiated between primary and secondary orders. Blood vessels are not shown in the illustration adapted from Rezede de Souza et al. (2010).

Fig. 3.26: The intestinal tract of Tamandua tetradactyla. Adapted from Mitchell (1905).

Fig. 3.27: Two specimens of the ileocolic region of Myrmecophaga tridactyla. Adapted from: A: Huntington (1903); B: Rezende de Souza (2010).

IV Euarchontoglires

Introductory remarks Together with the Glires (rodents and lagomorphs), the Scandentia or tupaiids or tree shrews, the dermopterans or flying lemurs and the primates form the superorder Euarchontoglires. Within these, recent molecular studies support supraordinal clade, called Euarchonta, including Scandentia, Dermoptera and Primates (Silcox et al., 2005; Janečka et al., 2007). Szalay (1977) speaks of “tupaiid-primate-dermopteran ties”. Especially the tree shrew–primate relationship has led to some confusion. Campbell (1974) writes that tree shrews “are neither primates nor representatives of a group that directly gave rise to primates” (page 139). “The literature on primates and tupaiids is bedeviled with inaccurate statements, frequently a result of misinterpretation of previous writings” (Van Valen, 1965, page 142). For example, Helmstaedter et al. (1977) investigate the stomach “of the Monkey” in a paper dealing with Tupaia belangeri. Van Valen (1965) concludes that a “tupaiid-primate relationship is possible, but unlikely, and that the similarities between recent tupaiids and primates are probably convergences” (page 149).

11 Scandentia Goodman (1966) states clearly that tree shrews are distinct not only from primates, but also from insectivores. In a DNA investigation by Roberts et al. (2009) of the relationships within the Tupaiidae, the result was confusing: Not all species of the genus Tupaia are monophyletic! On the other hand, a compilatory tree published by Olson et al. (2005) shows clear monophyly of the Tupaia species. In a slightly earlier study, the same authors (Olson et al., 2004) reviewed morphological evidence for elucidation of phylogenetic relationships amongst tree shrews. The morphological aspects considered are very limited: different dental characters, skeletal elements of the carpus, as well as presence or absence of the caecum in tree shrew species, are taken into account. However, these authors argue “that the rigorous and critical examination of more characters is desperately needed” (Olson et al., 2004, page 64). According to Helgen (2005a), Tupaia glis has been used as a “wastebasket taxon” (Sargis et al., 2013), but these latter authors showed that there are four species that can be separated from T. glis. Ni and Qiu (2012) describe Late Miocene tupaiid material from southwest China. Tree shrew fossils are extremely rare because “the fossil record of definitive dermopterans and scandentians is extremely limited” (Silcox DOI 10.1515/9783110527735-004

et al., 2005, page 139). Recent Scandentia can be subdivided into two families (Sargis et al., 2013), the Tupaiidae with 19 species in four genera and the Ptilocercidae with one genus and one species (Ptilocercus lowii, the pen-tailed tree shrew) (Helgen, 2005a). According to this author, the Tupaiidae comprise 15 species of the genus Tupaia, as well as Anathana ellioti (Madras tree shrew), 2 species of Dendrogale (D. melanura and D. murina, Bornean and northern smooth-tailed tree shrew) and Urogale everetti (Mindanao tree shrew). According to Sargis (2004), Ptilocercus lowii is quite distinct from all other Tupaiidae and shows more plesiomorphic characters than the other tupaiids, which are diurnal animals and partly adapted to an arboreal and climbing way of life. Although Ptilocercus also lives on trees, it is nocturnal (Campbell, 1966; Holst, 1988). As Tupaia balangeri is susceptible to infection with human hepatitis B virus (Cao et al., 2003), this species is used as model for biomedical research. Feldhammer et al. (2007) give a succinct account of the geographical distribution of tree shrews: They are restricted to the Oriental faunal region, ranging from India, southern China, and the Philippines southward through Borneo and the Indonesian islands (map in Roberts et al., 2009). Throughout their range, tree shrews occur in forested habitats up to an elevation of 2400 m. In the list of threatened species published in 2012 by the International Union for the Conservation of Nature (IUCN) (http://www.iucnredlist. org/initiatives/mammals/analysis/red-list-status), information on the status of the Scandentia species is given: In two species the status of conservation is not known and three species have stable populations. However, 15 species show a decreasing tendency, in most cases because of manmade degradation of habitats by excessive deforestation activity in Southeast Asian tropical forests. Tree shrews or Scandentia are widely distributed in Southeast Asia and inhabit a wide range of arboreal, semi-arboreal, and forest floor niches. tree shrews arose approximately 63 million years ago (Janečka et al., 2007). According to Thenius and von Holst (1988), the greatest species richness of tree shrews exists on Borneo. The first scientific record of a representative of the mammalian order Scandentia, which only lives in Southeast Asia (Roberts et al., 2009), can be found in accounts of the third – his last – voyage of Captain Cook (1776–1779) (Makita et al., 1996), but much more recently, Emmons (1991) still writes: “Ecologically, tree shrews (Scandentia, Tupaiidae) are one of the most poorly known orders of mammals” (page 642). Despite extensive morphological descriptions and behavioural studies in captivity, understanding of their ecological roles does not allow comparison with other mammalian orders. Concerning their biotope, some

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differentiation is possible: Ptilocercus lowii (pen-tailed tree shrew), Dendrogale melanoleuca (Bornean smoothtailed tree shrew) and Tupaia minor (pygmy tree shrew) live exclusively on trees, most other species spend considerable time on the ground. In DNA investigations of tree shrews (Roberts et al., 2009), little evidence was found to precisely root them. Thenius and von Holst (1988) mention that the Scandentia, compared with insectivores, have a more developed brain, a primate-like auricle and a bony ring about the eyes, which are positioned laterally. These and other characters made Simpson (1945) and Campbell (1966) believe that tree shrews belong to primates (lemurids). Hafleigh and Williams (1966) even call the tree shrew a true primate. It has already been mentioned that Scandentia are separated form insectivores and primates, and they are distinctive rather than related to either primates or insectivores (Goodman, 1966). As frugivores, tree shrews play an important role ecologically as seed dispersers. Shanahan and Compton (2000) mention that seeds that had been ingested by tupaias and had passed their digestive tract had practically all germinated after 4 days when voided by the animals.

11.1 Food of Scandentia Tupaia belangeri, the northern tree shrew, is the most abundant species under the order Scandentia (Yamada et al., 1999). Different species of tree shrews (Tupaia spp.) studied in the field in Sabah, Malaysia, by Emmons (1991) show intense frugivory, which is concentrated on small and soft fruits. For example, Tupaia longipes (long-footed tree shrew), T. tana (large tree shrew) and T. glis (common tree shrew) chew fruits, drink the liquid and spit out the fibre (Emmons, 2000); they reject indigestible fibres and other parts of fruits before swallowing the pulp (Emmons, 1991). Tree shrews like Ptilocercus lowii (pen-tailed tree shrew), Tupaia  minor (pygmy tree shrew), T.  gracilis (slender tree shrew), and T. longipes do not only eat fruit, but also eat invertebrate animal material (Emmons, 2000). The widest range of this type of food is eaten by T. tana. In contrast to their frugivory, the tupaiid species show strong differences in relation to composition of their food. For example, P.  lowii and T.  tana seem to be less drawn to fruiting trees than the other species. A comparison of what tree shrews eat with what is presumably available, shows that tree shrews generally eat the most common and easily available arthropods. Ants are by far the most numerous litter-fauna arthropods, and they are also the most frequent prey in the diets of terrestrial Scandentia. Beetles and spiders are likewise important in both in the habitat and in scat samples (Emmons, 2000).

Tree shrews eat a wide range of diverse diets (Gingerich, 1992); they are omnivorous – feeding on different fruits and invertebrates – as well as frugivorous (Yamada et al., 1999). Emmons (2000) studied six species of tree shrews in Borneo, one representative of the subfamily Ptilocercinae: Ptilocercus lowii, and five of the subfamily Tupaiinae: Tupaia minor, lesser tree shrew, T. gracilis, slender tr., T. longipes, plain tr., T. montana, mountain tr., T.  tana, large tr. These studies produced broad-based information on the food of tree shrew species, which is interspecifically variable. Generally, they eat fruit, but invertebrate foraging seems to supply the real staple; grasshoppers, crickets, spiders, beetles, caterpillars, ants, termites, millipedes and centipedes are taken. When eating food material, the lesser tree shrew, Tupaia minor, and the slender tree shrew, T. gracilis, treat seeds so delicately that they function as seed dispersers (Shanahan and Compton, 2000). In the pentail tree shrew (Ptilocercus lowii), food consists of insects and fruits, but this species is probably less insectivorous, as Lyon (1913) mentioned. Occasionally, meat is also eaten by this species (Liat, 1967). Emmons (1991) mentions that transit times of fruit through the gut are rapid and body size-dependent. For example, in the pygmy tree shrew, Tupaia minor (~60g body mass), the first defecation of marker dye can be observed after 13 to 29 min; in the large tree shrew, Tupaia tana, with a body mass of 220 g, it takes between 38 and 73 minutes before dyed particles appear. Another interesting aspect of the food has been described by Wiens et al. (2008) for the pen-tailed tree shrews (Ptilocercus lowii). These animals consume nectar of a palm species (Eugeissona tristis) that harbours a fermenting yeast community. The authors recorded a maximum alcohol concentration of 3.8% (mean, 0.6%; median, 0.5%), which is amongst the highest ever reported in a natural food. Yet, the flower-visiting tree shrews showed no signs of intoxication. They “might have developed…tolerance for fermented palm nectar over the course of up to 55 My” (Roberts et al., 2011, page 370). According to Wiens et al. (2008), it is yet unclear to what extent tree shrews benefit from ingested alcohol per se and how they reduce the risk of continuous high blood alcohol concentrations.

11.2 Gastric anatomy of Scandentia Tree shrews have a unilocular simple stomach without any squamous non-glandular mucosal lining. Emmons (2000) stated in her detailed book on tupaiids that “the stomach is simple”; no further information was given. Also, in papers from the 19th and 20th century (Oken, 1838;

11 Scandentia 

Owen, 1868; Flower, 1872; Lyon, 1913; Campbell, 1974), no further comments on gastric anatomy were given, even in papers that dealt with other sections of the digestive tract. Neither data on the macroscopic anatomy of the stomach of Scandentia nor illustrations are available in the literature, but some information on the histology has beeen published by Müller (1971), Helmstaedter et al. (1977) and Yamada et al. (1999). Yamada et al. (1999) found a group of endocrine cells in the stomach. This group included endocrine cells immunoreactive for gastrin, bovine pancreatic polypeptide, somatostatin, pancreatic glucagon and enteroglucagon. It is possible that serotoninimmunoreactive cells might play an important role in the peripheral regulation of gastric acid secretion together with other gut hormones. Helmstaedter et al. (1977) depict the unequally distributed glucagon-, somatostatinand gastrin-immunoactive cells in the gastric mucosa of Tupaia belangeri: The fornix houses the glucagonimmunoreactive A cells. HCl secretion and gastric motility is reduced by glucagon (Thews et al., 1991). Gastrin immunoreactive G cells can be found in the antrum pyloricum; these are cells stimulating HCl secretion. Yamada et al. (1999) mention that there is a considerably large number of gastrin-immunoreactive cells in the pyloric region. Somatostatin-immunoreactive D-cells negatively influencing gastrin secretion, can be found both in the fornix and in the pyloric antrum. Müller (1971) counted mucous neck cells, parietal cells and chief cells along the greater curvature of the stomach in four individuals of Tupaia glis between the cardia and the pylorus. From his data three diagrams were drawn that represent these cells as percentage of the total number of each separate cell type (Fig. 4.1). The English terminology (Müller’s paper is written in German) of cell types is  applied according to Hamilton and Mossman (1972) and Nickel et al. (1973). Tendencies in the distribution of cell types become visible: Mucous neck cells can be found in all three gastric region, but the pyloric region is free of parietal and chief cells. The highest numbers of parietal cells can be found in the corpus region, whereas chief  cells  are found in high numbers in the fornix of Tupaia glis.

11.3 Anatomy of the small intestine of Scandentia The information concerning the small intestine of Scandentia is very limited. Agungpriyono et al. (1999) published a short paper on measurements of the intestine in Tupaia javanica (Horsefield’s tree shrew): stomach 4.2 cm and total intestine 44.94 cm (100%), comprising the

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small intestine 37.5 cm (83.4%), caecum 0.98 cm (2.2%), and large intestine 6.46 cm (14.4%). The mucosal surface of the small intestine showed mucosal folds and intestinal villi. The intestinal villi varied in their shape, size and density depending on the portions of the intestine (Agungpriyono et al., 1999). The density of the villi was high in the duodenum. The shape of each villus of the intestine was leaf- or tongue-like in the duodenal and jejunal parts and low thick column-shaped or ridge-like in the ileal part. The height of the villi decreased towards the caudal portion. Uhr et al. (1993) studied 10 specimens of Tupaia belangeri and found a mean of 15 ± 1 Peyer’s patches in the small intestine, usually on the antimesenteric. The patches represent about 3% of the small intestinal surface.

11.4 Anatomy of the colon of Scandentia Makita et al. (1998) found a length of 4.0 to 5.5 cm of the large intestine of “all tree shrews examined”. The small intestine is considerably longer (59–67 cm) than the large one. Agungpriyono et al. (1999) differentiated only the colon descendens in Tupaia javanica. For the common tree shrew, Tupaia glis, Starck (1958) published an in situ illustration of the extremely short and straight colon (Fig. 4.2). This section of the gastrointestinal tract runs, situated slightly to the right of the midline and starting directly under the stomach, in caudad direction, not forming bends and without morphological subdivisions. It has a short mesocolon, which cannot be seen in the picture. The sketchy outline of the large intestine published by Straus (1936) gives practically the same impression (top line of Fig. 4.3). Hill (1958) published similar sketches for two species of Scandentia, Tupaia sp. and Ptilocercus lowii, the pen-tailed tree shrew.

11.5 Anatomy of the caecum of Scandentia In the Euarchontoglires, there is a high variability of – sometimes very prominent and voluminous – caeca. Only a few examples are represented in Tab. 4.1. The anatomy of Indonesian tree shrew (Tupaia javanica) has been compiled by Makita et al. (1996). Anatomical research papers of Tupaia so far published deal with retina, testis, spleen, pineal gland, alimentary canal in general, arteries, and placenta. Evolution of haemoglobulin, gene mapping, DNA analysis, plasma enzymes, and others topics have also been documented bibliographically by the same authors. No detailed papers about the anatomy of Tupaia

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Fig. 4.1: Three mucosal gastric cell types expressed as percentage of all counted cells of that type in Tupaia glis. Adapted from Müller (1969).

have come to the knowledge of the present author; Makita et al. (1998) gave measurements of a small diverticulum, which is possibly a “primitive form of a caecum”. He found a diameter of 0.25 to 0.40 cm and a length of 0.7 to 1.2 cm of that structure.

According to Flower (1872), the Tupaiidae are separated from Insectivora (Lipotyphla) by the possession of a short simple caecum. Emmons (1991) mentions that the intestines of species of the genus Tupaia consist of a long small intestine, rudimentary or no caecum, and a greatly

11 Scandentia 

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Fig. 4.2: The large intestine of the common tree shrew (Tupaia glis). Modified after a situs illustration by Starck (1958). Tab. 4.1: Caeca of five orders of Euarchontoglires. The numbers refer to: 3. Tullberg (1899), 4. Huntington (1903), 7. Böker (1937/1967), 8. Jacobshagen (1937), 9. Starck (1958), 10. Gorgas (1967), 11. Schultz (1972), 14. Snipes (1981). Order

Suborder

Scandentia

Tupaiidae

Dermoptera

Cynocephalidae

Primates

Strepsirrhini

Primates

Haplorrhini

Rodentia

Sciuromorpha

Rodentia

Castorimorpha

Rodentia

Myomorpha

Rodentia

Anomaluromor

Rodentia

Hystricomorpha

Lagomorpha

Caecum

Fig. 4.3: The large intestine in the Tupaia and 13 species of primates. Adapted from Straus (1936).

reduced, narrow, smooth colon. In Tupaia tana, the large tree shrew, Flower (1872) was unable to find a caecum. “The statement of the presence of a caecum as a family character, therefore, requires modification” (Flower, 1872, lecture VII, page 2). Other species have a small, simple, narrow pouch (Lyon, 1913). This author found a caecum in Tupaia belangeri, the northern tree shrew, and T.  splendidula, the ruddy tree shrew. The mean caecal length of 8 measurements in 7 species is approximately 1 cm. Lyon (1913) states that this cannot be called “a ‘large caecum’ and can scarcely have any definitive function” (page 14). From older literature, the author cites that the genus Anathana (Madras tree shrew) possesses a long and narrow caecum with a length of about 3 cm. Kakuni et al. (2002) measured and depicted the caecum of Tupaia javanica (Horsfield’s tree shrew, Fig. 4.4). This species has a body weight of 71.5 ± 10.2 g, the length of the small intestine is 60.8 ± 3.9 cm, the large intestine 5.0 ± 0.6 cm (diameter 0.4 ± 0.0 cm), and the diverticulum 0.9 ± 0.2 cm (diameter 0.3 + 0.2 cm). Compared to the ileum and colon, the caecum is generally without intestinal villi and lymphatic nodules. An overview of possible differentiations of the caecum in Scandentia has been compiled by Hill (1958).

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Fig. 4.4: The caecum of Tupaia javanica. Adapted from Kakuni et al. (2002).

His presentation is based on a multitude of authors, but here reference will be made to the compilator. The shape of the caecum in different species is variable. A moderate caecum is found in Tupaia glis (Common treeeshrew) and T. splendidula, but in T. tana, a caecum is absent. In the only species of the Ptilocercidae, Ptilocercus lowii (pen-tailed tree shrew), a short (8 mm) “embryonic” conical caecum is retained. Here, the ileum empties into the right wall of the colon at the base of the caecum, the angle between the latter and the ileum being crossed by a short, triangular peritoneal fold, the “mesotyphlon”. There is a faint constriction at the base of the caecum, but no caecocolic sphincter muscle. In Tupaia tana, the hindgut is capacious, especially at its cranial end, with the caecum represented merely by a bulge of the anterosinistral wall. In contrast to this, Anathana ellioti exhibits an elongated cylindrical caecum of more or less uniform calibre with a rounded, blunt apex.

11.6 Short remarks on digesta transit in Scandentia Emmons (1991) determined transit times of fruit through the gut of different species of tree shrews. Mean times to first defecation of marker dye are after about 20 min (range, 13–29 min) in Tupaia minor (60 g mass) and 57 min (range, 38–73 min) in Tupaia tana (220 g mass). The rapid food transit times for tree shrews are probably linked to the narrow diameter (small volume) of the entire tract and lack of fermentation chambers (Chivers and Hladik, 1980). Judging from the wet consistency of their faeces, tree shrews do not strongly resorb water from their digesta.

12 Dermoptera 12.1 Introductory remarks For both species of the Dermoptera or flying lemurs, the term “colugo” has been applied (Gray, 1870; Stafford, 2005;

Lim, 2007; Lim et al., 2013). Flying lemurs have been characterised as “most enigmatic mammals” by Janečka et al. (2008). The reason for this seems to be the still controversial systematic position of this eutherian order. Nie et al. (2008) write: “Scandentia and Dermoptera have a closer phylogenetic relationship to each other than either of them has to Primates” (page 1). Nevertheless, Dermoptera are living relatives of Primates (Janečka et al., 2007), and the two surviving species, Cynocephalus volans, the Philippine flying lemur, and Galeopterus variegatus, the Sunda flying lemur (Stafford, 2005), are probably separated from each other since about 20 Mya, i.e. the Miocene. Dermoptera and Primates can probably be derived from a common phylogenetic root (Thenius and Kraft, 1988), but they have a very restricted palaeontological documentation. Dermopterans represent, together with tree shrews (Scandentia), the closest outgroup of the primates (Marivaux et al., 2006). According to Rose (2006), only one single fossil, Dermotherium from Thailand, has been documented as dermopteran. This fossil indicates that dermopterans may have diverged from other mammals by the end of the Eocene. Because of their geographic distribution in continental Southeast Asia, as well as on the islands west of the Wallace line, Olson et al. (2005) and Miravaux et al. (2006) compile Dermoptera and Scandentia as “Sundatheria”. According to Silcox et al. (2005), both orders are of Asian origin. The great antiquity of the order Dermoptera – late Eocene of Thailand (Miravaux et al., 2006), or even from the early Palaeocene (Rose, 1975; Ni et al., 2008) – combined with their modern geographic range, indicate a relictual distribution of the flying lemurs. The two surviving species are geographically clearly separated: Cynocephalus volans lives on the southeastern islands of the Philippines, Galeopterus variegatus inhabits the islands of the Sunda Shelf area and the Southeast Asian mainland (Stafford and Szalay, 2000). Both species are inhabitants of tropical forests. For example, for Galeopterus variegatus, a 95% forest canopy cover is necessary for survival (Lim et al., 2013). Stafford and Szalay (2000) state that both species are morphologically and ecologically distinct. Cynocephalus has a more robust masticatory apparatus and might be better adapted to shearing with the anterior (premolar and canine) dentition and vigorous molariform chewing. Galeopterus, on the other hand, has a more gracile masticatory system and appears adapted to shredding or puncturing with the anterior dentition and to crushing with the molariform dentition. Stafford and Szalay (2000) propose the idea that it may be useful to designate four subspecies of Galeopithecus variegatus: G.  v.  variegatus from Java and its surrounding islands, G.  v.  temminckii from Sumatra, as well as from islands close by, G.  v.  bornanus from Borneo and

12 Dermoptera 

surroundings, and G.  v.  peninsulae from the Malay Peninsula, mainland Southeast Asia, and associated islands. On the other hand, Cynocephalus variegatus is not subspecifically subdivided.

12.2 Food of Dermoptera The main food of calugos is of plant origin (Kuo, 2000); no material of animal origin is eaten; both species of this order are strictly florivorous. The diet of Cynocephalus volans, the Philippine flying lemur, consists mainly of leaves, buds and flowers from a variety of tree species. Most of the time, they prefer young leaves because these contain higher nutritional value than old leaves. Dermopterans also might eat fruits and sap. They use their enlarged tongue and specialised lower incisors to pick leaves. Wischusen and Richmond (1998) observed that Cynocephalus volans heavily used young leaves at the end of branches for food. Peaks in foraging occurred just after sunset and a few hours prior to sunrise. Although Harrison (1961) uses unclear nomenclature, it is probable that he investigated Galeopterus variegatus. The investigated stomachs contained fragment of leaf only and this plant material represents 100% of the gastric contents. The same species was also studied by Lim (2007) in Singapore. He lists seven native trees, of which the flying lemurs feed on young leaves, as well as flower buds.

12.3 Gastric anatomy of Dermoptera The stomach of the Sunda flying lemur, Galeopterus variegatus, which, according to Wallace (1869), represents a large organ, is strongly lengthened by extension of both the cardiac and the pyloric region (Leche, 1886, Fig. 4.5, upper panel). This corroborates the description given by Chapman (1902), who speaks of an elongated and drawn out organ, which resembles that of Pteropus sp., the flying fox (Chiroptera). The cardiac region represents a blindsac and is shorter and wider than the pyloric region, which is separated from the small intestine by a prominent incisure and a prominent pyloric valve. In a specimen of Cynocephalus volans with a body length of 42 cm, Wharton (1950) determined a stomach length of 25.4 cm (60%), and a fornix (?) that had a length of 7.6 cm (18%). (The whole intestinal tract had a length of 335 cm and the caecum was 48.3 cm long.) An excellent description of the stomach and its arterial supply in the Philippine flying lemur (C. volans) was published by Schultz (1972) (Fig. 4.5, lower panel): The stomach is long and has a large fornix. On the lesser curvature, there is

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a sharp incisura angularis, and on the greater curvature, there is an incisure opposite to the entrance of the oesophagus. The pyloric region is long and extended and has a relatively small diameter. Leche (1886) gives some information on some characteristics of the tunica mucosa of Galeopterus variegatus and Chapman (1902) of Cynocephalus volans. In both species, the mucous membrane of the cardiac region is smooth and that of the pyloric region is characterised by prominent folds running parallel to the organ’s longitudinal axis (Chapman, 1902). In the oral section of the pyloric region, prominent folds are formed by the mucosa, most of them parallel to the longitudinal axis of the stomach (Leche, 1886). Some of these folds continue the course of oesophageal folds. In both species, the part immediately orad of the pylorus has no folds and is smooth (Leche, 1886; Chapman, 1902).

12.3.1 Arterial supply of the stomach in Cynocephalus volans (Schultz, 1972) The description of the arterial supply of the stomach of Cynocephalus volans will completely refer to the excellent account and illustration (Fig. 4.5, lower panel) given by Schultz (1972). This was translated from German by the present author: Within the abdominal cavity, three unpaired branches of the aorta abdominalis (1) can be differentiated: the A. coeliaca (2), A. mesenterica cranialis (10) and A. mesenterica caudalis (12). Between the two Aa.  mesentericae lie the two Aa. renales (11) to the kidneys. The A. coeliaca (2) divides into three branches, the A. lienalis (3), A. gastrica (5) and A. hepatica communis (6). The A. gastrica (no separation into right and left A. gastrica) supplies the stomach in the region of the lesser curvature with many branches. The A. hepatica communis (6) runs to the liver via A. hepatica propria (7) and with a second branch (8) to the pylorus; this branch continues as A.  gastroepiploica dextra (9). The A. lienalis (3) supplies the spleen, as well as the fornix gastricus (4). Branches from both the A.  gastroepiploica dextra (9) and the A. lienalis (3) supply the hindgut.

12.4 Anatomy of the small intestine of Dermoptera The midgut of the flying lemur, Cynocephalus volans, has villi intestinales (Schultz, 1972). At the beginning of the small intestine, they are flattened and can be found in a zigzag arrangement perpendicular to the longitudinal axis. Further aborad the villi become more finger-shaped. The tunica muscularis of the midgut is similar to that of other mammalian species.

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Fig. 4.5: Stomachs of two species of Dermoptera. Schematic tree of arteries is also given. Adapted from Leche (1886) and Schultz (1972).

12.5 Anatomy of the colon of Dermoptera The intestines are long and convoluted – according to Kuo (2000), they can approach 4 m in length. The illustration published by Schultz (1972) of the gastrointestinal tract of Cynocephalus volans depicts the arterial supply of the different sections of the gastrointestinal tract. The arterial branches are shown in Fig. 4.6. It should be clearly stated that the delineation of different sections from each other could only be established with the help of arteries depicted

by Schultz (1972) as well as with his detailed comments. The most distal branch of the A. mesenterica cranialis of Cynocephalus volans supplies the proximal colon (colon ascendens with taeniated and haustrated walls, seen between arrowheads “1” and “2” in Fig. 4.6). The following colon transversum or intermediate colon, which is free of taeniae and haustra (between “2” and “3”), is supplied by a more proximal branch of the A. mesenterica cranialis. It is very uncommon for mammals (Schultz, 1972) that an extension of the A. lienalis supplies the colon descendens

12 Dermoptera 

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Fig. 4.6: The gastrointestinal tract of Cynocephalus volans, the flying lemur. Modified after an illustration by Schultz (1971). Between pylorus and 1: small intestine; between 1 and 2: Colon ascendens or proximalis; between 2 and 3; Colon transversum or intermedium; between 3 and 4: Colon descendens or distalis.

or distal colon (between “3” and “4”). The short rectal section obtains its arterial blood from branches of the A. mesenterica caudalis. Between the caecum and the colon of the flying lemur; a sphincter can also not be found and there is no clearly discernible border between both sections of the large intestine, caecum and colon. The short proximal colon is, together with the caecum, characterised by taeniae and haustra. However, more than 80% of the colon have a smooth wall without taeniae and haustra and with a narrow diameter similar to that of the small intestine.

12.6 Anatomy of the caecum of Dermoptera According to Schultz (1972), the caecum of Cynocephalus volans is well differentiated and strongly haustrated; the lumen is subdivided by taeniae and haustra (Fig. 4.6), but the last five-sixths of the colon do not have these differentiations and a sharp border between colon and caecum cannot be observed. Taeniae and haustra can only be found in the proximal colon.

12.7 Functional remarks on the gastrointestinal tract in Dermoptera The Philippine flying lemur, Cynocephalus volans, has a simple gut and a large caecum (Wischusen et al., 1994), combined with short times for passage of digesta (Wischusen and Richmond, 1998). The capacity of the gastrointestinal

tract in the flying lemur ranged from 139.7 to 283.7 g or from 12.7 to 15.0% of the body weight, which is within the range of other herbivores (Parra, 1978). The mean retention time is extremely short in C. volans: 14 h, compared with the data of two other arboreal folivores, namely the forestomachfermenting Bradypus variegatus, the brown-throated sloth (632 h), and the hindgut-fermenter Phascolarctos cinereus, the koala (100–213 h). These differences suggest that the flying lemur has a reduced capability to digest fibre and selects food low in fibre (Wischusen et al., 1994).

13 and 14 Primates General overview The suborder Strepsirrhini comprise 23 genera with 88 species, the suborder Haplorrhini 46 genera and 288 species (Groves, 2005). To obtain a first overview, the differentiation of the gut, represented here as relative volumes of the small intestine, caecum and colon (the sum of all three is considered as 100%, raw data from Chivers and Hladik, 1980) was depicted in a triangular diagram (Fig. 4.7, left panel) for four classes of the food index, which have already been explained in Tab. 1.4 and 1.5. In contrast to the small intestine and the colon, the relative volume of the caecum in the Haplorrhini is always low, but in the Strepsirrhini, the data of Chivers and Hladik (1980) demonstrate for Lepilemur mustelinus (weasel lemur) and L.  leucopus (white-footed sportive lemur) – both species are omnivores – the caecum is relatively

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Fig. 4.7: Food index, as defined by Langer (2008), compare with Tab. 1.4, and relative volumes of three sections of the digestive tract (as published by Chivers and Haldik, 1980) in the two suborders of primates.

voluminous. It is worth mentioning that the florivorous primates (food index > 100) all have a relatively small caecum, but can have a voluminous colon, i.e. they are not caecum digestors. Although the data from Chivers and Hladik (1980) for haplorrhine species indicate that the caecum is relatively small, measurements of volumes by Milton (1981) show a caecum that comprises more than 40% of the gut in Alouatta palliata (mantled howler) and even about 75% in Ateles geoffroyi (Geoffloy’s spider monkey). It is not possible to determine whether any of the two sets of data is based on incorrect measurements. Omnivorous strepsirrhine species – not the strict herbivores! – tend to develop a caecum with relatively large volumes. These are characterised by a body mass between 100 and 1000 g (Fig. 4.8). These findings indicate that the primate caecum is not a differentiation related with high body mass nor with low food quality. Information on the morphology of the caecum in primates is extremely unbalanced and the number of papers dealing with the comparative anatomy of that organ is very limited. The anatomy of the caecum in non-hominid primates has been investigated and presented systematically in publications by Owen (1866), Flower (1872) and Hill and Rewell (1948); more recent papers deal with very few, or even only one species. In his excellent review, Hume (2002) indicates that omnivores can have a caecum in which microbial fermentation takes place. A caecum, which is set off from the net oral-aboral flow of digesta, can represent a “safe harbour” for microbes, which, together with fine digesta particles, may be “washed back” from the proximal colon into the caecum (Hume, 2002). It has to be mentioned again that the haplorrhine digestive tracts considered here do not have a relatively voluminous caecum. Measured volumes give a good idea about the sites where digesta are handled and to what degree the different sections of the tract can contribute to digesta retention. However, in many investigations, only data on the length of gut section

is supplied without consideration of the diameter of calibre. When we consider the relative length of the small intestine, caecum and colon in some Primates (Starck, 1958) (Fig. 4.9), the caecum does not play a considerable role, at most arising to 20% of the relative length in the total gut. The above creates the impression that the caecum in primates is not a functionally important organ during the digestive process. Amerasinghe et al. (1971) collected data on the internal surfaces of the stomach and on the small and large intestines (the latter not differentiated between the caecum and the colon) (Fig. 4.10). In a species of the Strepsirrhini (Loris tardigradus, red slender loris), two forestomach-digesting haplorrhine species (Trachypithecus vetulus, purple-faced langur, and Semnopithecus entellus, northern plains grey langur) and a species with a one-chambered (unilocular) stomach, Macaca sinica, (Toque macaque), it is demonstrated clearly that the large intestine provides around 30% of the surface of the total gastrointestinal tract. As the internal surface is related with the ability to absorb products of the digestive process, one can argue that large intestine, consisting of the colon and caecum, is of similar importance in the species investigated by Amerasinghe et al. (1971), i.e. in species that might practise alloenzymatic forestomach fermentation and in those where only autoenzymatic digestion takes place. A comparison of two illustrations, one for the Strepsirrhini (Fig. 4.11) and one for the Haplorrhini (Fig. 4.12), both based on the publication by Hill and Rewell (1948), as well as a third illustration (Fig. 4.13), which compiles drawings that were originally published by Owen (1866) and Flower (1872), gives a “generalised” impression of caecal differentiations. In the Strepsirrhini, the organ is relatively long, slender and narrow, for example, in the brown greater Galago, Otolemur crassicaudatus. The caecum can even be curled spirally as in Lepilemur mustelinus (weasel lemur). In Varecia variegata (black-and-white ruffed lemur), the caecum is not only spiralled in a two-dimensional plane,



13 and 14 Primates 

Fig. 4.8: Body mass and relative volumes of small intestine, caecum and colon (as published by Chivers and Haldik, 1980) in the two suborders of Primates.

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Fig. 4.9: Percentages of the length of the total gut, represented by small intestine, caecum and colon. Raw data on the gut regions are from Starck (1958).

Fig. 4.11: Caeca in Strepsirrhini: Lemuriformes (black). Compiled from Hill and Rewell (1948).

Fig. 4.10: Internal surface of small intestine, caecum and colon as percentages of the surface of the whole gastrointestinal tract in four primate species. Black symbols: Haplorrhini; white symbol: Strepsirrhini. Adapted from Amersasinghe et al. (1971).

but forms a three-dimensional shape. Eulemur macaco (black lemur), on the other hand, represents a strepsirrhine primate with a zigzag caecal shape. In some haplorrhine species, we can also find a long, slender and narrow caecum (e.g. Tarsius bancanus, Horsfield’s tarsier, or Pithecia monachus, monk saki). The caecum in the two families Hylobatidae (gibbons and siamangs) and Hominidae

(gorilla, orangutan, bonobos, chimpanzees and man) (Fig. 4.12) as well as in the caecum is relatively short and voluminous. On its apex of Hylobatidae and Homindae, a special differentiation, the appendix vermiformis, can be found. After a few examples of caecal differentiations have been depicted and were briefly described, the morphology of the primate digestive tract will be presented in the order according to Groves (2005). In the following morphological description, the present author will mainly refer to information that was originally supplied by Hill and Rewell (1948).

13 Strepsirrhini (“wet-nosed” primates) 13.1 Introductory remarks The Strepsirrhini or wet-nosed primates are subdivided into three infraorders and 88 species (Groves, 2005): The Lemuriformes comprise four families, the Cheirogaleidae



Fig. 4.12: Caeca in different species of Haplorrhini (black). Compiled from Hill and Rewell (1948).

(21 species), Lemuridae (19 sp.), Lepilemuridae (8 sp.) and Indriidae (11 sp.). The second infraorder, the Chiromyiformes, comprises only one family, the Daubentoniidae (1 sp.). The third infraorder, the Lorisiformes, has two families, the Lorisidae (9 sp.) and Galagidae (19 sp.). Recent strepsirrhines live in the tropics of the Old World: Lemuriformes and Chiromyiformes inhabit Madagascar, but the Lorisiformes can be found in Africa and southeast Asia (Hoffmann, 2012). In addition to extinct fossil families, Strepsirrhini belonging to the family Lorisidae have been found in late Eocene deposits at Fayum in Egypt, dated about 36 MYBP. They appear to be the oldest strepsirrhines yet discovered worldwide (Simons, 1998). Hoffmann (2012) gives information on the distribution and time range of fossil genera of the Strepsirrhini.

13.2 The food of Strepsirrhini According to Kirk and Simons (2001), dental studies on fossils demonstrate a remarkable dietary diversity. Some

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Fig. 4.13: Caecal region in Primates (black). Adapted from A: Owen (1866); B–E: Flower (1872).

strepsirrhines specialised on insectivory, but also frugivores can be found, as well as combinations of frugivory with insectivory and even strict folivory. Cristoffer (1987) generalised by stating that a small body size can be correlated with insectivory, whereas a large body size correlates with folivory. For example, Hladik (1967) showed that Microcebus murinus (grey mouse lemur, approximately 0.05 kg body weight) and Arctocebus calabaresis (golden angwantibo, approximately 0.4 kg) (Fig. 4.14) prefer insects and Avahi laniger (eastern wooly lemur, approximately 1.2 kg) and Lepilemur mustelinus (weasel lemur, approximately 1.0 kg) are more folivorous. Information showing similar tendencies has been published by Milton (1986). Using information on the food index, as listed in Tab. 1.4, a boxplot diagram for Strepsirrhini and Haplorrhini was compiled by the present author in Fig. 1.7. It shows considerable variability for both suborders between insectivory (low food index) and folivory (high food index); a clear tendency cannot be differentiated. The following discussion of different families, genera or species will be more informative.

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Fig. 4.14: Percentages of leaves, fruits and insects in Lorisiformes (bold type, open rings) and Lemuriformes (normal type, black triangles) with mean relative gastric surfaces (given with the species names). Raw data from Hladik (1967).

Data on the types of food eaten by Lemuriformes as well as Daubentonia madagascariensis (aye-aye) and Lorisiformes can be found in the monograph published by Hoffmann (2012); in the latter infraorder, this author speaks of “Loriformes”. Major differences in food choice with respect to protein concentrations, condensed tannins and alkaloids were revealed by Ganzhorn (1988) in chemical analyses of more than 400 plant parts eaten by seven different species of Lemuriformes. On the other hand, insects represent a source of “dense” energy, as Raubenheimer and Rothman (2013) remark. Strepsirrhini can be obligate or occasional insectivores. Typical protein concentration in ants or termites lies at 40 to 60%, which means that insects generally represent high-quality food, but they also vary substantially in quality (Raubenheimer and Rothman, 2013). There are primates that possess chitinases, for example, in the lorisid potto, Perodicticus potto (Stevens and Hume, 1995). Petter (1962) published a table on the food regime of 19 prosimian species, which does not present quantitative information, but shows clearly that genera of the Cheirogaleidae (Microcebus and Mirza, mouse lemurs, Cheirogaleus and Allocebus, dwarf lemurs, as well as Phaner, forkcrowned lemur, live on insects and fruits. The lesser mouse lemur (Microcebus murinus) has generally been described as mainly insectivorous (see remarks above on another species within this genus), with a secondary preference for

fruit, but it also feeds upon flowers and leaves and preys upon a number of small animals, such as spiders, small chameleons, tree-frogs, etc., as well as insects (Martin, 1972). In addition, it has been observed that mouse lemurs feed upon sap exuding from lianes and tree trunks. As early as 1802, Buffon mentions that Lemur catta (ring-tailed lemur) is frugivorous and also eats meat. Leaves are not mentioned in the description. This early description has been differentiated by Martin (1972), who found that species of the genera Lemur and Varecia (ruffed lemur) feed predominantly on flowers and fruits, whilst Hapalemur (bamboo lemur) is more or less folivorous. This latter species specialises on bamboo leaves, but fruits may be eaten on occasion. According to Petter (1962), the following species of the Lemuridae eat fruits and leaves: Varecia variegata (ruffed lemur) and four species of the genus Eulemur: E. macaco (black lemur), E. fulvus (brown), E. mongoz (mongoose), E. rubriventer (red-bellied), as well as Hapalemur griseus (bamboo) and Lemur catta (ringtailed lemur). This information on the latter species has been corroborated by Wilson and Hanlon (2010). Martin (1972) studied the weasel lemur, Lepilemur mustelinus, which is folivorous. In the table compiled by Petter (1962), this species eats leaves and fruits. A similar food is eaten by the Indriidae: The main diet of the Indri (Indri indri), according to Quinn and Wilson (2002) consists of leaves, fruits, and flowers from all levels of the forest canopy. Petter (1962) mentions for Indri indri, Propithecus verreauxi and P. diadema (Sifakas) and Avahi laniger (eastern wooly lemur) that they also eat bark in addition to fruits and leaves. Investigations on Avahi laniger by Norscia et al. (2012) showed a considerable seasonal variation of food composition: From June to August, 100% of the time, adult leaves are eaten; from September to December, young leaves and flowers are also taken. Toxic substances in food can either be completely avoided or they may be “diluted” by ingestion of many different plant species so as not to exceed a toxic threshold concentration. The aye-aye (Daubentonia madagascariensis) is a specialized frugivore and insectivore, feeding upon a range of fruits and concentrating mainly on wood-boring grubs, which are attained by using the specialised rodent-like incisors and the filiform middle finger of the hand (Petter, 1962; Martin, 1972). Pollock et al. (1985) notes that this species also investigates galls to eat insect, for example, beetle larvae. On the other hand, Iwano and Iwakawa (1988) describe how aye-ayes are able to gnaw open the hard ramy nuts and eat the contents of this fruit. In an account of sap-eating and the ingestions of gums, “gummivory” according to Nash (1986), this author writes: “Gums are complex polysaccharides which, like foliage, require fermentation for digestion” (page 113).



Gum feeding has evolved several times in primates and is most prominent amongst nocturnal strepsirrhines. In Phaner sp. (fork-crowned lemur), approximately 65% of the diet consists of gums and in Mirza (Microcebus) coquereli less than 20% of the food consists of gum (Nash, 1986). Kingdon (1971) gives information on the food of Perodicticus potto (potto) with a geographical range from Sierra Leone to Kenya, a species of the Lorisidae: Approximately 60% of the wild potto’s diet is resin, about 30% is insects and the remainder is fruit and other foods” (page 282). The percentage of resins is seasonally very variable. In addition to plant saps, the potto eats a wide range of foods, namely, insects, fruits, leaves, moss, lichens, eggs, molluscs and fungi. Nekaris et al. (2010) corroborates that Perodicticus potto eats saps, but two West and Central African species (Kingdon, 1997, Cole, 2000, Groves, 2005) of Arctocebus do not. Nekaris et al. (2010) also present a list considering ingestion of plants saps – “exudativory” or “gummivory” – by five species of South Asian Lorisidae. Loris lydekkerianus, the grey slender loris, takes sap and another one, L. tardigradus, the red slender loris, does not. In the Galagidae plant exudates, saps and resins, are eaten by many species. For example, Müller (1988) writes that the southern needle-clawed bushbaby, Euoticus elegantulus, which lives in the upper levels of the canopy, ingests a food consisting of up to 75% of tree saps, only 5% consist of fruits and 20% of insects. On the other hand, the same author mentions that Allen’s bushbaby, Galago alleni, from lower forest levels do not take saps in considerable amount, but 73% of the ingesta are fruits and 25% insects. G.  demidoff (Prince Demidoff’s bushbaby) also lives in the lower forest canopy and ingests 10% saps, 19% fruits and as much as 70% of insects (Müller, 1988). Kingdon (1971) characterises this species as primarily insectivorous – 78% of the diet. On the other hand, 18% of stomach contents consisted of gum or resin. Galago moholi, the South African galago, lives on a diet of insects and the gum produced by certain trees, mainly Acacia spp. (Lawes, 2005). Gum is collected from the damaged bark by scraping it from the surface with the help of almost horizontal canines and incisors. The gums consist predominantly of carbohydrates and water, with small quantities of protein and minerals (Nash and Whitten, 1989). The soluble polysaccharides in gum reach the hindgut, where they are digested faster than particles of insect material, allowing this galago to subsist on gums (Caton et al., 2000), which represent an important year-round food resource (Lawes, 2005). The dusky bushbaby, G. matschiei, feeds mainly on fruit and resin during February, but according to Kingdon (1971), the food of animals of that species collected in November, consisted mainly of insects. G.  senegalensis, the Senegal bushbaby, eats a wide range

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of food with considerable seasonal variability (Kingdon, 1971). Most important food constituents are insects. When resins are flowing from Acacia trees (gum arabic), this is a major food item of the Senegal bushbaby. The chemistry of the gums, which are eaten by this species, suggests that “this preference…may relate to the presence of compounds (e.g. flavonoids) having nutritional or hormone-like action” (Nash and Whitten, 1989, page 27). The role of such compounds in foraging selectivity may be complex. According to Kingdon (1971), Otolemur crassicaudatus (brown greater galago) eats fruits, seeds, insects and occasionally vertebrates, as well as resin, but generally relies on a greater extent of fruit. Seasonally, it can subsist largely on plant exudates. When there is a decrease in the availability of invertebrates in winter, this galago species increases gum feeding (Lawes, 2005). Gum is available throughout the year.

13.3 The stomach of Strepsirrhini 13.3.1 Gastric anatomy of Strepsirrhini Mitchell (1905) writes that “ancestral history is at least as important as adaptation to present function” (page 524). Because of this, it seems appropriate to refer to the gastric anatomy of the three strepsirrhine infraorders Lemuriformes, Chiromyiformes (not represented in this chapter) and Lorisiformes, although many sources discuss them jointly. Hladik (1967) presents data (to be found at the species names of Fig. 4.14) that give an impression of the gastric surface in four species of the Lemuriformes (Microcebus murinus, Cheirogaleus major, Lepilemur mustelinus and Avahi laniger, normal print in the ternary diagram), as well as of five species of the Lorisiformes (Arctocebus calabarensis, Galago demidoff, G.  alleni, Euoticus elegantulus and Perodictius potto, bold print in diagram). The triangular diagram characterises the relative importance of leaves, fruits and insects as constituents of the food. The two lemur forms eating mainly leaves have a relatively large internal gastric surface. What is the reason for this relatively large surface? Does fermentation of digesta as well as absorption of fermentation products begin in the stomach or should the absorptive surface be large to avoid that easily digestible material to be submitted to fermentation? As fruits contain high amounts of easily digestible constituents, mainly sugars, most of the lorisiforms and lemuriforms eating considerable amounts of fruits, have large relative gastric surfaces. Hladik (1967) determined the gastric surface in square centimetres relative to the square of the body length (Bl = head + body). Although only a rough approximation, the data in Tab. 4.2, to which food regimes are added (also from Hladik, 1967), they give some impression of the gastric

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Tab. 4.2: Internal gastric surface relative to the square of body length in Strepsirrhini. Relative gastric surface Means Cheirogaleidae

Lepilemuridae Indriidae

Lorisidae Galagidae

Cheirogaleus major Cheirogaleus major Cheirogaleus major Cheirogaleus major Microcebus murinus Lepilemur mustelinus Avahi laniger Avahi laniger Avahi laniger Arctocebus calabarensis Perodicticus potto Euoticus elegantulus Galago alleni Galago alleni Galago alleni Galago demidoff Galago demidoff Galago demidoff Galago demidoff

Lemuriformes 50 56.3 60 40 75 45 45 70 70 60 91.7 95 120 Lorisiformes 30 30 30 30 65 65 60 58.3 65 50 55 43.8 40 35 45

Food Mainly fruits, flowers, grains, insects, no leaves Mainly fruits, flowers, grains, insects, no leaves Mainly fruits, flowers, grains, insects, no leaves Mainly fruits, flowers, grains, insects, no leaves Mainly insects, some fruits, flowers, no leaves Mainly leaves, some fruits, flowers, no insects Mainly leaves, very little fruits, flowers, no insects Mainly leaves, very little fruits, flowers, no insects Mainly leaves, very little fruits, flowers, no insects Mainly insects, some fruits, flowers, insects, no leaves Fruits, flowers, grains, insects, some leaves Mainly fruits, flowers, insects, no leaves Fruits, flowers, grains, insects, no leaves Fruits, flowers, grains, insects, no leaves Fruits, flowers, grains, insects, no leaves Mainly insects, some fruits, flowers, insects, no leaves Mainly insects, some fruits, flowers, insects, no leaves Mainly insects, some fruits, flowers, insects, no leaves Mainly insects, some fruits, flowers, insects, no leaves

Raw data are from Hladik (1967). Taxonomy according to Wilson and Reeder (2005).

absorptive or secretory surface. The Lemuriformes Microcebus murinus and Cheirogaleus major are primarily insectivorous and their relative stomach has a mean surface of 54.00 ± 13.87 cm2/Bl2. Two species (Lepilemur mustelinus and Avahi laniger) are mainly folivorous and the relative surface amounts to 86.25 ± 26.89 cm2/Bl2. Leaves do not play a great role in the Lorisiformes that were measured by Hladik (1967). Two species that are mainly insectivorous (Arctocebus calabarensis and Galago demidoff): 41.00 ± 9.62 cm2/ Bl2 and eaters of fruits and flowers (Galago alleni, Euoticus elegantulus and Perodicticus potto): 54.00 ± 14.75 cm2/Bl2. In Lemuriformes and Lorisiformes, folivores tend to have a relatively larger gastric surface than the insectivorous representatives. Is this fact related with alloenzymatic digestion of plant material in the gastric lumen? Insectivores, on the other hand, eat a food with considerable percentages of easily digestible protein and fats. In this case, the relative gastric surface is relatively small. To obtain an idea of the gastric shape in Strepsirrhini, outlines of this organ, as published by the following authors were compiled in Fig. 4.15: Owen (1866), Flower (1872) and Razanahoera-Rakotomalala (1981). In all cases, the stomach is clearly a unilocular (one-chambered) organ, but the general shape is variable. In Lepilemuridae, like Lepilemur, as well as in the Indriidae (with Avahi laniger), the stomach is elongated and pyriform, with a long pyloric segment (Hill, 1958). On the other hand, a simple, globular sac is the type of stomach found in

the Lemuridae (Eulemur) and the Daubentoniidae and Galagidae (Fig. 4.15). It is not completely clear whether different gastric shapes within one species are the effect of different filling with gastric contents. In Hapalemur, the bamboo lemur, to give an example, there was some variation in the shape of the stomach (Davies and Hill, 1954). They depict a pyriform organ, whilst Campbell et al. (2000) show a stomach of Hapalemur griseus which looks almost “human-like” with a clearly differentiated fornix. This is in full accordance with a photo of the stomach from the same species, which was supplied to the present author by Professor Mike Perrin, School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa (Fig. 4.16). In the Lorisiforms, especially in the Galagidae, cardiac and pyloric orifices lie close to each other and the lesser curvature is very short. These variations may be due to poor fixation, or as has already been mentioned, by different degrees of filling. In the weasel lemur, Lepilemur mustelinus, the organ is elongated. According to Davies and Hill (1954), the incisura angularis cannot clearly be discerned in the outlines of L. edwardsi, depicted in Fig. 4.15. In the wall of the pyloric antrum, two longitudinal muscle bands placed ventrally and dorsally and resembling taeniae coli were differentiated by Davies and Hill (1954) and Hill (1958). These were absent in Hapalemur sp. In the above-mentioned compilatory figure, the stomach of Eulemur macaco (black lemur) is depicted according to Flower (1872). The stomach is rather more elongated than that of Otolemur. An illustration of the “large



13 Strepsirrhini (“wet-nosed” primates) 

Fig. 4.15: Outlines of stomachs of different species of the Strepsirrhini. Adapted from different authors.

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Fig. 4.16: Posterior wall of the stomach of Hapalemur griseus. Photo supplied by Prof. M. Perrin (Pietermaritzburg, RSA).

stomach” (Quinn and Wilson, 2002) of the Indri, Indri indri, is not available. Flower (1872) mentions that the stomach of this species is very short and globular, with a small fundus and a large and distinct pyloric cavity folded back on the lesser curvature, so that the pyloric and cardiac orifices are nearly approximated. In the illustration in Fig. 4.15 of Avahi (wooly lemur), this situation cannot be seen. In addition, Hill (1958) mentions for Avahi, as well as for Propithecus, a distinct tendency to sacculations by virtue of two longitudinal bands along the ventral and dorsal surfaces of the stomach. The second strepsirrhine infraorder, the Chiromyiformes, has only one species in the family Daubentoniidae, Daubentonia madagascariensis, the aye-aye. Two publications by Owen (1866) and Quinn and Wilson (2004) describe the stomach as “simple and subglobular” (Fig. 4.15), and Hill (1958) writes that the aye-aye (Daubentonia) retains a simple subglobular stomach, with the cardia located nearer to the pylorus than to the fundus. According to Owen (1866), it has a length of 8.30 cm. The cardiac orifice lies closer to the pylorus than to the tip of the fornix (the author speaks of the “cardiac end”). Between the cardiac and pyloric orifices, a narrow band of fine “aponeurotic fibres” (Hill, 1958) runs along the lesser curvature, from which fibres of the outer muscular layer radiate. A little beyond the cardia runs an internal, narrow, crescentic mucosal fold transversally to the long axis and divides the cavity partially into distinct cardiac and corpus compartments (Hill, 1958, writes “pyloric compartments”). On the lesser curvature, a torus pyloricus, a short thick longitudinal prominence according to Owen (1866), narrows the pyloric aperture to a subcircular shape. For the brown greater galago, Otolemur crassicaudatus, Flower (1872) remarks that the cardia lies very close to the pylorus. This gives the organ a round, pouch-like shape. According to that author, the stomach is oval with a very large projecting fornix, a detail that is not prominent in the outline in Fig. 4.15. 13.3.2 Internal lining of the strepsirrhine stomach Only very little has been published about the internal mucosal lining of the stomach of Strepsirrhini. For example,

Hill (1958) described a smooth mucosal area that occupies the lesser curvature between the cardia and the pylorus of Lemur and Lepilemur. There are also long, coarse folds radiating in all directions from the cardia, chiefly towards the fundus or fornix. Fayed et al. (2010) give some superficial information about the heterogeneity of proper gastric gland cells, mucous neck and foveolar cells in Nycticebus coucang, the slow lori. Caton et al. (2000) mentions for Galago moholi (Moholi bushbaby) and G. senegalensis (Senegal bushbaby): “The gastric mucosa is folded into longitudinal rugae, which are more numerous in the vicinity of the greater and lesser curvatures” (page 42). The most detailed description on the gastric internal lining is from Davies and Hill (1954), who studied Hapalemur griseus, the grey bamboo lemur. “Except at the pylorus, the wall was relatively thin throughout. The mucous membrane was thrown into radiating folds at the cardiac orifice; these became less distinct and irregular in the body of the organ, giving way in the pyloric antrum to a few poorly developed longitudinal folds” (page 183). The text continues on page 184: “In the cardiac portion and body the gland ducts were short; each received several tubules. The fundic and cardiac glands showed two types of cells”, the chief or proper gastric cells and the much larger parietal or oxyntic cells with central nuclei. “These were not placed between the central cells and the basement membrane, as in man, but abutted directly on the lumen. The parietal cells occurred mainly in the neck and adjacent part of the body of the gland, the deeper portions being composed” mainly of chief cells with “only occasional oxyntic cells. The latter, though plentiful throughout the body of the organ, were most numerous at the cardiac and, but absent in the pyloric part. Here the mucous membrane was thinner, and the glands, tubules and ducts shorter but wider”. Although outlines of stomachs are available for diverse strepsirrhine species, the present author was only able to find one figure showing the distribution of gastric epithelial lining in Eulemur macaco, the macaco or black lemur and Otolemur crassicaudatus, the brown greater galago or thick-tailed bushbaby (Suzuki et al., 1991): At the cardia, a very narrow strip of cardiac gland mucosa is depicted, but the area of fornix gastricus and corpus gastricum is lined by proper gastric mucosa. The pyloric antrum and pylorus itself are lined with pyloric mucosa. 13.3.3 Functional remarks concerning the strepsirrhine stomach Investigations on digesta passage through the gastrointestinal tract of strepsirrhines have been conducted by Campbell et al. (2002, 2004a, b). It can be speculated that the wide range of food regimes that can be found in Strepsirrhini could be related with morphological



differences between gastric shapes. These can be stretched, showing a relatively wide distance of pylorus from cardia. Alternatively, they can represent a globular organ with close proximity of the influx and efflux openings. The time of food acquisition is not related with gastric morphology and feeding times cannot be explained by variations of food chemistry (Faulkner and Lehman, 2006). According to these authors, Avahi laniger is feeding during the night in 5.39% of the time available and is inactive in 82.25%. Feeding time, food quality and gastric shape do not clearly covariate with each other, but different lemur species eat parts of different plant species and show different reactions to chemical plant components and different food passage times can be observed (Ganzhorn, 1985). Primates, including strepsirrhines, exhibit a preference for foods with a low concentration of condensed tannins and a high protein-to-fibre ratio, as Garber (1987) writes. Even folivorous lemur species, which Ganzhorn (1992) investigated, select leaves with high concentrations of easily extractable protein or low concentrations of fibre, or both. There is considerable interspecific variation in the digestibility of structural cell wall carbohydrates. For example, Sheine (1979) presents comparative data: The ring-tailed lemur, Lemur catta, and L. fulvus, the brown lemur, consume foods which are high in cellulose, such as leaves, whereas the black and white ruffed lemur, Varecia variegata, and the silvery greater galago, Otolemur crassicaudatus, consume fruits, which are low in cellulose.

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The leaf and bamboo diets of Sifakas, Propithecus sp., and the grey bamboo lemur, Hapalemur griseus, generally possess more insoluble fibre relative to other plant parts and have higher levels of insoluble fibre and require longer residence time for microbial processing compared to the diets of Varecia variegata (black and white ruffed lemur) and Eulemur fulvus (brown lemur), which have lower recorded leaf intakes (Campbell et al., 2004a). According to Kolar (1988), the difference in food composition between Hapalemur and Propithecus, on the one side, and Varecia and Eulemur, on the other, is not so clear, as it was stated by Campbell et al. (2004a). These latter authors published a table informing about the time when 50% of the contents had left the stomach in the above-mentioned four lemuriform species. These data have been compiled in Fig. 4.17 together with information on food characteristics and body size according to Kolar (1988). Propithecus verreauxi stores larger ingesta for long periods of time in the stomach, perhaps allowing for greater particle size reduction before transport into the small intestine (Campbell et al., 2004a).

13.4 General remarks on small and large intestines of Primates The list of data on length, internal surface and volume, one the one side, and small intestine, caecum and colon, on the other (Tabs. 1.5 and 1.6), as well as food classification (Tab. 1.4) can be compiled for all available

Fig. 4.17: Gastric emptying time of 50% contents in four strepsirrhine species. Barium-impregnated Polyethylene spheres were used as markers. White bars: small spheres (1.5 mm); hatched bars: large spheres (5.0 mm). Raw data are from Campbell et al., (2004a) and Kolar (1988).

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eutherians in diagrams (Tab. 1.1), which presents an overview, but has to be differentiated according to different families. Triangular diagrams, based on information on gastric, caecal and colonic differentiation, from Tab. 1.6, for these different taxa can be found for primates in

Fig. 4.18 (Cheirogaleidae and Lemuridae), Fig. 4.19 (Galagidae, Daubentoniidae, Lepilemuridae), Fig. 4.20 (Indriidae, Lorisidae), Fig. 4.21 (Aotidae, Hylobatidae), Fig. 4.22 (Atelidae, Cercopithecidae), Fig. 4.23 (Cebidae) and Fig. 4.24 (Hominidae, Tarsiidae, Pithecidae).

Fig. 4.18: Dimensions (surface or volume) of stomach, caecum and colon: Cheirogaleidae and Lemuridae.

Fig. 4.19: Dimensions (surface or volume) of stomach, caecum and colon: Galagidae, Daubentoniidae, Lepilemuridae.

Fig. 4.20: Dimensions (surface or volume) of stomach, caecum and colon: Indriidae and Lorisidae.



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Fig. 4.21: Dimensions (surface or volume) of stomach, caecum and colon: Aortidae and Hylobatidae.

Fig. 4.22: Dimensions (surface or volume) of stomach, caecum and colon: Atelidae and Cercopithecidae.

Fig. 4.23: Dimensions (surface or volume) of stomach, caecum and colon: Cebidae.

Whilst insectivorous and carnivorous eutherians show no modification of the colon, this organ comes into play as a differentiated structure in many groups. In Primates, the influence of all three considered sections on the gastrointestinal tract will be taken into account under

consideration of the type of food the animals eat: The Lemuridae (lemurs) (Fig. 4.18), which are florivorous, show differentiations of the colon (raw data in Tab. 1.6), whilst in the faunivorous Cheirogaleidae (mouse lemurs), only the stomach and caecum play a role. Bushbabies

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Fig. 4.24: Dimensions (surface or volume) of stomach, caecum and colon: Hominidae, Tarsidae, Pitheciidae.

(Galagidae) and weasel lemurs (Lepilemuridae) (Fig. 4.19), both of which eat food with considerable meat content, have a well-developed colon, whereas the aye-aye (Daubentonia madagascariensis, Daubentoniidae), which eats intermediate food, has a differentiated caecum, but no differentiation in the colon. A comparison of indris and loris (Fig. 4.20) shows differentiations of the gastrointestinal tract that are characteristic for one of each group. In the Indriidae, the colon does not show differentiations of its wall, but in the Lorisidae, it is haustrated. The following primate families, such as the Aotidae (owl monkeys) and Hylobatidae (gibbons) (Fig. 4.21), as well as the spider monkeys (Atelidae) and the old world monkeys (Cercopithecidae) (Fig. 4.22) eat a food of intermediate quality or a florivorous type of food and all have a gastrointestinal tract with welldifferentiated caecum and colon. In the Cebidae (capuchin monkeys) (Fig. 4.23), there are a few species of the genus Cebus eating an intermediate type of food with a non-haustrated colon, but in most representatives of this primate family, the colon has taeniae and is haustrated. In the great apes (Hominidae) and in sakis (Pitheciidae), both sections of the large intestine are differentiated in species that eat a very wide range of food (Fig. 4.24).

tube without any special differentiation. The description by Owen (1866) of the duodenum in the aye-aye (Daubentonia madagascariensis) does not present details, but makes the general remark that the duodenum, after its usual curve, crosses the spine below the root of the mesentery, then turns up the left side. According to Razanahoera-Rakotomalala (1981), the two genera Avahi

13.4.1 Anatomy of the small intestine of Strepsirrhini Overviews of the small and large intestines of different species of the Strepsirrhini can be found in Figs. 4.25 and 4.26. A differentiation between the three sections of the small intestine is not possible, but it can be seen in Fig. 4.26 b and e that the small intestine is surprisingly short. However, Fig. 4.25, shows a strongly winding

Fig. 4.25: Small and large intestines in four species of Strepsirrhini (Primates). Arrowheads indicate base and apex of caeca; the stars mark the tip of the colonic loops. Adapted from Mitchell (1905).



and Lepilemur, of which the external shape is shown in Fig. 4.26 a and b, have villi intestinales in the duodenum. They have a height of 2 mm in the duodenum of Avahi and 1 to 1.5 mm in Lepilemur. Enterocytes, adapted for absorption by microvilli, and goblet cells, producing mucus, as well as argentaffin cells, can be found, but in both genera, Paneth cells are absent. Lieberkühn’s glands are present, lymphatic cells are dispersed and a two-layered lamina muscularis mucosae is differentiated. The glandulae duodenales in the tela submucosa are relatively thin (“peu épaisses”) and

Fig. 4.26: Gastrointestinal tract in five species of Strepsirrhini (Primates). Arrowheads indicate base and the apex of caeca; the stars mark the tips of the colonic loops. Adapted from Chivers and Hladik (1980, 1984) and Razanahoera-Rakotomalala (1981).

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stretch over a distance along the duodenum (“s’étendent assez loin dans la région duodénale”, RazanahoeraRakotomalala, 1981) in Avahi, but form a compact “collar”, with a width of 1 cm in Lepilemur. 13.4.2 Anatomy of the colon of Strepsirrhini Illustrations of different qualities and descriptions of the large intestinal differentiations in strepsirrhine primates have been published for different families. A graphic overview has already been given above (Fig. 4.3). According to Mitchell (1905), the caecum is present in Mirza cocquereli, the giant mouse lemur (Cheirogalidae), but is very short (Fig. 4.25 a). In addition to this, the large intestine shows two distinct regions, namely, a short colonic loop and a straight portion that proceeds towards the rectum. There is only one apex of the loop, which is marked by an asterisk in the above-mentioned illustration. The caecum in a representative of the primate family Lemuridae, Eulemur mongoz, the mongoose lemur, is very prominent, which is also true of the ansa coli in this species (Mitchell, 1905) (Fig. 4.25 b) (ansa [lat.] = handle, loop). The colon descendens, which cannot be separated from the rectal portion is nearly straight and longer than in Mirza cocquereli. In her extensive study on the digestive strategies of nonhuman primates, Caton (1997) illustrates the digestive tract of a species of the genus Varecia, but in this connection creates some confusion: According to Groves (2005), there are two species belonging to that genus, Varecia rubra and Varecia variegata. In her illustration 7.10, Caton (1997) depicts Varecia varecia rubra, and in her illustrations 7.11 through 7.13, she speaks of Varecia variegata rubra. Despite this terminological confusion, the authors demonstrates that the colon proximalis is very short and that in the intermediate section there is a prominent ansa coli. The distal colon is straight and relatively short. Chivers and Hladik (1980) combine anatomical considerations with information on the food. In Lepilemur leucopus (White-footed sportive lemur), which feeds on leaves or gums, caecotrophy represents the reingestion of a special type of faeces, which are produced in the caecum. This process allows efficient use of a diet with high-fibre content and helps to explain why the small intestine in L.  leucopus is one of the shortest amongst mammals. On the other hand, Fig. 4.26 b shows a complex large intestine, not only with a long and sacculated (taeniated?) caecum, but with intensively sacculated proximal and intermediate parts of the colon as well. Two flexures (stars) can be found in the colon of L.  leucopus. In her

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Fig. 4.27: Ventral views of the large intestine in Lemur catta in naturalistic and semischematic illustrations after Starck (1958).

doctoral thesis, Razanahoera-Rokotomalala (1981) presents an illustration (Fig. 4.26 a) of the gastrointestinal tract of the eastern woolly lemur, Avahi laniger, which is a member of the lemuriform family Indriidae. The colon ascendens is dilated and has taeniae. It proceeds into a strongly looped intermediate colonic section where two ansae can be identified (stars); the colon descendens is relatively short. A more complex situation was demonstrated in another species of the Lemuridae, the ring-tailed lemur (Lemur catta), which was depicted semi-schematically by Starck (1958) (Fig. 4.27). The caecum and colon lie completely dorsally, pushed there by the small intestinal loops, as can be seen in the left panel of the illustration. The course of the ansa coli is very complicated, especially in the middle section. According to Starck (1958), the ansa coli is homologous to the colon transversum. It lies to the right of the abdominal cavity. The colon ascendens is fixed to the dorsal abdominal wall and the colon descendens is dorsally situated and proceeds as rectum; a colon sigmoideum does not exist. The aye-aye (Daubentonia madagascariensis) has an unspectacular large intestine, as was depicted by Owen (1866) (Fig. 4.28 a). The most proximal part of the colon ascendens is dilated, but taeniae cannot be seen; the remainder of the colon ascendens is straight and proceeds to the hairpin-like loop that represents the colon transversum (asterisk). Differentiations in the colon descendens cannot be seen in the illustration from Owen (1866). A species belonging to the family Lorisidae, Arctocebus calabarensis, the golden potto, which eats food of animal origin, possesses a simple colon (Fig. 4.26 c and Fig. 4.28 b). The ansa coli is a simple U-shaped loop,

which has, as Hill (1958) writes, “only minor kinks” (page 173), i.e. smaller curved loops or bends. According to Chivers and Hladik (1984), this species has one of the most unspecialised large intestines in terms of morphology. The caecum is short and conical caecum (stars in Fig. 4.26 c and Fig. 4.28 b) and the colon has a simple, smooth wall. In two publications, illustrations of the intestinal tract of another species of the Lorisidae were presented. For Perodicticus potto (potto), a mainly frugivorous species that feeds partly on animal matter (Chivers and Hladik, 1980), Mitchell (1905) demonstrated that the caecum is long and capacious (Fig. 4.25 c). The colon is long and has two prominent colonic loops (two asterisks in the illustration) in its intermediate section (colon transversum). A relatively short colon descendens proceeds towards the rectal section and forms the end of the hindgut. In contrast, a drawing published by Chivers and Hladik (1984), shows only one ansa coli loop in the transverse colon (Fig. 4.26 d) and a dilated proximal colon. According to Chivers and Hladik (1980), this section can have one or two taeniae coli. These differentiations are not shown in the illustration presented by Mitchell (1905) (Fig. 4.25 c). The ambiguous results of Mitchell (1905) and Chivers and Hladik (1980) indicate that there seems to be a tendency in the Lorisidae, at least in the potto, to differentiate either the colon ascendens by increasing the diameter and by forming sacculations or the colon transversum by intensive formation of one or more colonic loops. Euoticus elegantulus, the southern needle-clawed bushbaby, is a species within the family Galagidae. According to Müller (1988), plant saps make up to 80% of the food. Gums require fermentation for digestion



(Chivers and Hladik, 1980), and for this process, an elongated and coiled caecum is found as well as a very specialised colon (Hill, 1958), which is haustrated and bears three well-defined taeniae (Fig. 4.26 e). Between the taeniae lie “bubble-like” dilatations, which are called “haustrations”. According to Hill (1958), the proximal colon shows considerable elongation and forms a loop with an apex (asterisk in the illustration). In Galago senegalensis (Senegal bushbaby), the ansa is very complex and bent upon itself at least twice (Hill, 1958) (Fig. 4.28 c). This illustration also demonstrates that the caecum of G.  senegalensis is extremely long and sacculated, but that the colon ascendens of this species is smooth and not dilated. In a third species of the Galagidae, the northern greater galago (Otolemur garnettii), Mitchell (1905) was able to show that the caecum is long and capacious as well as the colon (Fig. 4.25 d). This species has

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well-marked compound colic loops and a long straight rectal portion.

13.4.3 Concluding remarks to the colon of Strepsirrhini The morphological differentiations of the colon might reflect the taxonomic relationships among the three infraorders and seven families. However, any relationship between form and taxonomy could not be verified for the colon of the Strepsirrhini! In the infraorder Lemuriformes, Mirza coquereli, of the family Cheirogaleidae is characterised by a relatively simple colon with a short proximal section. In the family Lemuridae, an ansa coli can be seen in the transverse or intermediate colon of Eulemur mongoz (Fig. 4.25 b). Formation of a knot-like differentiation of the colon

Fig. 4.28: Large intestines in three species of Strepsirrhini (Primates). Arrowheads indicate base and apex of caeca; the asterisks mark the tips of the colonic loops. Adapted from Owen (1866) and Hill (1958).

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transversum can be seen in Lemur catta (Fig. 4.27). In the third family of the infraorder Lemuriformes, the Lepilemuridae, the sacculation of the proximal colon in Lepilemur leucopus allows efficient use of as diet very high in fibre content and with the use of reingested caecal contents during the process of caecotrophy (Chivers and Hladik, 1980). In the infraorder Chiromyiformes, the material of one family, Daubentoniidae, was available. The only remarkable differentiation of the colon is a sacculation at the very beginning of the colon ascendens in Daubentonia madagascariensis. The transverse colon is represented by a sharp bend and in the colon descendens is a smooth tube. Arctocebus calabarensis is a species in the infraorder Lorisiformes, family Lorisidae. The colon transversum of Arctocebus c. forms a single ansa coli with one tip or apex (asterisk in Fig. 4.26 c and Fig. 4.28 b), but there is a lengthening tendency of that section with the formation of two ansae coli in Perodicticus potto (Fig. 4.26 d). In the second family of the Lorisiformes, the Galagidae, the colon ascendens and transversum in Euoticus elegantulus has taeniae and is haustrated (Fig. 4.26 e). In Galago senegalensis, two loops are differentiated in the colon transversum, and in the third available species of the Galagidae, Otolemur garnettii, both colon ascendens and colon transversum are intensively coiled and looped (Fig. 4.25 d).

13.5 Anatomy of the caecum of Strepsirrhini Remarks on the caecum can already be found in the chapter on colon anatomy, but further information is given in this section. In the Cheirogaleidae (Cheirogaleus sp.), the caecum is short, as it can be in the Lemuridae, where Hapalemur sp. has a bag-shaped caecum with the ileal and colic openings closely approximated. However, in another representative of the Lemuridae, the caecum is long and capacious, as in Lemur sp. According to Starck (1958), the caecum in Lemur catta, together with the colon, lies totally dorsally and the loops of the small intestine lie ventral of the caecum, which has a form that is depicted in Fig. 4.27. A long and capacious caecum can also be found Lepilemur sp. (Hill and Rewell, 1948), which has an organ that is enormously elongated and terminates in a conical tip (Fig. 4.26 b and Fig. 4.11). An additional type of differentiation can be seen in the Indriidae, where Avahi sp. (Fig. 4.26 a) and Indri sp. are characterised by a much

convoluted caecum. Hill and Rewell (1948) write that the caecum in Daubentonia madagascariensis is short, rounded and bag-shaped without apical narrowing. This is in accordance with the illustration published by Owen (1866) (Fig. 4.13 A), but not with their own one (Fig. 4.11). In Galago sp. (Galagidae), the caecum is long and capacious with its basal sac-like part being more dilated than the adjacent proximal colon. Also, in Loris sp. (Lorisidae), the basal portion of the caecum is sac-like and thin-walled, but the terminal portion has a thick-walled narrow lumen. In some genera, the caecum is convoluted or spirally coiled. In the Lemuridae (Lemur sp.) and Lepilemuridae (Lepilemur sp.), the caecum is elongated and spirally twisted or is coiled. In Euoticus sp. (Galagidae), the distal part of the caecum forms a hook-like apex (Fig. 4.11, bottom right). Hill and Rewell (1948) mention for two genera of the Indriidae, Avahi sp. and Indri sp., a caecum which is intensively convoluted or coiled and ends abruptly by narrowing into a thin pointed apex. However, in another genus and species of the Indriidae, Propithecus verrauxi, the long caecum is not spirally coiled. This shows that the caecal form is highly variable within primate families. According to Hill and Rewell (1948), the terminal segment of the caecum is separated from the remaining caecum in the Daubentoniidae. Also in Galago sp. (Galagidae), the basal sac is divided by a transverse sulcus (Fig. 4.11, bottom line, right). In Arctocebus sp. (Lorisidae), constrictions can be found at the caecocolic and ileocolic junctions. Very prominent “constrictions” are the semilunar folds, which are formed on the caecum when longitudinal muscular bands, the taeniae, are formed. Between these taeniae, the wall of the caecum bulges out, forming the haustra, which are often – and erroneously – called “sacculations”. The latter are structure characteristic for non-taeniaeted sections of the digestive tract. In two genera of the Cheirogaleidae, Cheirogaleus sp. and Microcebus sp., taeniae are present in the caecum. For the latter genus, neither taeniae nor haustrations are depicted in the drawing published by Hill and Rewell (1948) (Fig. 4.11, top left). The authors found, at least, two definitive taeniae in the caecum of Avahi (Indriidae). Haustrations, separated by transverse sulci, can be found along the whole length of the caecum. In two genera of the Lorisidae, Nycticebus sp. and Perodicticus sp., permanent haustrations can be seen along the whole length of the caecum because taeniae are present. In representatives of the haplorrhine Hominoidea (Hylobatidae plus Hominidae), an appendix vermiformis is differentiated



that extends from the caecal apex. Hill and Rewell (1948) indicate in their text that an appendix might be present in Nycticebus sp. (Lorisidae), but their illustration, depicted here in Fig. 4.11 (bottom left), only shows a narrow conical tip of the caecum.

14 Haplorrhini (“dry-nosed” primates) 14.1 Introductory remarks The Haplorrhini or dry-nosed primates have 46 genera and 288 species (Groves, 2005). They include two infraorders, a small one, the Tarsiiformes (tarsiers with 1 genus and 7 species) and the more differentiated Simiiformes (monkeys and apes with 45 genera and 281 species, Groves, 2005). The Simiiformes are further subdivided into two parvorders, the Platyrrhini (flat-nosed or New World monkeys with 4 families, 16 genera and 128 species) and a second parvorder is represented by the Catarrhini (Old World monkeys with 3 families, 29 genera and 153 species). In a study on Platyrrhini, Rosenberger (2011) states that abundant gaps in biological information, combined with anatomical studies, often make an overview difficult. In addition to the families Hylobatidae (gibbons) and Hominidae (apes and man), the Catarrhini comprise the family Cercopithecidae, which itself has two subfamilies, the Cercopithecinae (11 genera and 73 species) and the Colobinae with 10 genera and 59 species (Groves, 2005). With the exception of the Colobinae the Haplorrhini have a simple unilocular (one-chambered) stomach and will be dealt with in the following in a more compilatory fashion, whilst the Colobinae are characterised by a plurilocular, but nevertheless simple stomach, which means that it is lined exclusively with glandular mucosa. The multichambered stomach types of the Colobinae will find special attention in the following text. According to Gingerich (2012), this eutherian taxon made its first appearance in the fossil record during the global warming event that marks the beginning of the Eocene, but the specific origin of primates, including the Haplorrhini, amongst more primitive eutherians had not been established when the textbook of Carroll (1988) was written. However, a recent publication (Ni et al., 2013) presents data on the most basal member of the tarsiiform clade, Archicebus achilles, which was probably

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a diurnal, arboreal and primarily insectivorous primate and lived in the lower Eocene of present-day Hubei Province, China. During the early stages of their evolution, 50 MYBP, primates were small insect-eating animals (Andrews and Martin, 1991); later during the Eocene, 45 MYBP, they became primarily frugivorous, and by the late Eocene (35–40 MYBP), even herbivorous. A seed-to-leaves evolutionary pathway may be a widespread phenomenon in primates (Rosenberger et al., 2011). Fossil platyrrhines from the middle Miocene from different parts of South America and the Caribbean are frugivores or folivores/ frugivores (Cooke, 2011), but Alouatta and Brachyteles represent the most folivorous Platyrrhini (Rosenberger et al., 2011). Recent primate species are mainly inhabitants of forests, e.g. 44 species in Africa and 42 in South America. In addition, five African species inhabit savannahs, but none in South America live in savanna-like biomes (Bourlière, 1973). Although the Cerrado of Brazil is considered an open habitat formation (da Fonseca et al., 1999), only the gallery forests along rivers in the Campos Cerrados hold a diverse primate fauna (Robinson and Ramirez, 1982). In a savannah-type habitat, both plant and animal food are patchily distributed (Milton, 1987). Not only the uneven distribution of food might cause problems, but the content of difficult-to-digest substances in the eaten plant material can have a detrimental effect: Together with hemicellulose and cellulose lignin represents insoluble fibres. Hemicellulose is virtually unfermentable compared with cellulose and lignin (Conklin-Brittain et al., 2006). To access digestible plant cell contents, these materials first have to be mechanically ground and “milled”. This process, as well as mineral contents in the food, causes “microwear” on teeth, as Kelley (1990) determined. This can be used to infer fine dietary distinctions, even in fossil mammal species. Because of their high anatomical differentiation, the Colobinae will be discussed in a separate section.

14.2 General remarks on food Morphology of the mammalian stomach determines efficiency of digestion (Parra, 1978; Stevens, 1988). According to Bodmer (1991), who studied Amazonian ungulates, the surface area of the stomach is a good predictor of dietary types and, related with this, resource partitioning between species. This statement can also be generalised for primates. It is also true that folivorous primates occupy smaller

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home range areas in relation to their body weight than do frugivores and omnivores (Milton and May, 1976). This reflects the fact that foliage is more uniformly distributed and more common than, for example, fruits (Fleagle, 1988). When mammals, including Haplorrhini, select food, they prefer ingestion of protein and lipid, but fibre, phenolics and alkaloids are avoided (Whiten et al., 1991). In addition, Oftedal (1991) states that ingested energy will depend both on the composition of the food and the extent to which various constituents, including fibre, are digested. Fibre in the food is not only high in mature leaves, but can even be high in flowers, fruits and soft parenchymatous material in stems of vascular plants (piths), which can be important resources for African apes when fruits are scarce (Wrangham et al., 1991). It should also be mentioned that insects also contain significant but variable amounts (8–27% of dry matter) of chitin, which is a relatively indigestible structural carbohydrate (Oftedal, 1991). Hohmann (2009) presents a list on food constituents in primates, which was originally published by Rowe (1996). From these data, a triangular diagram was drawn for 97 species (Fig. 4.29), which is principally similar to a diagram published by Chivers (1994) on 80 primates. Using information on the food index, as listed in Tab. 1.4, a boxplot diagram for Strepsirrhini and Haplorrhini was compiled by the present author in Fig. 1.7. More details will be discussed below.

14.2.1 Food of the Tarsiiformes, Tarsiidae The nutritional niche of faunivores is represented by Tarsiidae (Fig. 4.29). Tarsiers inhabit different Indonesian islands where they search for animal prey (Cartmill, 1994), such as insects, arachnids and small vertebrates (Fleagle, 1988).

14.2.2 Food of the Simiiformes, Platyrrhini The Platyrrhini or New World monkeys mix florivory with insectivory (Fig. 4.29). According to Oppenheimer (1982), the capuchin monkey (Cebus capucinus) eats fruits and insects and Perry and Ordoñez-Jiménez (2006) describe seasonally varying food for the same species; in March, April and May more than 50% of their ingested material consists of plant matter, in June, July and August, more than 50% is represented by insects. In contrast to the Cebinae, the Alouattinae or howler monkeys are florivores. For example, the red howler monkeys (Alouatta seniculus), studied by Braza et al. (1983), are strictly vegetarian, feeding on approximately equal amounts of leaves and fruit, the third choice being flowers and legume pods. According to Milton (1979, 1981), Milton et al. (1980) and Milton and McBee (1983), the mantled howler monkeys (Alouatta palliata) are highly folivorous, eating young and mature leaves, but sometimes also fruits. In this species,

Fig. 4.29: Food composition (see Table 1.2.4) of 97 primate species. Raw data from Rowe (1996), fide Hohmann (2009).



gas chromatography produced evidence of fermentation producing volatile fatty acids in the caecum and absorbing them from that organ (Milton and McBee, 1983). The closely related spider monkey, Ateles geoffoyi, is primarily frugivorous (Milton, 1981). According to the same author, howlers have capaceous hindguts and slow food passage rates. On the other hand, spiders have smaller hindguts and are able to process great quantities of food per unit time; in both cases, gastric digestion is not of great importance. Milton et al. (1980) argue that a diet composed primarily of leaves may pose a considerable problem in terms of providing sufficient energy to meet daily requirements. The structural carbohydrates (cellulose and hemicelluloses) in leaves may provide a potentially rich energy source for howlers, providing cellulolytic microorganisms are present in the caecum and colon in sufficient quantities for efficient fermentation activities. Data presented by Milton et al. (1980) support the view that howlers have high concentrations of cellulolytic microorganisms that are able to degrade plant structural carbohydrates efficiently.

14.2.3 Food of the Simiiformes, Catarrhini: Cercopithecidae In the Old World monkeys, the food eaten by different species is also variable (Fig. 4.29). Ménard (1985) and Ménard and Vallet (1986) investigated the feeding ecology of Barbary macaques (Macaca sylvanus) in Algeria. These animals prefer grains, but leaves follow second. There is considerable seasonal change and in winter leaves of Dactylus glomerata (orchard grass) can represent about half of the food. According to Ménard and Vallet (1988), mature cedar leaves can become an important food item during winter. There are also representatives of the Cercopithecinae that are frugivorous and others that are not exclusively florivorous, but which also eat invertebrate prey. For example, Lawes et al. (1990) call the samango or blue monkey (Cercopithecus mitis) of Angola a frugivorous species. During periods of food abundance, the monkeys concentrate their attention on items of greater energy value. They also eat young leaves, shoots, flowers and occasionally insects and mushrooms; in some regions, they are fond of termites, grasshoppers, ants and grubs, as Kingdon (1971) describes. According to Harrison (1984), the green monkey, Chlorocebus sabaeus, is omnivorous and eats diverse food. In this species, fruit represents 50%, flowers and seeds each 13%, leaves 7%, gum 3%, fungi 1% and invertebrates 13%. The food of the cercopithecid

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subfamily Colobinae will be mentioned, together with information on the digestive tract anatomy, in a separate section below.

14.2.4 Food of the Simiiformes, Catarrhini: Hylobatidae and Hominidae Gibbons (Hylobatidae) have to be called omnivorous, although they specialise on a diet of ripe fruit, such as figs. Their staple food changes seasonally when they eat young leaves, as well as invertebrates, such as termites and arachnids (Fleagle, 1988). This considerable variability in Hylobatidae is also documented in Fig. 4.29 (white diamonds). Tutin and Fernandez (1985) compared food of Gorilla gorilla (gorilla) and Pan troglodytes (chimpanzee) in Gabon, western Central Africa. Both of them are omnivorous and eat fruit regularly in addition to leaves, stems, pith and bark; they cannot be called folivores. Anthropologically, it is of interest to obtain information on the diet of human ancestors. According to Teaford and Ungar (2000), the early hominids could have eaten both abrasive and nonabrasive foods, so that they were well suited for life in a variety of habitats. Through time, the australopithecines acquired the ability to feed on hard objects. The authors believe that the australopithecines were not preadapted for eating meat, but this conclusion runs counter to recent isotope work suggesting that the australopithecines did in fact consume significant amounts of meat (Sponheimer and Lee-Thorpe, 1999).

14.3 Anatomy of the stomach of Haplorrhini 14.3.1 Tarsiiformes and Simiiformes: Platyrrhini As has already been mentioned in the introductory remarks, the cercopithecid subfamily Colobinae will be discussed in a separate section. For the infraorder Tarsiiformes (family Tarsiidae), only little information is available for the stomach; no good illustration was found. Hill (1958) writes that the stomach of Tarsius is a simple, globular sac with the cardia and the pylorus lying very close to each other. In the infraorder Simiiformes with the Platyrrhini and Catarrhini, the situation has to be called unbalanced. Although some information on the type of food of platyrrhine primates is available (see above), anatomical information on the stomach is very limited. From Hill (1958) and Stevens and Hume (1995), a compilatory illustration of stomach outlines in Cebidae

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(marmosets and tamarins), Atelidae (spider monkeys) and Aotidae (night monkeys) was produced (Fig. 4.30). The stomach of Aotus trivirgatus (three-striped night monkey), was depicted by Hill (1958) and the mucosal lining of Lagotrix lagotricha (brown wooly monkey) is given schematically; in all other cases the illustrations present the external aspect. In platyrrhines, the trend is towards a globular fornix, a conical corpus and a cylindrical pyloric segment (Hill, 1958). The same author also gives the outline of the stomach of Callithrix sp. with a lengthened and cylindrical fornix. Information on the mucosal lining of the stomach is made available for Lagotrix lagotricha by Stevens and Hume (1995). The unilocular organ is simple, i.e. it is only lined with glandular, not with squamous stratified mucosa.

14.3.2 Simiiformes: Catarrhini 14.3.2.1 Cercopithecoidea: Cercopithecinae It can generally be stated that the stomach, in primates as in other mammals, represents a storing volume for digesta

Fig. 4.30: Outlines of stomachs of three platyrrhine species. Adapted from Stevens and Hume (1995).

and therefore has to be able to adapt to different degrees of filling. “The slow and gradual increase of basal pressure during gastric filling as well as the almost immediate adaptation to volume changes indicate a mechanism of gastric relaxation to maintain low intraluminal pressure in the filled stomach” (Stadaas, 1975, page 140). In studies on the human stomach, Schwizer et al. (2002) were able to show that ingestion of a meal produces at least two responses, namely “receptive relaxation”, which allows the stomach to accept a volume load without a significant rise in gastric pressure, and “adaptive relaxation”, which modulates gastric muscular tone in response to the specific properties of the meal ingested” (page 59). Distrutti et al. (1999) showed that gastric wall tension, but not intragastric volume determines perception of gastric normal distension. A compilatory illustration was created from three sources (Fig. 4.31). In some cases, the gastric shape reminds of a human stomach (Macaca mulatta, rhesus monkey, as shown by Hill, 1958; Stevens and Hume, 1995), or Cercopithecus cephus (moustached guenon) by Chivers and Hladik (1980), but Cercopithecus can also show a globular gastric shape (Huntington, 1903), as can also be found in Chlorocebus pygerythrus (vervet monkey, Stevens and Hume, 1995). The gastric shape of Papio anubis (olive baboon) has a voluminous, almost globular fornix, but a cylindrical corpus and pars pylorica (Stevens and Hume, 1995). It is assumed that the exclusively glandular lining of the stomach, as it was described by Vidal et al. (2008) for Macaca fascicularis (crab-eating macaque or Cynomolgus monkey), is representative for all Cercopithecinae. The fornix showed deep gastric pits (foveolae), but was free of parietal cells, which were present in the corpus region. Mucosal folds can be found both in the fornix and corpus. Also, in the pars pylorica, glandular pits can be found in the mucosa.

14.3.2.2 Hominoidea, Hylobatidae and Hominidae. Discussion of the mesogastria Because of clinical importance in human medicine, many of the investigations on primate gastric form and function have been undertaken in man. Most of the information based on published literature refers to the human stomach. This organ is often shaped like the letter “J” and has a horizontal or slightly ascending pyloric part (Moore, 1992). However, the shape and positions of the stomach are “greatly modified by changes within itself and in the surrounding viscera” (Gray and Goss, 1973, page 1219). To investigate the development of the gastric shape, Macarulla-Sanz et al. (1996) referred to embryological



Fig. 4.31: Outlines of stomachs of four cercopithecine species. Adapted from different authors.

investigations in the human stomach. These authors separated the ontogenetic right (paries posterior in the adult) from the left gastric wall by drawing a plane between the lines of dorsal and ventral lines of attachment of the two mesogastria, the mesenterial plane (Fig. 4.32). The left wall of the stomach predominates in growth over that of the right. As a consequence of the overall increase in gastric wall growth to the left, Nebot-Cegarra et al. (1999) believe that the stomach of the human embryo undergoes “heterogeneous and multifactorial rotation”. Kanagasuntheram (1957) states that the position of the gastric nerves and the attachment of the mesogastria to the curvatures of the stomach cannot be regarded as reliable criteria in favour of a rotation of the stomach. Most of the changes can be explained by simple growth processes. The left side of the stomach anlage increases in size, whereas the right side remains unchanged (Dankmeijer and Miethe, 1958). The left side forms the “grosse tubérosité”, which represents, most probably, the fornix without any indication of a rotation. This is corroborated by Dankmeijer and Miethe (1961),

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who found mitotic activity on the left side of the anlage, continuing longer than on the right side. LiebermannMeffert (1969a) emphasises that the definitive or final position of the human stomach, produced by pure growth processes, ends with the completion of the fundus and takes place at the same time as the differentiation of the stomach muscle layers. The stomach undergoes no real mechanical rotation, but outpocketings of the peritoneal cavity, so-called recessus, enable rapid undisturbed growth (Liebermann-Meffert, 1970). In the unilocular stomach, as it can be found in Homo sapiens, the dorsal mesogastrium is not attached to the whole greater curvature. This means that during ontogenetic development the line of fixation “moves” over the gastric surface from the region of the curvatura major to the paries posterior (back wall). In his insightful thesis on some aspects of the embryological development of the human stomach, Miethe (1960) asks what the significance of the line of attachment of the mesogastrium dorsale to the embryonic stomach might be. Does it mark the division of the paries anterior (front wall) from the paries posterior (back wall)? It appeared that the line of attachment of the mesogastrium dorsale to the embryonic stomach changes position (Miethe, 1960, page 78). The attachment of the mesogastrium dorsale does not mark the division of front wall from the back wall, but is only dependent on the growth of the bursa omentalis. The supply and drainage of the stomach by blood and lymphatic vessels as well as nerve supply, subdivides the anatomically right side of the stomach (paries posterior) into an ontogenetically right and left side (Langer, 1988). This is illustrated in Fig. 4.32. The omenta or mesogastria are peritoneal duplicatures that “lead” blood and lymphatic vessels and nerves towards the intra-abdominal organs, but they also serve other purposes. Detailed accounts, which mainly deal with the dorsal mesogastrium and the greater omentum formed by it, has been given in a publication edited by Liebermann-Meffert and White (1983). For example, absorption of fluid and solutes from the peritoneal cavity is accomplished by the omentum majus (Liebermann et al., 1983). The greater omentum also shows phagocytosis (Liebermann and White, 1983) and is able to reduce haemorrhage from injuries (Düring, 1983). Schwalbe (1912), Aschoff (1918), as well as Bauer (1923), depict a remarkable number of different human gastric shapes, indicating the high variability of the unilocular stomach. Moynihan (1904a, b) presents examples that some gastric shapes, for example, the “hour-glass stomach” may be indicative of a pathological situation, such as ulcers of malignant character. According to Cunningham (1906),

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Fig. 4.32: Craniad view (A) of the semischematic transversal section through the fornical region of the human stomach along the plane indicated in the lower panel (B). The lines of fixation of both mesogastria are marked in both panels. Adapted and corrected after Langer (1973).

hour-glass stomachs are formed because the greater curvature, not the lesser curvature, is folded in (he speaks of “tucking-in”). The present author assumes that this formation of transverse “folds” close to the greater curvature may be related with the orientation of the fibrae obliquae. This type of differentiation on the greater curvature is illustrated by Forssell (1912), Jefferson (1915), Elze (1919) and Farthmann (1973), and will be discussed in the following section. 14.3.2.3 Musculature of the gastric wall, mainly of the human stomach It is characteristic for a unilocular stomach that a third – internalmost – muscular layer is developed in addition to the outer stratum longitudinale and the internal stratum circulare. An oblique layer (fibrae obliquae) of the tunica

muscularis is added from 16th week onwards (Dattatray et al., 2012), but Plenk (1931) found oblique muscles in a 9-week embryo. According to Pernkopf (1924), the development of the fibrae obliquae starts later than in the other two layers of the tunica muscularis. The musculature running circular around the fornix belongs to the innermost layer, the fibrae obliquae (Welch, 1922). Fig. 4.33, shows a human stomach (originally published by Owen, 1868), which had been inverted – inside out – the tunica mucosa has been peeled off. The oblique fibres can be seen in the fornix gastricus and the corpus gastricum, but not in the pars pylorica, nor along the lesser curvature of the corpus, where circular fibres are visible. Coincident with the development of the fornix, Welch (1923) found that the number of muscular layers increased to three by the formation fibrae obliquae at a body length



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Fig. 4.33: Human stomach, muscular coat inverted to show the architecture of the tunica muscularis. Adapted from Owen (1868).

of 24 to 33 mm or a post-conceptual age of 8 to 9 weeks (Hinrichsen and Christ, 1990). The unilocular stomach has a complex architecture of the tunica muscularis; the lamina muscularis mucosae will not be considered in the following discussion. The differentiation of the tunica muscularis into an external stratum longitudinale, an intermediate stratum circulare and an internal oblique layer (fibrae obliquae) (Aufschnaiter, 1894; Forssell, 1913; Pernkopf, 1937; Liebermann, 1966) represent appropriate means to compare and homologise gastric regions not only in unilocular, but also in many multichambered stomachs (Pernkopf, 1937; Farthmann, 1973; Langer, 1988). Because of this, the tunica muscularis will be discussed in the following in some detail. Generally, only two of the three muscular layers contribute to the formation of the tunica muscularis in different sections of the stomach, which is therefore bilayered in most cases (Forssell, 1913). The terminology on gastric anatomy in humans has been applied by different authors, such as Waldeyer (1908), Lewis (1912), Jefferson (1915), Torgersen (1942), Farthmann (1973). The Terminologia Anatomica (TA, 1998), published by the “Federative Committee on Anatomical Terminology”, is ambiguous, especially in the more aboral section – pars pylorica. In addition, the terms used in unilocular stomachs of domestic mammals (cat, dog, pig and horse) were consulted in the Illustrated Veterinary Anatomical Literature published by Schaller (1992). A table, representing a compromise between different – and partly contradictory – terms is compiled in Tab. 4.3 and depicted in Fig. 4.34. The gastric region from the distal end of the oesophagus to the proximal part of the duodenum, the ampulla duodeni, is also listed.

On the side of the greater curvature, the stomach is externally separated from the oesophagus by the incisura cardinalis (TA, 1998), which obtained its name from the cardia. The fornix or fundus gastricus follows, succeeded aborally by the gastric body, corpus gastricum, which ends at the level where the incisura angularis can be formed by contraction of the circular musculature on the side of the lesser curvature. Along this same curvature, extending from the cardia onwards the incisura angularis, runs the gastric groove or sulcus or canalis gastricus, which is marked in Tab. 4.3 by “#”. (Jefferson, 1915; TA, 1998, also called canalis salivalis according to Strecker, 1905, “Magenstrasse” of Bauer, 1923, “Schlundrinne” according to Pernkopf, 1937, or sulcus salivalis of Waldeyer, 1908). Veterinary anatomists (Schaller, 1992) also speak of the sulcus ventriculi. Bauer (1923) found the Magenstrasse in 11 of 12 investigated human specimens. The muscular loop, formed by the oblique fibres, is not only differentiated into muscular ridges on both sides of the gastric groove, but also contributes to the closure of the stomach; a true cardiac sphincter cannot be found. Bauer (1923) also states that it is the surface of the mucosa that makes the gastric groove visible by longitudinal folds. Elze (1919) emphasises that the terms “pars pylorica” and “antrum pyloricum” are used variably; he prefers “canalis egestorius” together with Forssell (1912, 1913) and Keet (1974). This term will not be applied in the present text. The distal or aboral section of the stomach is represented by the pars pylorica, which, in TA (1998), is not considered synonymous with the antrum pyloricum. The pyloric part can be subdivided, which is clearly described and depicted by Torgersen (1942) (Fig. 4.34).

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Tab. 4.3: Terminology applied in the human gastric region.

Lesser curvature

Incisura angularis

      #  #  #        

Oesophagus     Cardia Fornix (fundus) gastricus Corpus gastricum

             

Pars pylorica or antrum pyloricum   Sinus pyloricus Membrana angularis   Canalis pyloricus Pylorus   Ostium pyloricum   Ampulla duodeni  

  Greater curvature Incisura cardialis                    

#: Sulcus (canalis) gastricus, Magenstrasse. Compiled from: Waldeyer (1908), Lewis (1912), Jefferson (1915), Baum (1923), Torgersen (1942), Farthmann (1973), Schaller (1992) and Terminologica Anatomica (1998).

Fig. 4.34: Schematic view of the human stomach. The arrowhead marks a site where the incisura angularis can be formed. Modified from Torgersen (1942).

The greater curvature bulges out as sinus pyloricus (orad) and canalis pyloricus (aborad). Between both, bulging out the lesser curvature, lies the membrana angularis. Aborad of the canalis pyloricus lies the pylorus, a sphincter, which is able to close the ostium pyloricum. Although applying another terminology, Aschoff (1918) mentions a narrowing, which he calls isthmus ventriculi at the border between the corpus and the pars pylorica. The lower section of the corpus and the transit to the pyloric part (he speaks of “vestibulum”) are the site where the isthmus can be formed. Aschoff

(1918) indicates that the isthmus is a transient constriction that is not always formed at the same site of the organ. Generally speaking, it should be stated that the shape of the pars pylorica shows considerable functional change; peristaltic waves run over this section of the stomach (Braus and Elze, 1956). Wernstedt (1907) believes that the canalis pyloricus is the result of a strong contraction in this region; when the contraction stops, the canalis disappears. Under consideration of the muscular architecture of tunica muscularis, Torgersen (1942, 1968) discusses comparative aspects. The “segments” of the human stomach will be mentioned in oral/aboral direction: Torgersen (1942) characterises the fornix as lying above the upper segmental loop (Fig. 4.34). This “blindsac” has separate inner fibres, which encircle the fornix (Pernkopf and Lehner, 1937). Smooth muscular cells that belong to the innermost layer start at the incisura cardialis and run towards the greater curvature (upper dashed line in Fig. 4.34); they represent the “upper segmental loop”. The lesser curvature itself is free of oblique musculature, which forms the two bundles that run parallel to the curvatura minor and contribute to the lips that delimit the sulcus or canalis gastricus (Gillenskoeld, 1862; Strecker, 1905). Muscular half-rings (fibrae circulares), running from oblique muscular lip to the lip on the opposite side, form the bottom of the gastric groove (LiebermannMeffert, 1969b) (Fig. 4.33, Fig. 4.34). The corpus gastricum lies between upper and lower segmental loop of oblique musculature (Torgersen, 1942). To put it the other way round: The fibrae obliquae are characteristic only for the corpus and fornix, but not for the pars pylorica (Pernkopf and Lehner, 1937). The pars pylorica or antrum pyloricum show a complex arrangement. Retzius and Crepelin (1857) depict



the human antrum pyloricum (pars pylorica) and show an external longitudinal muscular bundle, called the ligamentum pylori. This differentiation is neither mentioned in NH (1989) nor in TA (1998). Torgensen (1942) and Farthmann (1973) show (Fig. 4.34) that muscles of the sinus pyloricus converge towards the lesser curvature; this is the region where the incisura angularis can be formed by contraction of circular musculature. The membrana angularis (Forssell, 1913; Farthmann, 1973) has musculature which fans out towards the lesser curvature and converges on the greater curvature. Finally, the canalis pyloricus is characterised by converging muscles on the lesser curvature, forming a muscular torus pyloricus, which is not a prominent structure in the human sphincter pylori. For the purpose of comparative investigations, understanding the principle of the architecture of the tunica muscularis, the lamina muscularis mucosae, which belongs to the tunica mucosa, should not remain completely unmentioned. According to Kaufmann (1971), orientation of the lamina muscularis mucosae forms a “screw” with steep outer and flat inner layers, i.e. externally parallel to the longitudinal axis of the stomach and almost transverse internally. In man, the lamina muscularis mucosae is differentiated in the 10th week (Hinrichsen, 1990). This is later than the formation of the tunica muscularis, which shows both circular and longitudinal muscle layers from the 10th week onwards; the parasympathetic ganglia of the myenteric or Auerbach’s plexus are discernible between the circular and longitudinal muscle layers starting 13 weeks.

14.3.2.4 Remarks on the histology of the tunica mucosa in the unilocular, mainly human, stomach Cells of the gastrointestinal mucosa are among the most rapidly proliferating cells of the body (Johnson, 1988), and their generation length amounts to about 1 day for epithelial cells (Lipkin et al. (1963). There are regional differences in mucosal cell proliferation. Hansen et al. (1976) indicate that the number of DNA-synthesising cells and the mitotic frequencies were higher in antral mucosa compared to mucosa in the fundic part of the human stomach. Although one might speculate differently, the nutritional spectrum is not necessarily related with characteristics of the histological development of the tunica mucosa, as Müller (1971) remarks. In a handbook of comparative anatomy of vertebrates, Pernkopf (1937) depicts the distribution of four types of mucosa in the region of the human stomach: (1) squamous, non-glandular mucosa can be found in the oesophagus, whereas (2) cardiac mucosa in man consists of glandulae gastricae (NH, 1989) and is found as a small ring around the cardiac opening (Fanghänel et al., 2003). (3) proper gastric and (4) pyloric types of

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mucosa follow in the gastric corpus and the pars pylorica. The same situation can also be found in the chimpanzee, Pan troglodytes (Suzuki et al., 1991) and in species of New World monkeys (Platyrrhini). According to Krause et al. (1978), the human cardiac gland region begins about 3 mm above the termination of the oesophagus and extends about 3.4 cm into the proximal stomach. In other mammals, e.g. pigs, it is much more extensive (Welsch, 2003). Suzuki et al. (1991) present the information that cardiac mucosa can be found in the fornix gastricus and the proximal section of the corpus gastricum in Lagothrix lagotricha (brown wooly monkey, Atelidae) and in different species of the Cercopithecidae. The proper gastric glands (glandulae gastricae propriae) form the histological regio gastrica (Mosimann and Kohler, 1990) and line the fornix and corpus in humans, so that Vidal et al. (2008) can justly describe the fornix and corpus as similar histologically. The mucous cell of the cardiac gland of the histological regio cardiaca are morphologically similar to the mucous neck cells of the fundus (Krause et al., 1978). Mayersbach (1954) found the glands generally free of parietal cells, but these cells can be found in very small numbers in the glandular tubes. Berger (1934) investigated the human stomach and concentrated on the HCl-producing parietal cells, which can be found in any region of the organ and which were described in detail for humans by Gusek (1961) and Ito (1981). The present author produced an illustration from Berger’s (1934) material that informs about tendencies in cell numbers along the gastric wall (Fig. 4.35), showing that their number increased from the cardia to the corpus gastricum via the lesser and greater curvature, as well as on both facies of the stomach towards the corpus gastricum. In the antrum pyloricum, the number of parietal cell decreases along the lesser curvature and these cells are almost absent at the level of the pylorus. As an effect of HCl production by parietal cells, the human stomach is practically sterile or only sparsely populated by microbes (Bauchop and Martucci, 1968; Bauchop, 1971). The glandulae pyloricae are glands of the pars pylorica (Mosimann and Kohler, 1990). According to Krause et al. (1977), the human pyloric glands consist of three cell types: mucous cells, parietal cells and endocrine cells. Vidal et al. (2008) discuss the confusing terminology that is related with the mucosal “outfit” of the stomach: The mucosa of fornix and corpus contains abundant parietal and chief cells and has previously been termed the “fundic mucosa”. Similar confusion can arise when describing the cardia. The cardiac gland region is characterised by the presence of mucus-secreting cells and a lack of parietal and chief cells. This mucosa is often termed the cardiac mucosa. However, when this term is used in pigs, to give just a non-primate example, cardiac mucosa can

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Fig. 4.35: Number of parietal cell per 0.02 mm² in the tunica mucosa at different distances from the cardia (marked X) in the human stomach. Raw data from Berger (1934).

be found in the fornix gastricus and portions of the corpus gastricum (Vidal et al., 2008). The gastrointestinal mucosa contains different endocrine cells (Grube, 1982, 1986). In man, it is the largest and perhaps most complex endocrine organ in the body (Johnson, 1988). Released from the antral mucosa during a meal by vagal stimulation, gastrin is the most potent stimulant of gastric acid secretion. Gastrin has a variety of effects on motility, pancreatic secretion, and pepsin secretion. The only effect of gastrin in addition to the stimulation of gastric acid production is its growth-stimulating effect on gastrointestinal mucosa. In addition to gastrin mentioned by Johnson (1988), Welsch (2003) also names the following hormones as products of the human gastric tunica mucosa: somatostatin, serotonin, histamine, pancreatic polypeptide and other peptides. The cardiac and pyloric gland regions, as well as the superficial, generally columnar surface epithelial cells of the proper gastric gland region produce mucin and bicarbonate (Forssell and Olbe, 1987). In addition, mucin is also synthesised in the mucous cells in the neck of the glandular tube (Waldron-Edwards, 1972). Mucinproducing cells are predominant in the gastric mucosa. Gastric mucin is a mixture of molecules of different sizes, made up of a protein backbone attached to characteristic oligosaccharide side chains. Mucus does not only lubricate the mucosa, but also represents the first line of defence against noxious gastric contents. The three-dimensional

mucin adherent to the mucosal surface provides a relatively stable protective layer, freely permeable to small ions such as H+ or Na+. The mucinogenic cells are being constantly formed, and mucin is being constantly secreted, so that the “gastric barrier” probably functions by virtue of the dynamic nature of its protective mechanism (Waldron-Edwards, 1972). The mucus layer has a variable thickness of less than 500 μm. “Both the surface neck cells and the mucus neck cells in the upper part of the glands secrete mucus” (Forssell, 1987, page 10). In addition to the above-mentioned protective function by secretions of surface and mucous neck cells, the population of the gastric tunica mucosa contributes to digestion. For example, Mayersbach (1953) mentions that the cardiac glands secrete gastric lipase. In the proper gastric gland region, the chief or zymogenic cells produce proteases, which are acidophilic. To reach their functional optimum, they need the acid production of parietal or oxyntic cells (Welsch, 2003).

14.3.2.5 Remarks on vascularisation and innervation Because of its great clinical significance, the arterial blood supply and venous drainage of the stomach of haplorrhine primates have been intensively studied in one species of the Hominidae, Homo sapiens (Guth, 1984). A great diversity of publications deal with the vascular supply and drainage of the human stomach. Within the gastric wall,



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a complex system of affluent arterial and effluent venous small vessels, as well as capillaries, can be made visible by corrosion cast investigations. The ontogenetic development of the capillary net has been studied in the tunica mucosa (Gorczyca et al., 1999). Considerable variations, for example, of macroscopic arterial vessels, have been documented: Lippert and Pabst (1985) classified and determined the frequency of “arterial variations in man”, expressed as percentage of the total number of recognised types of modification. This is not the site for detailed discussions of gastric arterial supply in humans, and the reader should refer to textbooks on human macroscopic anatomy. To give the treatment of gastric cancer a sound basis, lymphatic drainage of the human stomach has been intensively studied, e.g. by Sarrazin et al. (1980). It is characteristic that the three main drainage systems show considerable overlap. The cardiac system drains the fornix, the lesser curvature of the corpus and the pars pylorica and depends on long collecting ducts of the cardia region which directly reach the coeliac artery or blood vessels in the left renal sinus. The splenic territory of lymphatic drainage has its source close to the tip of the fornix gastricus and its collecting ducts accompany the short posterior gastric vessels. The hepatic drainage territory originates in the aboral section of the corpus gastricum from greater to lesser curvature and the total pars pylorica. The above-mentioned different growth intensities of the gastric walls, as well as the growth of the bursa omentalis (Miethe, 1960), has the effect that the right and left nervus vagus have different regions of supply, as has already been documented by Brandt (1920): The left vagus supplies the fornix and the upper two thirds of the corpus gastricum as well as the pars pylorica of the paries anterior (ventral side) of the stomach. The right nervus vagus supplies the cardia, the curvatura minor and some parts of the corpus gastricum as well as the prepyloric section on the paries posterior (dorsal side) of the stomach.

backwards from the pyloric orifice, followed by a second part that passes vertically and caudally (Ayer, 1948). The end of this second part and the following part form an acute angle between them. The third part passes cranially and to the left. The C-shaped concavity of the duodenum is filled by the pancreas; the capud pancreatis also touches the pars transversa duodeni. The procesus uncinatus of the pancreas “accompanies” the third duodenal part, the pars ascendens. The pars descendens duodeni has the shortest mesentery of all small intestines in Primates. As compared with other Primates, the anatomy of the human gastrointestinal tract is certainly the most intensively studied morphological structure. Villi intestinales could be identified as finger- and leaf-shaped surfaceincreasing structures by Da Costa (1972), and Trier (1963) identified Paneth cells at the base of crypts. Goblet cells producing mucus could also be found. Pink et al. (1967) describe absorptive-, Paneth-, goblet- and argentaffinecells in the lamina epithelialis of the small intestine. Six types of endocrine cells were detected in the duodenal mucosa in biopsies (Frexinos et al., 1973). Especially in the pars superior duodeni and the beginning of the pars descendens duodeni (“deuxième duodénum”) in humans, the total number of endocrine cells is high, representing 5% of the epithelial cells; in the pars transversa (“troisième duodenum”), they represent just 1 to 2%. Endocrine cells are rare amongst the enterocytes of the villi intestinales. In primates, Brunner’s glands are present in the tela submucosa of the duodenum. They form a “continuous carpet” beneath the lamina muscularis mucosae, but this “carpet” ceases just beyond the papilla of the ductus choledochus (Hill, 1958). In Macaca sp., isolated glands can be found down to the end of the duodenum. In Homo and in hominid apes, plicae circulares can be found in the small intestine, but in the orangutan, Pan troglodytes, they can rarely be found. In other primates, the presence of circular folds has been much disputed (Hill, 1958).

14.4 Small intestine of the Haplorrhini

14.5 Colon of the Haplorhini

According to Straus (1936), the topography of the duodenum in the orangutan (Pongo pygmaeus) is similar to that in man. The pars superior lies intraperitoneally, but the following sections are retroperitoneal, namely, the pars descendens and a terminal horizontal portion that is somewhat longer than the superior. “An ascending portion is clearly absent and in this the animal contrasts markedly with adult man” (Straus, 1936, page 19). In the Northern Plains grey langur, Semnopithecus entellus, the duodenum forms a C-shaped loop (no good illustration was found), consisting of a part that is directed

The suborder Haplorrhini consists of two infraorders, the Tarsiiformes and the Simiiformes (Groves, 2005). The compilation of outlines of the large intestine of Haplorrhini (Fig. 4.3), which has been adapted from the publication of Straus (1936), shows very simple situations in two species of the Tarsiiformes. This is in full accordance with an illustration that was originally published by van Loghem (1904) (Fig. 4.36). He mentions that the postcaecal section of the colon in Tarsius shows reduced growth. Grassé (1973) calls the situation in Tarsius sp. “primitive”. The colon transversum is very short and the colon

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descendens straight; according to Hill (1958) taeniae are lacking from the whole of the hindgut in Tarsius. As a whole, the colon is very short and lies on the left side of the abdomen (Klaatsch, 1892). According to this author, Tarsius has the shortest gastrointestinal tract of all species he investigated. Following Wilson and Reeder (2005), the second infraorder of the Haplorrhini, the Simiiformes, consists of the following families (those set in italics are considered in this text): Cebidae, Atelidae, Aotidae, Pitheciidae, Cercopithecidae with the two subfamilies Cercopithecinae and Colobinae. The Hylobatidae and the Hominidae also belong to the Simiiformes. From different sources, illustrations of the large intestine of the Cebidae have been compiled in Fig. 4.37. The large intestine of Callithrix sp. (Marmoset) has been illustrated by Klaatsch (1892), van Loghem (1904). It can be seen that the ileum opens into the large intestine perpendicularly and that the colon ascendens lies “in line” with the caecum. Considering the variability of the colon transversum in humans – which can run from right to left in a more or less straight horizontal line, or can form a loop – it is questionable whether the differences between the straight course of the colon transversum in Callithrix sp., as shown in the illustrations published by Klaatsch (1892), and, on the other hand, the small “loop” that is shown in the illustrations of van Loghem (1904) and Hill (1958), are of real significance. Vermes and Weidholz (1930) mention that the large intestine in Callithrix penicillata is “long”. A single taenia, on the greater curve of the colic arcade may appear in some Callithricidae, two taeniae, of a transient nature, have also been reported by Hill (1958); they can be seen in the illustrations originating from

van Loghem (1904) in Fig. 4.37. At the bottom of this illustration, the outline of the large intestine of Cebus capucinus, the white-headed capuchin, based on an illustration from Klaatsch (1892), is shown. The colon descendens is slightly longer than the colon ascendens and taeniae are lacking from the whole of the hindgut at all times in Cebus (Hill, 1958). According to Vermes and Weidholz (1930), the large intestine of Cebus paella, the tufted capuchin, has neither taeniae in its colon nor haustra. The same authors mention for three species of the Atelidae (Ateles belzebuth, the white-fronted spider monkey, Lagothrix lagotricha, brown woolly monkey, and Alouatta seniculus, the Venezuelan red howler monkey) that the colon is relatively short.

Fig. 4.36: Illustration of the large intestine in Tarsius tarsier. Adapted from van Loghem (1904).

Fig. 4.37: Illustrations of the large intestine in two species of Cebidae. Adapted from Klaatsch (1892) and van Loghem (1904).



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When three taenia occur, they are usually arranged equidistant from each other, one along the line of the mesocolic attachment, one dorso-laterally and the third ventro-laterally (Hill, 1958). This is the arrangement on the human ascending colon. At the flexura coli dextra, the positions change according to the manner of slinging of the transverse colon, but the bands return to their earlier disposition on the descending colon. Callimicio goeldi, Goeldi’s marmoset, is unique among Primates in having no mesocolic taenia. The other two are situated dorsomedially and ventro-medially equidistant from the mesocolic attachment. In contrast to the situation in the Cebidae, the large intestine of the Cercopithecidae is relatively long. This is corroborated by the high relative volume of the large intestine (above 50% of the total gastrointestinal tract) in two species of Cercopithecus (Fig. 4.38) as has been presented by Bruorton and Perrin (1991). Illustrations of the large intestine of the genus Macaca have been published by (van Loghem (1904); Fig. 4.39, and Straus, 1936, Fig. 4.3). From these illustrations, it is unclear whether the general shape of the colon can be compared with a simple upside-down “U” or whether a caudally directed loop can be found. Here, again, individual variability can be the reason for the variable shapes depicted by different authors. However, van Loghem (1904) shows a taenia on the total course of the colon. The same is also true in Cercocebus sp. and Cercopithecus sp., which are both depicted in illustrations, which were originally published by Chivers and Hladik, 1980). The subfamily Colobinae of the Cercopithecidae Fig. 4.39: Illustrations of the large intestine of Cercopithecidae. Above the dashed line a species of Cercopithecinae and below three Colobinae can be found. Adapted from different authors.

Fig. 4.38: Relative volume of stomach, small and large intestines in two species of Cercopithecus. Raw data from Bruorton and Perrin (1991).

is of great interest because they have a voluminous forestomach with taeniae and haustra. The question comes up whether the consequence of pre-acid microbial fermentation in the forestomach might be a morphological reduction in the large intestine? Illustrations, originally published by Polak (1908) and Ayer (1948), are presented at the bottom of Fig. 4.39. The northern plains grey langur, Semnopithecus entellus, has a relatively long caecum with three taeniae, which extend to the colon (Ayer, 1948). According to Polak (1908), the colon ascendens in two species of Colobus is long and forms a kneelike bend. The colon transversum forms a loop, which is not shown in Polak’s (1908) illustrations and taenia and haustra cannot be found in these presentations. The illustrations of the colon of Colobus guereza (mantled guereza) and Trachypithecus vetulus (purple-faced langur) show

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that branches of the A. mesenterica inferior extend up to the flexura coli dextra. According to Hill (1958) the large intestine of a representative of the primate family Atelidae, the black howler monkey, Alouatta caraya does not show any traces of taeniae and haustra. On the other hand, for Pongo pygmaeus, the orangutan, as a representative of the family Hominidae, the same author presents an illustration of the large intestine with impressive taeniae and haustra. Contrary to conditions in man (Homo sapiens), the more distal section of the colon transversum of the orangutan forms a considerable loop, which is much more extensive that the human colon transversum loop, that has been impressively demonstrated in the x-ray photos published by Altaras (1982). A simple criterion, like the digesta contents in different sections of the large intestine, gives an impression that this section of the gut itself is differentiated. Because of medical interests, the large intestine of humans has been intensively studied. Roith (1903) differentiated

sections of the human large intestine. In Fig. 4.40, three sections of the large intestine are depicted in a ternary diagram: The caecum together with the colon ascendens represents one section, which is followed by the colon transversum. The final section is composed of the colon descendens and colon sigmoideum. Data of digesta contents for different sections of the large intestine in humans of different ages are considered: Age dependence of filling in patients that died of different diseases, cannot be seen, but one thing is obvious: The colon descendens plus the colon sigmoideum always contain less than 50% of the digesta and liquids in the large intestine. On the other hand, the caecum plus the colon ascendens, on the one hand, and colon transversum, on the other, seem to be a functionally uniform space, which together represents the preferred site of digesta storage in the human large intestine. On the other hand, the movement of digesta from the opening of the ileum into the large intestine in humans takes place in three to four “steps” of mass movements into the colon sigmoideum (Pichotka, 1975). When Roith

Fig. 4.40: Digesta contents in three sections of the large intestine in humans that died of different causes. Raw data from Roith (1903).



(1903) found reduced contents in the colon descendens and sigmoideum in cadavers, this might be the result of the last defecation before death. It has already been mentioned above that the large intestine is a site where food of plant origin is degraded. Milton (1987) studied different species of the Hominidae under consideration percentage of the total feeding time when plant material is ingested (Fig. 4.41). This compilation of her data indicates that an intensive use of plant food means that a high percentage of the volume of the gastrointestinal tract is represented by the large intestine (the caecum and the colon are not differentiated here). Mountain gorillas (Gorilla gorilla) are almost exclusively herbivorous. Orangutans (Pongo pygmaeus) and siamangs (Symphalangus syndactylus) both eat notable amounts of leaves, shoots, stems and/or bark, as well as fruit and some insect matter. Chimpanzees (Pan troglodytes) focus very strongly on fruit in the diet, eating some foliage and a low percentage of animal matter. In “average” humans, where only two thirds of the feeding time deals with plant food, the relative volume of the large intestine is considerably reduced. Pichotka (1975) even claims that the human large intestine is not necessary for life and that nutritional deficits cannot be found in patients where the large intestine had to be removed completely. Although patients who had to submit to such a radical removal do not agree to the statement of Pichotka (1975), it indicates that an effective digestion of a more omnivorous food, as it can be found in

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many humans, can be accomplished with relatively little participation of the large intestine.

14.6 Caecum of the Haplorrhini The caecum can either lie intraperitoneally, being completely covered with peritoneum (Berry, 1895a) or it can be “soldered” to the dorsal abdominal wall. In man – contrary to conditions in domestic mammals – the caecum is a part of the colon (Simic and Ilic, 1976); in many species, the boundary of the caecum against the colon ascendens is difficult to determine and cannot clearly be differentiated from the following section of the large intestine. In the Cebidae (e.g. Saguinus, Callithrix, Cebus, Saimiri) and Atelidae (Lagothrix and Alouatta), the caecum is capacious, hook-shaped and the apex is bluntly and broadly rounded (Hill and Rewell, 1948, [Fig. 4.12] and Flower, 1872, [Fig. 4.13 E]). Starck (1958) writes that the terminal part of the caecum in Callithrix jacchus makes a hairpin-shaped sharp bend, which reaches far to the left, but the caecal tip shows to the right. According to the same author, the cranial tip of the caecum in Lagothix lagotricha shows craniad and to the right. In the Aotidae and the Pithecidae, the caecal apex is not broadly rounded, but a narrowed and hook-shaped distal end of the organ is formed; in Tarsiidae, its distal portion is narrowed and curved (Fig. 4.12). In the Cercopithecidae, there is a strong demarcation between the strongly sacculated

Fig. 4.41: Contribution of volumes of stomach, small and large intestines relative to volumes of the total gastrointestinal tract in five primate species. Adapted from Milton (1987).

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proximal caecal sac and the narrow and thick-walled apical segment (Hill and Rewell, 1948). In the Cercopithecidae, as well as in the Hylobatidae and Hominidae, the caecum is characterised by taeniae and haustra, generally in three rows. However, Hill and Rewell (1948) mention only two distinct taeniae, as well as a third “indistinct” one for the cercopithecid genus Erythrocebus sp. According to Starck (1958), the caecum of Colobus polykomos has taeniae and haustra, and in Pygathrix nemaeus, two poorly developed taeniae can be found in the wall of the organ, but the apex is covered by a complete longitudinal muscle coat (Caton, 1998). Following Ayer (1948), the proximal section of the caecum has three taeniae in Semnopithecus entellus, but at the apex, these taeniae merge and form a continuous coat. It has been made clear previously (Langer and Takács, 2004) that the number of three taeniae and three rows of haustra represents a differentiation of the gut wall that is very efficient in the regulation of digesta transit. In Hylobatidae and Hominidae, a narrow appendix vermiformis is differentiated on the apex of the caecum with a sudden reduction of diameter or calibre between the apex and the appendix vermiformis. This organ is rich in lymphatic tissue and in some species, for example, in Pan troglodytes, it can be really “vermiform” = worm-like. In the chimpanzee, it can be longer than 30 cm and intensively coiled or convoluted (Hill and Rewell, 1948). According to Vermes and Weidholz (1930), the appendix vermiformis is absent in the Cebidae, Atelidae and Cercopithcidae. The human caecum – and especially its appendix vermiformis – has been studied extensively over the course of a long time. For example, Treves (1885) characterised four types of differentiation of the distal part of the caecum (Fig. 4.42): The first type is characterised by a conical shape of the apex region, where the appendix begins; there are three approximately equidistant taeniae. In a second case, the distal end of the caecum is bluntly rounded with two bulging haustra. There is a sharp reduction of the calibre from the caecum proper to the appendix vermiformis. The present author is sceptical whether the following two types of caecal form are really permanent differentiations. In the third type of caecal differentiation, the part that lies to the right of the taenia libera grows quite out of proportion and the true apex with the beginning of the appendix lies between the two bulging haustra and close to the root of the appendix. The haustra between the ventral taenia libera (black in all four figures) and the taenia omentalis (hidden in all four panels and lying to the left, i.e. anatomically to the right of the caecum) are strongly dilated. In type 4, the section to the right of the taenia libera grows excessively so the appendix lies dorsal

and to the left of the angle between distal ileum and proximal colon (Treves, 1885). The differences in the position of the appendix vermiformis relative to the caecum are of importance during surgical appendectomy. The caecum is a region of the digestive tract which is of great importance as a site where microbes live, multiply and help to degrade food into absorbable molecules (“alloenzymatic digestion”, Langer, 1988). According to Gebbers and Laissue (2004), bacterial colonisation of the human newborn intestinal tract begins immediately after birth and lasts throughout the first year of life. The production of mucus represents the micro-environment which covers the mucosa and represents the source for microbial metabolism (Abrams, 1977), thus forming “biofilms”. Abrams (1977) states that the mucosa-microbe interaction is influenced by immunological factors and helps to maintain the qualitative and quantitative equilibrium of the normal microbial flora of the intestine. Certain bacteria can only become pathogenic after adhesion or even penetration of the intestinal lining (Bazin, 1980). Hess et al. (1975) show in a diagram that passage of digesta is very slow in the caecum and the length of the contact between digesta and mucosal epithelium

Fig. 4.42: Four types of human caecum and appendix vermiformis. Modified after Treves (1885).



increases drastically in the caecum and colon ascendens, as does the concentration of microorganisms, normal and pathogenic ones (Gebbers et al., 1981). Microbes in the gut, including the caecum, play an important metabolic role. Synthesis of vitamins B7 and K, ion absorption, fermentation of dietary fibres are the effects of microbial activity. However, the contribution of the human caecum to bacterial multiplication and number cannot clearly be differentiated from the contribution of the colon. Stevens and Hume (1998) mention that most of the urea entering the hindgut is hydrolysed to ammonia by bacteria attached to the epithelial surface, but a differentiation between the colon and the caecum is not made. Caecum fermenters represent one type of alloenzymatic digestion; a clear illustration of a caecum fermenter was given by Hladik (1978) (Fig. 4.43): After a food has been ingested by Lepilemur leucopus, protein content decreases in the stomach because it is partly digested, but later in the caecum, protein increases drastically; it shows the highest value of the total large intestine, certainly because of the high concentration of microbial protein. Foregut fermenters are found in the subfamily Colobinae of the family Cercopithecidae, colon fermenters are the non-colobine Cercopithecidae, as well as Hylobatidae, Pongidae and Hominidae; finally caecum fermenters are represented by Daubentoniidae, Lemuridae, Cheirogaleidae, Lorisidae, Cebidae and Callitrichidae. Caecal and colonic microbes produce volatile fatty acids (VFAs), also in humans. For example, in the caecum, Cummings et al. (1989) measured approximately 130 mmol/kg and observed a progressive decline towards the distal colon. Almost all the produced VFAs are

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absorbed and contribute 6 to 9% of the human energy requirements (McNeil, 1984). This absorption makes 75% of the original carbohydrate energy available to the human, 25% is used by the gut microflora for growth or is partly lost as hydrogen and methane gas.

14.7 Appendix vermiformis in Primates A caecum with a true vermiform appendix is characteristic of gibbons (Hylobatidae) and Hominidae, including man (Cave, 1936). According to the same author, there might be a capud caeci with lymphoid follicles in subprimate forms. The true appendix vermiformis arises from a capacious caecum and is a differentiation of that organ. Formation of a double caecum is extremely rare, but has been described in a human patient by Kabay et al. (2008). According to Köpf-Maier (2000), the human appendix can lie in retrocaecal and retrocolic positions; it can extend, alternatively, in a “pendulous position” into the lesser pelvis and it can either be positioned before (prae-ileally) or behind the distal ileum (retro-ileally). There is a wide range of the relative length of the appendix as compared with the caecum. In male Nycticebus borneanus, it can be as low as 0.69; in an adult white human female, it was as long as 2.5 times the length of the caecum (Straus, 1936). The fact that an appendix can be removed from human patients without negative consequences does not mean that the organ is useless (Muthmann, 1913), nor is it a vestigial organ (Keith, 1912). Even relatively recent papers still mention this uselessness and vestigial situation in their introductions, but indicate a relationship with the

Fig. 4.43: Protein content (% of dry weight) of food and digesta in five regions of the digestive tract in Lepilemir leucopus. Raw data are from Hladik (1978).

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establishment of a body defence (Malla, 2003; Smith et al., 2009, 2013; Cakmak et al., 2014). According to Berry (1895b), the appendix atrophies with increasing age in man. A function of the appendix may be to maintain cultures of microbes in a state that is able to perform their function on the digesta contents of the caecum (MacEwen, 1904). Eggeling (1920) believes that the human appendix vermiformis represents a rudimentary organ, formed out of a more voluminous caecum. The presence of a vermiform appendix can be considered as a shared, derived character uniting the Hominoidea (apes and humans) (Fisher, 2000). In two publications remarks on the ontogeny of the caecum and its appendix can be found. According to Grand et al. (1976), the caecum in man is first identified in the 5th week of foetal life, and in the 10th week of foetal development, the caecum can already be found in the lower right quadrant of the abdominal cavity (Fröber et al., 1991). This means that there is no descensus caeci. This is in contrast to a statement of Larsen (1993), who writes that after the 11th foetal week the caecum is displaced inferiorly, pulling down the proximal hindgut to form the ascending colon. In the same period of time, i.e. by the 11th to 12th foetal” week, taeniae and haustra appear (Grand et al., 1976). The ontogenetic differentiation of an appendix has beeen investigated in the 20th century. According to Jacobshagen (1922), the caecum is differentiated on the side opposite to the line of fixation of the (dorsal) mesentery, i.e. it is a structure that is positioned on the ontogenetically ventral side of the gut anlage. The caecum is formed in the 5th or 6th foetal week and the human appendix vermiformis can first be discerned during the 8th foetal week; Gluckmann (1939) states that the appendix appears at the beginning of the second month of pregnancy, which is in accordance with a statement in the textbook of Hamilton and Mossman (1972), who mention 39 days. The belief of Gluckmann (1939) cannot be corroborated that the formation of an appendix is related with the development of upright body position, which produces tension on the developing caecum and provokes its hypertrophy. In a later publication, Gluckmann (1947b) repeats his statement on the relationship between differentiation of an appendix and upright body position.

14.8 Cercopithecoidea: Colobinae (mainly dealing with the stomach) 14.8.1 Introductory remarks Distribution maps of African and Asian colobines, as well as a review of biotopes and data on colobine body masses

can be found in Oates et al. (1994). The evolutionary history of colobines was studied by Delson (1994). In the Late Miocene and in the Pliocene of southern Europe (Maschenko and Marareskul, 2011) and in the Pliocene of eastern Africa, colobines were more numerous than cercopithcines. According to Delson (1994), the earliest colobine, Mesopithecus pentelicus, lived in Eurasia. In Europe, colobines were dominant members of the primate fauna. The oldest definitely colobine fossil from Africa lived between 10 and 9 million years ago (Miocene) in central Kenya. At that time, the flora of that area was influenced by the presence of C4 plants with grasses and dwarf shrubs – all materials that are difficult to digest. Wang et al. (2013) differentiated the Colobinae into two “subtribes”, one from Africa with the three genera Colobus, Procolobus and Piliocolobus. The Asian “subtribe” is represented by the Presbytina with seven genera that are, according to Wang et al. (2013), clustered into two groups, the odd-nosed monkeys, comprising Pygathrix, Rhinopithecus, Nasalis and Simias, and the langurs with the genera Presbytis, Trachypithecus and Semnopithecus. According to Vun et al. (2011), the genus Presbytis is clearly separated from Trachypithecus and Semnopithecus and Karanth et al. (2008) separate the “leaf monkeys” of the genus Trachypithecus from the langurs of the Indian subcontinent. This already indicates that the colloquial names applied in the literature to the three genera Presbytis, Trachypithecus and Semnopithecus are used quite confusingly. For example, the 11 genera of Presbytis are either called “leaf monkeys”, “langurs” or “Surilis” (Groves, 2005). In the case of 17 species of the genus “Trachypithecus”, the colloquial names “leaf monkeys” and “langurs” are also applied, as well as “lutungs”. The seven species of Semnopithecus are called “grey langurs” (Groves, 2005). Compilations on the phylogeny of Colobinae (Delson, 1975; Wang et al., 2012) indicate that the Asian genera together are monophyletic. Colobus and Piliocolobus from Africa form a clearly monophletic group that is separated from the Asian genera (Wang et al., 2012). The separation of Asian from the African line took place about 12 MYBP, i.e. in the Miocene (Delson, 1994). After the Colobines separated from the cercopithecine stock in the Miocene, the plurilocular colobine stomach must have evolved together with the salivary apparatus (Napier, 1970).

14.8.2 Food of the Colobinae Fibre has a negative effect on foliage selection of colobines; lignin and cellulose in foliage vary in concentration and protein levels also determine foliage selection.



In addition, colobine forestomach microbes can have effects on toxins influencing food selection. To accomplish efficient alloenzymatic digestion and microbial detoxification, colobids practise long bouts of rest during the day (MacKinnon and MacKinnon, 1980). The digestive efficiency of these forestomach-fermenting Colobinae is significantly higher than of large intestinal fermenting primates, such as howler monkeys, Alouatta sp. (Edwards and Ullray, 1999). The retention times and rates of passage of digesta are similar in both types of digestive strategy. The digestive systems of colobine monkeys do not constrain them to folivorous habits. They can digest seeds efficiently (Kay and Davies, 1994). Fruit parts, leaf parts and the occasional insect may all be ingested in a single feeding period and digested effectively. The flexibility of the colobine digestive system may be its most important feature. Müller et al. (1983) speculate that the reduced basic metabolic rate, for example, in the mantled guereza, Colobus guereza, is an adaptation to folivory or to specialisations in the digestive process. The Colobinae are able – although they do not always apply this ability – to digest a low-quality food. Hladik (1979) separated primates into three feeding grades: The first grade ranges from true insectivory (Loris, Arctocebus) towards diets including fruits together with insects (Saguineus, Saimiri). The second grade ranges from insects and other invertebrates to green parts of plants to fruits and/or seeds (Cebus, Cercocebus, Macaca, Papio, Pan). The third grade ranges from frugivorous habits to species obtaining nutrients mainly from leaves (Indri, Lepilemur, Ateles, Gorilla, Alouatta) and digesting them in the colon-caecum section (large intestine) of the gut. In a detailed study, Davies et al. (1988) demonstrate that the differentiation of the colobine stomach into a plurilocular organ does not automatically mean that the species of this primate subfamily can be identified as “roughage eaters”. It is a general problem that the anatomical differentiation of the gastric region in colobines is sometimes “overstretched” by identifying observations with processes in ruminants. For example, Matsuda et al. (2011) observed regurgitation followed with remastication in Nasalis larvatus, the proboscis monkey. These authors speculate that this process would ensure that coarse particles are reduced in size to be alloenzymastically digested at a faster rate – a process resembling ruminant digestive processes. The actions observed in the proboscis monkey are not as complex as the procedures taking place in the ruminant oral cavity, pharyngeals region, oesophagus and stomach, as has been discussed in detail, for example, by Ruckebusch et al. (1981) and Kaske (2000). As long as such thorough studies have not been done in the Colobinae, one should refrain from “creating” analogies.

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Feeding habits are diverse among species of Colobinae (Edwards and Ullrey, 1999). Although Ullrich (1961) writes that colobids are primarily folivores, preferring young leaves, calling all Colobines “leaf-eaters” is premature according to Harrison (1986). Colobines shift to fruits and seeds, but animal matter does not play a great role (Waterman, 1984). It is, however, documented that food preferences within this primate subfamily are quite variable (Oates, 1994). McKey et al. (1981) studied Colobus satanas (black colobus) in Cameroon. The proportion of leaves in the diet of this species was low compared to most other colobine species, and the monkeys spent over half their feeding time eating seeds. A compilation of the types of food that are eaten by Asian colobine species (Pan and Oxnard, 2003) is presented as “X” in Tab. 4.4 In this illustration, Presbytis rubicunda and P. melalophos are indistinguishable. However, Davies et al. (1988) compared the chemistry of plant material eaten by Asian Presbytis rubicunda and P. melalophus, the banded and the maroon leaf monkeys. Both species prefer leaves with high content of protein and low levels of fibre and both treat their nutritional problems differently: P. melalophus eats a wide range of leaves, but P. rubicunda relies on rare trees with higher quality leaves. In relation to the two sympatric Asian colobine species, Bennett and Davies (1994) ask how the two species can coexist without one out-competing the other? Trachypithecus vetulus (purple-faced langur) eats a foliage diet, supplied by abundant evenly distributed food sources. Semnopithecus entellus (northern plains grey langur), on the other hand, feeds from widely dispersed and large food sources. Gautier-Hion (1983) studied the food of a colobine species from Central Africa. The author found in Gabon that the percentage of leaf material eaten by Colobus guereza, the mantled Guereza, is much higher (~50%) than in Cercopithecines without forestomach (~1–16.5%). This indicates that the complexity of the guereza stomach helps to digest leaf material. Piliocolobus badius, the red colobus food consists of 74.8% leaves, 4.2% fruits, 2.6% arthropods (Struhsaker, 1980) and has to be characterised as folivore. Yeager (1989) calls the proboscis monkey, Nasalis larvatus, a folivore/frugivore practicing seed consumption with considerable seasonal variation. On the other hand, Goodman (1989) mentions a grey leaf monkey (Presbytis hosei), which was seen in Sabah, Borneo, to take and eat eggs and possibly a hatchling from a bird’s nest. Foraging behaviour contributes to the procurement of optimal food. For example, Piliocolobus badius from West Africa and Trachypithecus franciosi, François’ langur,

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Tab. 4.4: Food eaten by Asian species of Colobinae. Bark Langurs Presbytis rubicunda Prebytis melalophos Presbytis comata Semnopithecus entellus Trachypithecus vetulus Trachypithecus phayrai Trachypithecus francoisi Trachypithecus obscurus Trachypithecus cristatus Odd-nosed monkeys Nasalis larvatus Pygathrix nemaeus Rhinopithecus avunculus Rhinopithecus roxellana Rhinopithecus bieti Rhinopithecus brelichi

X

Twigs

Grass

X

Herbs

X

Buds

X

Fungi

Lichen

X

X X

X

X

X X

X X

Leaves

Flowers

Seeds

Fruits

X X X X X X X X X

X X X X X X X X

X X

X X X X X X

X X X X X X

X X

X

X X

X X X

X X X X X X

Animal

X

X

Raw data from Pan and Oxnard (2003).

from China are selective in their choice of food and regularly select particular parts of particular species (CluttonBrock, 1975; Zhou et al., 2006). On the other hand, food eaten by Colobus guereza (mantled guereza) is much more monotonous than that of Piliocolobus badius (Struhsaker and Oates, 1979), which eats a variable diet (Teaford, 1986). Selectivity of food intake by P. badius in Kenya was emphasised by findings of Marsh (1981): Contribution of plant parts to the eaten diet did not correlate with the availability of that material. C.  guereza dedicated about half of its feeding time to acacia leaves (Rose, 1978). For the black colobus, C. satanas, Harrison and Hladik (1986) write on page 295: “The Black colobus feeds predominantly on immature seeds, unlike most of its folivorous relatives, while the consumption of young leaves is second in importance”. Seeds “always dominate in the monthly diet”. Galat-Luong and Galat (1979) describe an even more “aberrant” type of food for Pennant’s red colobus: Piliocolobus pennanti was seen in Central Africa to feed on aquatic plants. Rhinopithecus bieti, black snub-nosed monkey from China, on the other hand, feeds primarily on lichens (Kirkpatrick et al., 2001). Waterman and Ross (1988) investigated chemistry of leaves that were selected by Colobines for food. According to these researchers, foliage is selected to maximise the intake of protein and to minimise the intake of fibre and tannins. It is interesting that toxic alkaloids in the foliage do not appear to be general deterrents to feeding since many such compounds can probably be detoxified by the foregut bacteria.

From the above comments on colobine food, it becomes plausible that species belonging to this primate subfamily may be of ill health in zoos. For example, Aiello and Moses (2010–2013), in Merck Veterinary Manual, write that rich, rapidly consumable diets given to colobines may frequently cause gastrointestinal problems and dietary changes should be accomplished gradually to allow the gastric microflora to adapt. Hollihn (1971) mentions that the most common disease in captive colobines is diarrhoea, which is to be found most frequently when no leaves are available.

14.8.3 Short account of previous publications on the macroscopic anatomy of the stomach in Colobinae More than two centuries ago, Van Wurmb (1787) mentioned that the stomach of a Southeast Asian species of the Colobinae, the proboscis monkey, Nasalis larvatus, is exceptionally (“buitenmaaten”) large and of monstrous (“onvormig”) size. In a more recent publication on the microbiology and food in African rainforest herbivores, Waterman et al. (1980) speak of “colobine monkeys with ruminant like digestive tracts”. However, the stomach of the Colobinae is quite different from that of the ruminants, as will be shown in the following. The number of more detailed investigations in the digestive tract of different species of the Colobinae is not large. Owen (1833, 1835, 1841), Carus and Otto (1835), and Keith and Wood Jones (1902) described the colobine



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stomach just briefly and Pilliet and Boulart (1898) gave a description that was partly influenced by analogies with the ruminant stomach; they call the sacciform forestomach “la panse”, the rumen. Otto (1825) presented a paper on the anatomy of Trachypithecus vetulus (purplefaced langur) and Duvernoy (1835) studied and depicted Semnopithecus entellus (Southern plains grey langur), which was depicted by Duvernoy (1835) (Fig. 4.44). This illustration shows clearly that the sacciform forestomach of this langur has a diverticle (praesaccus), which lies close to the cardia. Hombron and Jacquinot (1845), referring to Otto (1825), Duvernoy (1835) and Owen (1833, 1835), present additional observations: They describe the aspect of the stomach of Semnopithecus as similar to the large intestine of the horse because haustra and two longitudinal bands, taeniae, can be discerned. According to them, a “pear-shaped” and a colon-like section can be differentiated. Polak (1908) described the anatomy of the genus Colobus, and Berenberg-Gossler (1911) gives a very detailed description of Semnopithecus entellus and refers to a few other Colobinae, such as Nasalis larvatus (proboscis monkey). He also followed the embryological differentiation of the colobid type of stomach. A detailed anatomical description of Semnopithecus entellus is also given by Ayer (1948). Schwalbe (1912) subdivides the stomach of colobines into sections which can also be found in the stomach of humans: In both cases – humans, as well as in Semnopithecus sp. – the organ has a proximal pars digestioria and a distal pars egestoria. These, again, can be subdivided (Fig. 4.45). Hill (1952, 1958) presents very detailed investigations on form, position, and proportions of the whole colobine digestive tract under comparative aspects. Starck (1957, 1958) gives detailed information on the topography of

colobine abdominal organs. Kuhn (1964) extended these investigations by considering histology and function in the stomach of the Colobinae and Hollihn (1971) presented additional information on food uptake, behaviour, but also gastric anatomy in the guereza (Colobus guereza and C.  polykomos), the proboscis monkey (Nasalis larvatus), and the Douc langur (Pygathrix nemaeus). Chivers and Hladik (1980) published an excellent paper comparing primates with other mammals in relation to diet; they also considered colobine species. Suzuki et al. (1985) compared mucosal lining of the stomach among colobine, noncolobine Haplorrhini and strepsirrhine monkeys. After the publication of a treatise on the stomach of colobus monkey by Langer (1988), the results of an extensive and excellent study by Chivers (1994) became available: He treated the functional anatomy of the gastrointestinal tract comparatively and in considerable detail and Caton (1997, 1998, 1999) supplied valuable data on African and Asian Colobinae. The following discussion on the anatomy of the colobine stomach will refer extensively to the publications by Caton, Chivers and Langer.

Fig. 4.44: Stretched-out stomach of Semnopithecus entellus with modern terminology. Adapted from Duvernoy (1835).

14.8.3.1 General subdivision and position of the colobine stomach At the beginning of this section, the reader should be aware of some terminological misconceptions, which have been dealt with in some detail by Chivers (1994). The misunderstanding refers not only to anatomical aspects of the stomach, but also to functional facts related to the total gastrointestinal tract. The following is the verbal citation from pages 205 to 206 of Chivers (1994). In this context, it is the first point that is of importance here, the other two are cited to give the complete argument presented by that author: “First, no mammal has more than one stomach; what varies is the complexity of the stomach, so that ‘compound’ and ‘simple’ are more correct than ‘polygastric’ and ‘monogastric’, respectively. Second, it is

Fig. 4.45: Subdivision of the human and colobine stomach. Adapted from Schwalbe (1912).

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not just the caecum that provides a fermenting chamber (‘caecal fermentation’); the first part of the colon (primitive right colon, embryologically) is equally, often more, important, since it is usually, especially in the primates, much more voluminous than the caecum. Third, these parts of the gut are not ‘hindgut’, which refers only to the descending (left) colon and rectum, which are very similar in all mammals, and have a different blood supply (because of the different embryological origin) from the caecum and right colon, which develop from the ‘midgut’ loop. Hence, the need to refer to ‘caecocolic’, ‘midgut’ or ‘intestinal’ fermentation, in contrast to ‘forestomach’ fermentation” (Chivers, 1994). An illustration that shows the stomach of the northern plains grey langur, Semnopithecus entellus, has been published by Pernkopf and Lehner (1937) (Fig. 4.46). It gives an idea about the general gastric “layout”. Kuhn (1964) distinguishes three, and in some cases four, parts of the stomach in the Colobidae. The “saccus gastricus”, the “tubus gastricus” and the “pars pylorica” can be found in all species (Fig. 4.47) There are, however, a few species where a “praesaccus” forms a diverticulum of the “saccus gastricus” (Fig. 4.48) and lies topographically dorsal to the saccus gastricus (Caton, 1998). Langer (1988) showed the presence or absence of the praesaccus in different species of the Colobidae. Chivers (1994) mentions the difficulty to equate the dichotomy of ‘leaf-eaters’ and ‘seed-eaters’ with differentiation or absence of a praesaccus. Caton (1997) writes that the saccus of Presbytis melalophos and P. rubicundra, Trachypithecus vetulus, T.  cristaus and T.  obscurus, Semnopithecus entellus and Colobus polykomos, forming a tripartite stomach, is augmented by a presaccus only in

Fig. 4.46: Opened stomach of Semnopithecus entellus. Adapted from Pernkopf and Lehner (1937).

Fig. 4.47: Two aspects of the stomach of a juvenile Colobus guereza seen from the right (a) and left (b) side of the abdomen. Adapted from Langer (1988).

Nasalis larvatus and Pygathrix nemaeus (quadripartite, Caton, 1997). In addition, Langer (1988) mentions a quadripartite stomach for Presbytis chrysomelas and Procolobus verus. Procolobus eats 14–48% fruit parts annually and few mature leaf parts; Nasalis eats few mature leaves, specialising in fruit and young leaf parts and, according to Pan and Oxnard (2003), even on animal matter. “The functional significance of the praesaccus is not clear” (Caton, 1997, page 403). She suggests that because of its musculature the praesaccus of Pygathrix nemaeus might be a food mill. Chivers (1994) speculates that the expansion of the forestomach could be related to a seed-eating adaptation, but it would be more likely that the addition of the presaccus represents a “leaf-eating” adaptation. Differentiation or absence of a praesaccus was compiled in Tab. 4.5 under consideration of information published by the following authors: Otto (1825), Owen (1835) Keith and Wood Jones (1902), Polak (1908), Berenberg-Gossler (1911), Ayer (1948), Hill (1952, 1958), Starck (1957, 1958), Kuhn (1964), Bauchop and Martucci (1968), Moir (1968), Hollihn (1971), Bauchop (1977, 1978a, b), Langer (1988)

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Fig. 4.48: Dorsal aspects of stomach, greater omentum and resected diaphragm in three colobine species. Adapted from Langer (1988). Tab. 4.5: Tri- and quadripartite saccus caecus in colobine genera. Exclamation marks indicate diverging opinions of different authors. Tripartite saccus gastricus without praesaccus African genera Asian genera Colobus Semnopithecus (!) Trachypithecus (!) Presbytis (!) Quadripartite saccus gastricus with praesaccus African genera Procolobus Piliocolobus

Asian genera Semnopithecus (!) Trachypithecus (!) Presbytis (!) Rhinopithecus Pygathrix Nasalis

and Caton (1997). Both African and Asian colobine genera were considered. Kuhn (1964) and Langer (1988) made attempts to compare the anatomical terms used by different authors. Because of its complex form the position of the colobid stomach in the abdomen is different from that of other primates. The gastric sac lies in the left hypochondrial region; it is partly fixed to the diaphragm by a pars affixa. This pars

affixa is bordered by the peritoneum in that area where the visceral sheet passes into the parietal one, forming the ligamentum gastro-phrenicum (Fig. 4.49). The left hepatic lobe is pushed between the saccus gastricus and the diaphragm only in foetal Colobidae, but later during ontogeny, it lies ventrally. In a strongly macerated stomach of an (almost?) adult Procolobus verus (olive colobus), the praesaccus and saccus bulged out in the direction of the left abdominal wall (Fig. 4.48). In a cross-sectioned juvenile specimen of Presbytis melalophus (Sumatran Surili), a species without a praesaccus, the saccus situated in the left cupula of the diaphragm. Around the cardia the saccus gastricus is affixed to the centrum tendineum of the diaphragm. Only a small part of the gastric sac lies on the right side of the median plane. From this part the gastric tube first turns up slightly dorsally, then caudally (Figs. 4.50 and 4.51 a). It is attached to the gastric sac, on which it also turns slightly ventrally. Then the tube makes a sharp bend to the left on the caudal wall of the gastric sac and afterwards a U-turn. Subsequently it can be followed dorsally. With a constriction the tube is separated from the small pyloric part that lies near the medial plane and dorsalmost in the abdomen under the aorta descendens. The same general position of the different parts of the stomach have also been described, e.g. by Polak

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Fig. 4.49: Opened saccus gastricus (foetal) in two colobine species. White arrows point into the tubus gastricus or into the praesaccus (b only). Adapted from Langer (1988).

Fig. 4.50: Opened tubus gastricus of Nasalis larvatus (foetal) seen from the right side of the abdomen. White arrow points into the saccus gastricus. Adapted from Langer (1988).

(1908) and Hill (1952, 1958). The spleen, a triangular organ in the Colobidae, lies in a space formed by the left caudal wall of the saccus gastricus and the sharp U-turn of the tubus gastricus. Its relation to the greater omentum will be considered later. 14.8.3.2 Form of the colobine stomach In specimens with a simple gastric sac without praesaccus, the first part of the stomach is spherical or ovoid

(Fig. 4.52), with the transverse axis being slightly shorter than the cranio-caudal and the dorso-ventral axis. On the other hand, in those forms where a praesaccus has been differentiated, as in Procolobus verus or Nasalis larvatus, the very voluminous oralmost parts of the stomach, the saccus gastricus plus praesaccus, form a U-shaped structure (Hill, 1952) with the praesaccus forming a blind end and the saccus representing the connection towards the tubus gastricus. In juvenile and foetal specimens of



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Fig. 4.51: Stomach of Presbytis comata seen from the right (a) and left (b) side of the body. Adapted from Langer (1988).

Fig. 4.52: Two aspects of the stomach and greater omentum of a juvenile Colobus guereza, seen from the right (a) and left (b) side of the abdomen. The omental “apron” covers the gut. Adapted by Langer (1988).

Nasalis larvatus and Presbytis chrysomelas, the U-shape is not clearly seen because the praesaccus is much smaller than the saccus (8% of total saccus plus praesaccus in Nasalis larvatus, 15% in Presbytis chrysomelas and 50% in Procolobus verus). The small praesaccus is a dorsal diver-

ticulum directly touching the dorsomedial part of the left cupula of the diaphragm (Fig. 4.48 a). It is not wrapped into the greater omentum, but it lies directly dorsal of the line of fixation of this mesogastrium. Fig. 4.48 illustrates conditions of foetal specimens of Nasalis larvatus

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(proboscis monkey, a) and Trachypithecus cristatus (silvery lutung, b). The gastric tube is not visible in dorsal views because it is covered by the diaphragm, spleen, kidney, and adrenals. In addition, the great size of an (almost?) adult Procolobus verus (olive colobus) is also illustrated in a dorsal view in Fig. 4.48 c. Taeniae are characteristic for the gastric sac and the tube of the Colobinae (Fig. 4.47). They represent bands of the external muscular layer. Two of these structures can only clearly be differentiated on the saccus gastricus. The first one starts on the cardia, then turns left and in species with a praesaccus can be followed between saccus and praesaccus. In colobids with and without praesaccus, the above-mentioned taenia runs ventrally over the left wall of the saccus, crosses the greater curvature of this gastric compartment and can be followed dorsally until it passes over the tubus gastricus. The second taenia also starts at the cardia and after a very short length crosses over to the gastric tube where it lies directly opposite to the first-mentioned muscular band. Polak (1908) calls this taenia the “taenia curvaturac minoris” because it follows the lesser curvature. The firstmentioned muscular band is called “taenia curvaturae

majoris” by the same author because it follows the greater curvature which lies almost parallel to a transverse plane, a situation which has also been mentioned by Berenberg-Gossler (1911). This author describes the greater curvature to be “turned cranially”. A thickening of the external musculature, forming a star-like structure on the external surface of the saccus of Trachypithecus vetulus (Otto, 1825) could not be found in the available specimens. The two taeniae of the saccus gastricus are “anchors” for the semilunar folds that protrude into the lumen of the gastric compartment (Fig. 4.53, Fig. 4.54). These folds, as well as the haustra or pouches between them, are very probably functionally changing structures. In the small foetus of Presbytis comata (Javan Surili), semilunar folds could not be differentiated in the saccus (Fig. 4.51), but were clearly visible in other individuals; their number and depth changed. In the three species with a praesaccus, no semilunar folds could be discerned on this compartment. However, in Nasalis larvatus and Presbytis melalophus, the praesaccus did not yet have its adult dimensions, and in the available Procolobus verus, the whole stomach was badly decomposed.

Fig. 4.53: Two aspects of the stomach of a juvenile Colobus guereza seen from the right (a) and left (b) side of the abdomen. The curved white arrow points into the saccus gastricus. Adapted from Langer (1988).



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Fig. 4.54: Opened saccus gastricus of an adult Procolobus verus, seen from the left side of the abdomen. The white arrow points into the praesaccus. Adapted from Langer (1988).

The gastric tube is a structure curved in a characteristic manner as has already been described above. Polak (1908) found a third taenia in addition to the “taeniae curvaturae majoris et minoris”. This “taenia tertia” was found close to the lesser curvature in Colobus guereza (mantled guereza). In Semnopithecus entellus, Polak (1908) even found a “taenia quarta”. She mentioned that these two taeniae are equivalents of the two folds that line the internal gastric sulcus within the tubus gastricus. Investigations of the present author showed that there are no third and fourth taeniae in the tube. In a Colobus guereza, only two taeniae could be seen, in another specimen of the same species the two ridges of the gastric sulcus were (Fig. 4.53 a, b) shining through the wall and gave the external impression of taeniae. Also in the two Asian Colobidae, Nasalis larvatus and Procolobus verus, only two taeniae could be seen. The tubus gastricus presents the aspect of a haustrated colon, as Hombron and Jacquinot (1845) had already mentioned. Taeniae and the semilunar folds and haustra are formed between them (Fig. 4.47). On the ridges lining the gastric sulcus, taeniae and haustra can be “anchored”, although the sulcus gastricus itself is free of semilunar folds and haustra (Polak, 1908, and own findings, Fig. 4.50, Fig. 4.51, Fig. 4.53). The last third of the tubelike gastric part, which is called here the “pars pylorica”, is free of semilunar folds and haustra. Taeniae can also not be discerned on the external surface of this pyloric part (Fig. 4.47). A circular fold, which is not very prominent, separates the tube from the pyloric part and a pyloric constriction separates the latter gastric region from the duodenum.

14.8.3.3 Macroscopic and microscopic internal surface differentiations of the colobine stomach The internal surface of the stomach is sculptured not only through the epithelial lining and internal muscular

folds, but also by taeniae, semilunar folds and haustra. Semilunar folds and haustra are structures that change their position in both saccus and tubus gastricus according to functional conditions of the gastric wall. On the other hand, there are also constant internal folds: The lips begin at the cardia (Fig. 4.50; Fig. 4.51 a; Fig. 4.53 a, b; Fig. 4.54). In those species where a praesaccus is absent, one can be followed into the fold that narrows from ventral the entrance into the gastric tube (Fig. 4.53 b). The cardia is encircled by a U-shaped loop with the abovementioned fold forming one branch of this loop. The second branch can be followed from the cardia crossing under another fold into the tubus gastricus where it forms one of the lips of the gastric sulcus that runs along the lesser curvature. The sulcus ventriculi or sulcus gastricus of Pygathrix nemaeus, the red-shanked Douc langur, described by Caton (1998), follows the lesser curvature of the sacciform and tubiform forestomachs and lies between the above-mentioned two muscular folds on either side of the taenia curvaturae minoris, which forms the base of the groove. One lip is more prominent than the other one. The groove is lined with mucosa, which is similar to the forestomach sac (see in the section 14.8.3.7 Muscle Architecture of the Tunica Muscularis). In Procolobus verus, the right lip of the gastric sulcus continues into the fold that separated the saccus from the praesaccus (Fig. 4.54); this, however, was not the case in Nasalis larvatus. One fold forms the ventralmost lining of the opening of the gastric tube and a lip of the sulcus ventriculi runs along the lesser curvature of the gastric tube. The two lips of the gastric sulcus flatten and end at the sharp bend where the tube in situ turns sharply to the left at about the border between the second and the last third of this gastric compartment (Fig. 4.50). The lips do not extend into the pyloric part of the stomach which is separated from the end of the tubus by a very sharp fold. The internal epithelium appears smooth in the saccus and tubus gastricus as well as in the pyloric part. Only the

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immediate surrounding of the cardia is covered with squamous epithelium (Fig. 4.55) (as described by Hill, 1952) that shows small ridges “radiating” from the cardia in Nasalis larvatus. In the praesaccus of the same foetal specimen, the epithelium of the same macrosopical character could be seen over the whole internal surface of this compartment. The specimen of Procolobus verus was decomposed and a clear image of the mucosal lining could not be obtained. Hollihn (1971) describes the whole praesaccus of Nasalis larvatus and Pygathrix nemaeus to be completely lined with squamous epithelium. This is in disagreement with the findings of Kuhn (1964) and Langer (1988) who did not see the praesaccus to be lined with squamous epithelium. The mucosal lining of the pyloric part is also smooth, but extremely thick. The preservation in the specimens from museums that were available to the present author (Langer, 1988) was not sufficient for histological studies, but the following preliminary statements on the distribution of different types of mucosa can be made: Cardiac glandular mucosa lines the saccus gastricus and the proximal part of the tubus gastricus (Langer, 1988, Fig. 4.55). It seems possible at the present state of investigations that in some species non-glandular squamous epithelium lines the praesaccus (when present) and varying areas of the saccus gastricus. Proper gastric glands can be found in the caudal part of the tubus gastricus and pyloric glands are differentiated in the pars pylorica, at least in Colobus polykomos (Kuhn, 1964). The same author mentions that the border between proper gastric gland and pyloric gland areas is individually highly variable. In his study of the olive colobus monkey (Procolobus verus) Hill (1952) demonstrates that the width of the extension of oesophageal mucosa differs between species. Burkl (1958) found thin mucosa with squamous epithelium on longitudinal ridges that start at the cardia and can be followed along the saccus gastricus of Presbytis sp.

Fig. 4.55: Mucosal lining of the stomach of Colobus guereza. Semischematic illustration of the stretched-out organ. Adapted from Langer (1988).

In Pygathrix nemaeus, the saccus gastricus is lined with squamous epithelium, but in the tubus gastricus Burkl (1958) identified cylindrical or columnar epithelium. Cardiac mucosal lining as described by Bauchop (1978a) and depicted by Langer (1988) is able to absorb shortchain molecules. Parietal cells can only be found in the terminal region of the tubus gastricus. Saccus and tubus gastricus, play a considerable role in absorption. It is not possible to determine whether the saccus or the tubus is the most important site of absorptions. Functionally, it might function like the omasum of the Pecora in relation to absorptive activity. On the other hand, Schwarm et al. (2009) were not able to find a difference in the excretion of fluids and particles in the colobine monkeys, as compared to other foregut fermenters. 14.8.3.4 Volumes of the stomach regions in Colobinae Hill (1954) believes that the simple stomachs of Cercopithecidae, Pongidae and Hominidae are products of secondary simplification, whereas the complex form, as it can be found in the Colobinae, is a retained primitive feature. On the other hand, the same author considers similarities between the colobid and the pecoran stomach as physiological analogies as results of superficially similar organs. To obtain an idea of the relative size of the praesaccus, the saccus and the tubus gastricus, including the pars pylorica, Langer (1988) determined the volumes of different gastric compartments by filling them with moistened cellulose pulp. The volume of the whole stomach was considered as 100% and the percentage of the respective compartments could be calculated. The praesaccus and saccus of Nasalis larvatus, Presbytis chrysomelas, and Procolobus verus could be determined and compared with the respective sacci gastrici of the other specimens. Data on the volumes of these gastric sections that were originally published by Langer (1988) were compiled in a ternary diagram (Fig. 4.56) for six colobine species. Two species where from Africa: Colobus guereza and Procolobus verus, and four live in Asia: Presbytis crysomelas and P. comata, Nasalis larvatus and Trachypithecus cristatus. It is Procolobus verus, which has a very voluminous praesaccus (marked white on black), in Prebytis chrysomelas and Nasalis larvatus the praesaccus is relatively smaller. In three other species (measurements of two specimens of Colobus guereza were available), it is absent. This illustration is shown here to stimulate future investigators to do additional measurements in adult animals. In this case, all seven available specimens were subadult (Langer; 1988).



14 Haplorrhini (“dry-nosed” primates) 

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length, the rotation of the anlage has already occurred, bringing the curvatura major to the left and the curvatura minor to the right. He states that the gastric sac expands transversally, especially in its topographically left wall.

Fig. 4.56: Relative volumes of praesaccus (when present), saccus and tubus gastricus in different colobine species. Black on white: Praesaccus not differentiated; white on black: Praesaccus differentiated. Raw data from Langer (1988).

In the Colobidae, the relative volume of the saccus (plus praesaccus) increases during ontogeny, i.e. the gastric region that is set-off from the shortest connection between the cardiac and pyloric opening. In the adult animal, the saccus gastricus functions as a fermentation vat. The relative volumes of the gastric tube and of the pars pylorica, which both lie in-line between the cardia and the pylorus, are reduced during ontogeny. Because of unavailability of embryological material it cannot be determined how the position of the saccus gastricus changes. BerenbergGossler (1911) gives some information of the positional changes of gastric sections in Semnopithecus entellus. Hill (1954) mentions that as early as in an embryo with 9-mm

14.8.3.5 Gastric blood vessels in Colobinae This section on arterial vessels of the stomach is completely based on the text from Langer (1988), and long passages are cited verbally (pages 295–296): In a young Colobus abyssinicus it was possible to dissect the arterial supply of the whole stomach (Fig. 4.57). Kuhn (1964) indicates many variations between different individuals. After the aorta has crossed the diaphragm, the A.  coeliaca branches off and after a short course is subdivided into three arteries, the A.  hepatica, the A.  lienalis and the A.  sacci gastrici (name coined by Kuhn, 1964). The A.  lienalis approaches the hilus of the spleen, gives off small branches to that organ and proceeds along the larger curvature of the saccus gastricus as A.  gastroepiploica sinistra. In the investigated specimens, it could not be followed on the greater curvature of the gastric tube nor could anastomose with the A. gastroepiploica dextra that approaches from aborally, be found. This is in accordance with the description given by Kuhn (1964). The A. sacci gastrici subdivides into three branches. The first one, the A.  proventriculi, runs cranially in the sulcus between the tubus and the saccus gastricus, passes the oesophagus and then bends to the left on the dorsal extremity of the saccus gastricus. The second branch of the A.  sacci gastrici is the A.  gastrica sinistra. It runs a short length over the right dorsal part of the gastric sac, and then passes over to the lesser curvature of the tubus gastricus, where it anastomoses with the A.  gastrica

Fig. 4.57: Arterial supply of the stomach of a juvenile Colobus guereza. Adapted from Langer (1988).

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dextra, which is the third branch of the A. sacci gastrici. From the A. gastrica dextra, branches to the pancreas can be seen as well as a branch to the greater curvature of both the pars pylorica and the gastric tube. Contrary to findings by Kuhn (1964), a supply of the aboral gastric parts through branches of the A. mesenteria superior could not be verified in the available material. 14.8.3.6 Gastric mesenteries in Colobinae In Fig. 4.58, the whole stomach is stretched out and the line of fixation of the two mesogastria to the stomach is marked. It can be seen that the general situation of the mesogastria is similar to conditions in primates with a unilocular stomach. It has already been mentioned that the two taeniae on saccus and tubus gastricus and the lines of fixation of the mesenteries fall together. The ventral mesogastrium forms the lesser omentum. This is a structure that can best be seen from the right-hand side of the body (Fig. 4.53 a). Around the cardia, the saccus gastricus is fixed to the diaphragm. For the developing human fornix gastricus, Keith and Wood Jones (1902) describe a conical outgrowth, which arises chiefly from the left side of the dorsal mesogastrium and is attached to the diaphragm. This should be comparable with the fornix gastricus of Semnopithecus sp., which represents the sacciform forestomach. From the “pars affixa” or “area affixa” (Fig. 4.49) which is surrounded by the fold where the visceral peritoneal sheet turns over into the parietal sheet and which has been called “ligamentum gastrophrenicum” by Berenberg-Gossler (1911), the lesser omentum starts and forms the hepatogastric ligament. Only for a very short distance it is fixed to the gastric sac where it runs to the right and crosses over to the gastric tube (Fig. 4.58). Because of its sharp bend this part of the

Fig. 4.58: Both mesogastria in Colobus guereza. Adapted from Langer (1988).

stomach forms a clear lesser curvature, which proceeds to the pyloric part and the pylorus itself. The greater omentum as a differentiation of the dorsal mesogastrium is much more complicated. It also starts at the pars affixa of the gastric sac. Its line of fixation to the stomach follows the taenia curvaturae majoris and in species with a praesaccus passes over the praesaccus or between this and the saccus (Fig. 4.49 a, b). It can be followed along the wall of the saccus gastricus and crosses over to the greater curvature of the tubus gastricus which is followed down to the pylorus. Between the pyloric part of the stomach and the colon, a prominent gastrocolic ligament is formed with strong fibre bundles. 14.8.3.7 Muscle architecture of the tunica muscularis Ayer (1948) has already briefly illustrated the three muscular layers of the stomach of Semnopithecus entellus. For comparative reasons (Langer, 1973), the descriptions given by Ayer (1948) have to be extended. 14.8.3.8 Superficial layer The circular layer lies in many regions directly below the serosa of the gastric wall because the longitudinal layer is reduced to two taeniae of the gastric tube and sac (Fig. 4.59). They follow the greater and lesser curvature and end at the border between tubus gastricus and pars pylorica. However, in the pyloric part, a homogeneous external longitudinal muscular layer can be found; this gastric compartment is free of taeniae. In both saccus and tubus gastricus of Procolobus verus and Colobus guereza, the taeniae were rich in connective tissue with little musculature. On the other hand, the taenia curvaturae majoris of another Colobus guereza was found to be wide in the region where the gastrolienal ligament is attached to the stomach. This region of increased width of the taeniae might be identical with the region of a broad band of longitudinal musculature illustrated by Ayer (1948) in the fornix of Semnopithecus entellus. According to these findings, the fornix gastricus was deficient of circular fibres below the broad taenia. In the investigation by Langer (1988), however, there was a deep layer present below the superficial longitudinal musculature. 14.8.3.9 Deep layer This layer is formed by fibrae circulares and the fibrae obliquae. Their distribution is illustrated in Fig. 4.59. It can be seen that the opening of the oesophagus is surrounded by the cardiac loop (Fig. 4.60), formed by the oblique fibres. These fibres form the muscular ridge along



14 Haplorrhini (“dry-nosed” primates) 

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Fig. 4.59: Muscular layers of the gastric wall of Colobus guereza. Fibrae obliquae corporis: irregularly stippled; Fibrae obliquae fornicis: hatched; Fibrae circulares: Waves; Fibrae longitudinales: no signature. Adapted from Langer (1988).

the two lips of the ventricular sulcus. One muscular ridge does not run from the gastric sac to the tube, but onto the wall of the saccus gastricus. The “bottom” of the groove along the lesser curvature of the stomach is formed by circular fibres. These fibres also represent the deep layer of the whole wall of the pyloric part, but are only incompletely differentiated in the saccus gastricus. The corpus gastricum is not only formed by the tubus gastricus, but also by the distal part of the gastric sac. This means that the remaining part of the gastric sac represents the fornix where oblique fibres do not join the lips of

Fig. 4.60: View into the opened saccus gastricus of an adult Procolobus verus after removal of the tunica mucosa. Arrows point into the praesaccus. Adapted from Langer (1988).

the gastric sulcus. When a praesaccus is present, this lies in the region of the fornix gastricus. The pars pylorica is not only characterised by the absence of taeniae, but also by the absence of oblique fibres. The bulk of the muscular material of the small pyloric torus is formed by circular internal fibres. 14.8.3.10 Functional remarks on the stomach of the Colobinae Investigations into form and function of non-ruminant forestomach fermenters were stimulated by the comparative study of Moir (1965). That paper deals with Bradypodida (tree sloths, Pilosa, Folivora), Hippopotamidae and Macopodidae (kangaroos and their kin, Marsupialia); colobids are not mentioned. However, only 3 years later, in a stimulating comparative contribution to the Handbook of Physiology, Moir (1968) deals with colobid monkey. The late R. Moir is a mentor of comparative research in herbivore nutrition and physiology. The complex gastric anatomy of the colobine stomach is connected with fermentation in the stomach, including extensive cellulolysis (Kay et al., 1976), that can be found in these primates (Moir, 1968; Bauchop, 1977, 1978b). It has been suggested by Bauchop and Martucci (1968) that colobine monkeys benefitted from the microbial biosynthetic capacity producing vitamins and nitrogen. Oxnard (1966) found that Trachypithecus obscurus (dusky leaf monkey) and Semnopithecus entellus (northern plains grey langur) have blood serum levels of vitamin B12 that are sevenfold higher than those of non-colobine primates. It has been speculated (Bauchop, 1978a) that urea recycling via the gastric wall, a process of importance in ruminants, also affects the nitrogen and water balance of colobines. It should be mentioned that Ohwaki et al. (1974) contradict those findings that emphasise the importance of microbial fermentation in the colobine stomach. The type of food might contribute to the controversial

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position of these authors. According to Ohwaki et al. (1974), methane is absent from the gastric lumen of the king colobus, Colobus polykomos, as well as cellulolytic bacteria. Very little fibrous material is present, suggesting that “leaf eating” may not apply in Colobus polykomos because luminal acidity may be the factor preventing the development of methanogenic and cellulolytic bacteria (Ohwaki et al., 1974). The extensive studies of Caton (1997, 1998, 1999) also contributed insights into the function of the colobine plurilocular stomach. Caton (1999) speaks of gastro-colic fermentation because both regions of the gastrointestinal tract contribute to digestion as fermentation chambers. The pattern of digesta marker excretion from the tract in colobines has more in common with the pattern of other cercopithecines with a unilocular stomach than with ruminants and macropodids. According to Parra (1978), the body size of colobines is too small to make them able to rely completely on forestomach fermentation. Microbial activity in the stomach of the Colobidae has been demonstrated by many authors (Drawert et al., 1962; Bauchop and Martucci, 1968; Ohwaki et al., 1974; Kay et al., 1976; Bauchop, 1978a). The site of fermentation is the saccus gastricus, where pH 6.5 could be measured by Kay et al. (1976). On the other hand, a highly acid environment can be found in the tubus gastricus, although Kay et al. (1976) do not mention whether they measured in the oral or aboral part of the tube (Fig. 4.55), which have different types of mucosal lining. Microbial fermentation affords time. The enlarged saccus gastricus, for example, in the proboscis monkey, Nasalis larvatus, is responsible for digesta retention, but other selective retention mechanisms could not be found (Dierenfeld et al., 1992). It is interesting that retention time in captive animals was changed when more natural food was not available. For example, Van Nijboer et al. (2007) studied captive specimens of Trachypithecus auratus (Javan lutung); when vegetables were withdrawn, the mean retention time of both fluids and particles increased, but separation of fluids from particles could not be demonstrated. However, the values for formic, acetic, n-propionic, n-butyric, isovaleric and n-valeric acids produced in the stomachs of Procolobus and Presbytis, and determined by Drawert et al. (1962), agreed closely with those for cattle and sheep. Not only energetic aspects play a role in forestomach metabolites, it is certainly important for the mammalian host, that toxic plant materials that are ingested with the food, can be decomposed by the symbiotic microbes. This has been well documented in many studies for ruminants, e.g. by James et al. (1975), Dawson and Allison (1988),

Hofmann (1988), Gregg and Sharpe (1991). Secondary plant compounds like tannins, saponins or alkaloids may be ubiquitous in the food of Colobus angolensis (Angola colobus) (Moreno-Black and Bent, 1982), and its forestomach is said to be able to detoxify secondary compounds before absorption. On the other hand, colobines can select for food that has a lower content of detrimental constituents. In Presbytis johnii (South Indian leaf monkey), the most heavily used food items, found by Oates et al. (1980), are characterised by a low-fibre content and a very low condensed tannin content. However, neither class of those compounds is an absolute feeding deterrent; mature leaves contain considerable amounts of both. It is suggested by Oates et al. (1980) that the feeding deterrents can be tolerated because of their dilution in the gut. Waterman and Kool (1994) present very interesting aspects in relation to toxins in the food: Although no direct evidence of detoxification is available for colobines, leaves containing potentially toxic alkaloids can be eaten, for example, by Colobus satanas, the black colobus. The fermentation process in the forestomach can be reduced by substances that are not primarily toxic, but which are anti-microbial. The bodies of microbes that have contributed to alloenzymatic digestion of plant material, are passed from the fermentation vats (ruminoreticulum in ruminants, saccus gastricus in Colobinae) and have themselves to be digested. Their RNA is degraded by RNAse (Barnard, 1969). In the pancreas of Semnopithecus entellus (northern plains grey langur), Beintema (1990) found 280 μg ribonuclease/g tissue, a value comparable to that found in ruminants and other species with ruminant-like digestion in a plurilocular stomach. In the pancreas of man, a mammalian species without forestomach alloenzymatic digestion, low ribonuclease content (5 μg/g tissue) could be found.

15 to 20 Glires, short overview Morphological and molecular data support a concept of a cohort Glires, consisting of the two orders Rodentia and Lagomorpha (Hoffmann and Smith, 2005). The order Rodentia consists of 481 genera and 2277 species and represents the largest mammalian order (Wilson and Reeder, 2005). The Lagomorpha are not subdivided into different suborders; they eat a food rich in fibre, both sections of the large intestine – caecum and colon – are well differentiated. Five suborders are differentiated in the rodents: 1. Sciuromorpha (squirrels and their kin) with 61 genera and 307 species. No regularity or systematic relationship

15 to 19 Rodentia 



2.

3.

4.

5.

between food and anatomical differentiation can be discerned in this suborder.  Castorimorpha, (beavers and relatives; 13 genera, 102 species), show a tendency of species eating a low quality of food rich in fibrous material. They differentiate haustrations in the colon.  Myomorpha (mouse-like rodents; 326 genera, 1569 species). No regularity or systematic relationship between food and anatomical differentiation can be discerned. The colon does not contribute significant differentiations to the gastrointestinal tract. Anomaluromorpha (scaly tailed squirrels and spring hares; 4 genera, 9 species). For the Anomaluromorpha very little anatomical information is available. Hystricomorpha (porcupines and their kin; 77 genera, 290 species). Species eat very different types of food and have a haustrated or non-haustrated colon.

According to molecular dating, published by Montgelard et al. (2008), the order Rodentia arose during the Late Cretaceous between 71.4 and 89.2 Mya, i.e. before the Cretaceous-Palaeocene boundary. According to Churakov et al. (2010), rodents arose around 70 Mya. BinindaEmonds et al. (2007) position the basal diversification of the order Rodentia at 85.3 ± 3.0 Mya. In the early Eocene (49–54.8 Mya), Rodentia already appeared to be diverse and were present on all continents with the exception of South America. These estimates of Montgelard et al. (2008) are compatible with an early “explosion” of rodent diversity that gave rise to the suborders Hystricomorpha, Anomaluromorpha, Castorimorpha, and Sciuromorpha, as well as the Myomorpha.

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grouped together, i.e. the proportion of different sections of the gut is similar. In none of the species measured by Schieck and Millar (1985), the colon represents more than 40% of the total gut, but in some taxa, especially in the Arvicolinae, the caecum can account for about half of the total weight of the gut. Fig. 4.61 B shows that the caecum in rodents is of great quantitative importance in herbivorous rodents and lagomorphs. In those species that eat plant food, the caecum can account for up to almost 60% of the gut weight and the colon of the Sciuromorpha and Myomorpha never comprises more than 40% of the total gut weight. Herbivores can be found amongst the following rodent suborders: Xerinae, Zapodinae, Arvicolinae and Neotominae (as well as in the Lagomorpha) (Fig. 4.62). In his impressive study on the digestive tract of myomorph rodents, Behmann (1973) presents informative illustrations on three different modes how the ileum opens into the large intestine (Fig. 4.63). These illustrations are of principal importance and can be characterised as follows: A. At the border between the caecum and the colon ascendens – which both lie “in-line” and have similar diameters – the ileum opens perpendicularly into the large intestine.

15 to 19 Rodentia General remarks Within the rodents, the variability of gut forms is considerable. The functional importance of the small intestine, the caecum and the colon can be characterised by consideration of their volume, which, indirectly, can be represented by determining the wet weight of the sections including their contents. These data were measured for rodent species, as well as for Leporidae, belonging to the Order Lagomorpha, in a study published by Schieck and Millar (1985). In Fig. 4.61 A, the relative weights of gastrointestinal sections are compiled in a ternary diagram. With the exception of bank and water voles (Arvicolinae) species belonging to a suborder are closely

Fig. 4.61: Relative weights of small intestine, caecum and colon in different rodent and lagomorph taxa eating different types of food. Original data from Schieck and Millar (1985).

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Fig. 4.62: Three feeding types in rodent species suborders and in lagomorphs, characterized by Schieck and Millar (1985).

B. The opening of the ileum lies close to the site where the colon leaves the caecum. This latter section forms a blindsac with a much wider diameter than that of ileum and colon. C. In the genus Deomys, the ileum and colon lie “in-line” and have a small diameter; the caecum is just a small blindsac at the border between the small and large intestines. When a section of the digestive tract is discussed, the type of food eaten should be considered. Landry (1970)

Fig. 4.63: Different types of opening of the ileum into the caecum and colon. Adapted from Behmann (1973).

discussed the Rodentia as omnivores by considering three of the five rodent suborders, namely, Sciuromorpha, Myomorpha and Hystricomorpha, The author gives a long list of non-herbivorous food in rodents. For example, insectivory is widespread and may have been applied by rodents for a long time. He mentions a great versatility of the basic rodent mandibulo-cranial region, which makes it likely that adaptations to carnivory, grazing, bark-stripping, seed-eating might have arisen more than once. In addition to food, Schieck and Millar (1985) considered weight and length of the caecum in Sciuromorpha and Myomorpha. According to them, the caecum was relatively larger for herbivores than for granivores and omnivores. In the Castorimorpha, we find species that depend on fibrous plant material as food. The European beaver, Castor fiber, eats bark, branches and leaves of soft wood, as well as herbs (Freye, 1978). On the other hand, another castorimorph species, the southern spiny pocket mouse (Heteromys australis) eats leaves, fruits and especially palm seeds, which represent more than 50% of the weight of food residues in the cheek pouches (Sánchez-Giraldo and Díaz-Nieto, 2010). In the Myomorpha, the type of food is very variable. For example, the herbivore Ondatra zibethicus eats meat (of fish and other muskrats). The consumption of animal matter has the potential to play a major role in the nitrogen economy of muskrats (Campbell and MacArthur, 1996a). The authors assume that this food habit might be more widely spread in wild populations than was previously thought. However, in another study, the same authors (Campbell and MacArthur, 1998) found the broadleaf cattail (Typha latifolia) to be the dominant plant eaten as food. Woodall (1989), who studied water voles (Arvicola amphibius) eating high-fibre diets, stated that they had a significantly longer and heavier caecum than captive animals fed a low-fibre diet. When dietary cellulose in food was increased, some added cellulose was digested and the passage of food through the digestive tract was significantly faster on the diet with added cellulose. Studying the caecum of the field vole, Microtus agrestis, Snipes (1979a) stated that morphological findings are correlated with the herbivorous habit of this species. Ellis et al. (1994) studied five myomorph rodents from the pampa in Argentina and concentrated on the digestive tract structure, which was generally in close relationship to the diet of the respective species. He observed a continuum from a diet of seeds and insects (rich in protein) towards a diet rich in cellulose. The total length of the intestine related to body length was high in animals eating a low energy diet rich in cellulose. In addition to other relative parameters, Ellis et al. (1994) was also able to show that the caecum relative to body length was long in animals ingesting high

15 Sciuromorpha 

cellulose quantities, similar observations could also be made when caecal length was related to the length of the total intestine. In the capybara (Hydrochoerus hydrocharis), a hystricomorph species, the caecum as a fermentation chamber is responsible for a digestive efficiency that is comparable to that of ruminants eating a similar diet (Borges et al., 1996; Desbiez et al., 2011). According to Do Valle Borges and Colares (2007), the capybaras in Southeast Brazil showed a preference for aquatic grasses. Capybaras are selective grazers and according to Desbiez et al. (2011) six grass species represented 64% of total capybara diet. Most species consumed were selected and were not the most abundant species in the paddock. Another strictly herbivorous species of the Hystricomorpha is the mara (Dolichotis patagonum), which feeds on grass and herbs. Perennial grasses had the highest relative frequency (46.8%) in their food (Rodríguez and Dacar, 2008). Lessa and Costa (2009) studied a hystricomorph species, Thrichomys aperoides (Common punaré, Woods and Kilpatrick, 2005), or Thrichomys aperoides (Eisenberg and Redford, 1999; Cole, 2000), which eats considerable quantities of arthropods, especially hymenopterans and isopterans. It is an insectivorous rodent in the Campos Cerrados of Brazil that, in addition to insects, also consumes fruits and other plant parts (Lessa and Costa, 2009). Not only in the proximal colon of Cavia porcellus, the guinea pig, but also in its caecum, Takahashi and Sakaguchi (2006) found a bacterial activity higher than in the distal colon and rectum. This is possible because retrograde transport of bacteria towards the caecum takes place via a furrow in the colonic wall, which is the main route for this transport, which leads to an accumulation of bacteria within the caecum. Rodents and members of the order Lagomorpha are the two major groups of small mammals that show caecal fermentation combined with reingestion of faeces (Kenagy and Hoyt, 1980), a process called “coprophagy” (Eden, 1940; Southern, 1940; Frank et al., 1951; Thacker and Brandt, 1955). In a comparative study, Björnhag and Sjöblom (1977) demonstrated coprophagy in myomorphs (Lemmus lemmus, lemming) and hystricomorphs (Chinchilla lanigera, chinchilla and Cavia porcellus, guinea pig), and Herrera (1985) and Hirakawa (2001, 2002) describe this process in the capybara, Hydrochoerus hydrochaeris. Although reingestion of faeces is widespread in the order Rodentia, coprophagy is more strongly developed in the lagomorphs than in rodents (Kenagy and Hoyt, 1980). Coprophagy provides small mammals “with a very flexible form of using this digestive strategy. They have the advantage of microbial symbionts in the caecum to assist with cellulose breakdown,

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and can then return the products of this fermentation process through the stomach and small intestine” (Lee and Houston, 1993, page 431). One of the possible benefits of coprophagy is that it may enable them to extract more energy from their food. The benefits of coprophagy are larger for poor foods with low proportions of cell contents than for richer ones (Alexander, 1993). In addition to the ingestion of normal pellets of hard faeces (coprophagy), guinea pigs (Hystricomorpha) and mice (Myomorpha), as well as in lagomorphs, such as rabbits, eat a special soft faeces (Madsen, 1939; Frank et al., 1951; Ruckebusch and Hörnicke, 1977; Hörnicke and Björnhag, 1980; Hörnicke, 1981; Jilge, 1979, 1982; Gidenne et al., 1994; Bellier et al., 1995; Gidenne and Lapanouse, 1997; DeBlas et al., 1999), which is produced in the proximal colon ascendens and the caecum. This process is called “caecotrophy”, a term that was introduced by Harder (1950a). Bacterial counts in caecotroph are much higher (9.56 × 109) than in faeces (2.7 × 109). When special soft faeces is not available, for example, by applying collars to the experimental animals that make it impossible to reach the anus, guinea pigs and mice can run into health problems. The question arises how soft faeces are produced in the proximal colon ascendens and the caecum. A colonic separation plays an important role. Holtenius and Björnhag (1985) indicate the significance of a furrow in the proximal colon ascendens. They mention that the concentration of nitrogen and viable bacteria in Cavia porcellus was nearly twice as high in the colonic furrow compared to the open colonic lumen. When bacteria were infused experimentally into the proximal colon of guinea pigs they were transported in the furrow towards the caecum. Fluid transport is retrograde, followed by subsequent fluid reabsorption in the caecum.

15 Sciuromorpha 15.1 General remarks A very old ancestor of sciuromorph rodents is Acritoparamys atavus (Carroll, 1988), which is identical with Paramys atavus, as named by Chaline and Mein (1979). This species lived in the upper Palaeocene of North America. Squirrels have a masticatory apparatus that characterise them as “gnawers” (Cox et al., 2012). Although the dental morphology in Sciuromorpha is archaic, they are more evolved than Paramys. In a recent paper, Wu et al. (2012) write that rodents originated around 58 million

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years ago, shortly after the Cretaceous/Palaeocene boundary. According to these authors, the line to Sciuromorpha separated from the other rodents (beavers and mice) approximately 55 million years ago at the Palaeocene/ Eocene boundary. True Sciuromorpha, squirrels, can be identified living at about 25 million years ago, i.e. in the late Oligocene. This is in accordance with data presented by Niethammer and Krapp (1978), Gurnell (1987) and Fabre et al. (2012). The suborder Sciuromorpha consists of three families: Sciuridae and Aplodontidae form the Sciuroidea, and together with their sister group Gliridae (dormice), they form the Sciuromorpha (Huchon et al., 2002). The Aplodontidae with one species, Aplodontia rufa, the mountain beaver (Helgen, 2005c), the Sciuridae or squirrels with 51 genera and 278 species and the Gliridae (dormice and hazel mice) with 9 genera and 28 species (Holden, 2005). In a molecular phyletic analysis of Central American Sciuridae, it was emphasized that the genus Sciurus reaches its highest diversity in the Neotropics with 20 of the total 28 species, which are distributed from Japan and Eurasia to the Americas, especially Meso- and South America (Villalobos and GutierrezEspeleta, 2014). It should already be mentioned here that the determination of gastric length, as it is, for example, presented by Gorgas (1967), presents a certain ambiguity. Has the measurement been made along one of the curvatures or is the length measured from the cardia to the pylorus? The best type of measurement of gastric length, which is used here, is along the facies parietalis or visceralis, intermediate between both curvatures, from the tip of the fornix gastricus to the pylorus. However, in a considerable number of cases, the data given for the length of the stomach and the illustrations given in the same publication do not correlate with each other. This discrepancy can, for example, be found in the fundamental publication of Gorgas (1967). Illustrations will therefore be given without scales.

15.2 Food of the Sciuromorpha To obtain an idea of the type of food the sciuromorphs eat, two tables were compiled for European and Near Eastern sciuromorph species (Tab. 4.6) and for American representatives (Tab. 4.7), listing the food characteristics documented in the literature. Interspecific comparisons demonstrate that there is considerable overlap in resource utilisation, as Ivan and Swihart (2000) were able to show in studies of six species of Sciuromorpha in

Indiana. When information on a certain species is supplied by different authors, there can be differences in the food characteristics. For example, Storch (1978a) calls Dryomys nitedula, the forest dormouse, an omnivore, but Catzeflis (1995b) writes that this species is mainly a vegetarian. Most species are predominantly eaters of plant material, which sometimes also take – when available – relatively small amounts of animal material. In a few species, for example, those of the genus Spermophilus from North America, or species of the genus Eliomys from Europe, prefer animal matter as staple food. In the table, it is documented that reserve organs of plants, such as seeds, nuts or acorns, but also bulbs, fruits and buds are preferred food. Banfield (1981) shows that some sciurids, such as Tamiasciurus sp. (North American squirrels, Chaline and Mein, 1979), eat cones from conifers, very probably a food of limited quality. Another example of low-quality food is eaten by Eupetaurus cinereus, the wooly flying squirrel (Zahler and Khan, 2003), which is an unusual, little-known and rare mammal of the western Himalayas: They feed mostly or entirely on pine needles, which they degrade mechanically with high-croned (hypsodont) dentition, which is unique amongst the sciurids. In such a species, information on the anatomy of the digestive tract, including the stomach, is needed, but, as the authors write, not available. On the other hand, the northern flying squirrel, Glaucomys sabrinus, from North America eats conifer seeds, mushrooms, lichens (Flaherty et al., 2010) and Petaurista philippensis, the giant flying squirrel, consumes fruits (very often figs) and leaves. According to Nandini and Parthasarathy (2008), bark, flowers and lichens play a minor role in this species living in India. A good example for the periodic changes of food composition and – most probably – food quality is given for the edible dormouse Glis glis by Katzmann (2009). Over the course of the summer its staple food changes considerably from juicy fruits in June to nutritious seeds in September that prepare the animal for hibernation. The author speculates that the number of anaerobic bacteria in the digestive tract decreases over the hibernation period. However, an influence of this metabolic resting period on gut bacteria could not be shown. Cork and Kenagy (1989) compared another hibernating species, Spermophilus saturatus, the golden-mantled ground squirrel (Sciuromorpha), with the non-hibernating Peromyscus maniculatus, the North American deermouse (Myomorpha). Illustrations of the digestive tracts of both species show that stomach of Spermophilus saturatus is more voluminous than that of P. maniculatus. It can be speculated that this “reserve volume” contributes to the conservation of bacterial symbionts.

15 Sciuromorpha 

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Tab. 4.6: Food characteristics in different species of European and Near Eastern Sciuromorpha. Species

Food

Reference

Pteromys volans Sciurus vulgaris

Buds of Salix and Alnus, Pinus, young leaves, berries Seeds of conifers, ascorns, nuts, berries, buds, snails, eggs, young birds, galls Opportunists, generalists, granivores, herbivores Nuts, acorns, conifer seeds, tree buds, beetles, fruits, chestnuts Seeds of different trees, acorns, fruits, buds, mushrooms, eggs, young birds Conifer seeds, acorns, chestnuts, nuts, mushrooms, Seeds, fungi, lichens, berries Mainly vegetarian, seeds, fruits, conifer seeds, nuts, acorns, chestnuts, buds, blossoms, eggs Nuts, seeds, acorns, conifer seeds, hips, eggs Nuts, acorns, seeds, berries, mushrooms, buds, animal matter occasionally Acorns, tree buds, sap, chestnuts, seeds of conifers, fruits Seeds, buds, berries, wheat, oat Mainly vegetarian, buds, seeds, fruits, mushrooms, arthropods, small vertebrates Mainly vegetarian, fruits, seeds of trees, buds, wheat, rye, oat Bulbs, green pars of Gramineae, seeds, blossoms, Gryllus, rarely small vertebrates Papilionaceae, grasses, insects, corn Green leaves, flowers, seeds, underground plant parts, arthropods Grasses, corn, green plant parts, small vertebrates, bulbs Plants (herbs and grass), bulbs, seeds Grasses, herbs, roots, green plant parts Exclusively vegetarian, young, fresh plant parts Generalists, reeds, herbs, buds, blossoms, locusts, earthworms, snails, plant juices Omnivorous, mainly animal material, e.g. insects, small birds, molluscs, fruits, seeds, acorns Juicy fruits, berries Omnivorous, seeds, fruits, buds, invertebrates, young or small vertebrates Omnivorous, animal matter dominates, insects, millipedes, small vertebrates, fruits, seeds Omnivorous, insects, millipedes, beetles, fruits, acorns, berries, seeds Mainly vegetarian, seeds, small fruits, buds, arthropods, young birds Seeds of herbs Mainly herbivorous, buds, leaves, acorns, fruits, small birds Berries, acorns, fruits, eggs, insects Mainly vegetarian, fruits, seeds, buds, mushrooms, insects, snails, eggs, young birds Buds, fruits, mushrooms, acorns, nuts, chestnuts Mainly herbivorous, seeds, fruits, acorns, conifer seeds, fruits, insects Corn Mainly vegetarian, buds, leaves, blossoms, fruits, berries, insects, invertebrates Mainly vegetarian, seeds, acorns, fruits, berries, buds, insects Flowers, berries, nuts

Sulkava (1978) Wiltafsky (1984)

Sciurus vulgaris Sciurus vulgaris Sciurus vulgaris Sciurus vulgaris Sciurus vulgaris Sciurus vulgaris Sciurus vulgaris Sciurus anomalus Sciurus carolinensis Tamias sibiricus Tamias sibiricus Tamias sibiricus Spermophilus citellus Spermophilus citellus Spermophilus citellus Spermophilus suslicus Spermophilus xanthoprymnus Marmota marmota Marmota marmota Marmota marmota Eliomys quercinus Eliomys quercinus Eliomys quercinus Eliomys quercinus Dryomys nitedula Dryomys nitedula Myomimus roachi Glis glis Glis glis Glis glis Glis glis Muscardinus avellanarius Muscardinus avellanarius Muscardinus avellanarius Muscardinus avellanarius Muscardinus avellanarius

Gurnell (1987) Wiltafsky (1978) Zwahlen (1995) Münch (2005a) Krystufek and Vohralik (2005) Stefen (2009) Borkenhagen (2011) Krystufek and Vohralik (2005) Wiltafsky and Niethammer (1978) Krapp (1995a) Fernandez (1995) Münch (2005b) Ruzic (1978) Spitzenberger (2001) Krystufek and Vohralik (2005) Niethammer (1978) Krystufek and Vohralik (2005) Krapp (1978b) Müller (1995) Allgöwer (2005d) Storch (1978) Rehage (1984) Catzeflis (1995a) Görner and Stefen (2009a) Storch (1978) Catzeflis (1995b) Storch (1978) Storch (1978) Rehage and Preywisch (1984) Catzeflis (1995c) Görner and Stefen (2009b) Storch (1978) Rehage and Steinborn (1984) Catzeflis (1995d) Görner and Stefen (2009c) Borkenhagen (2011)

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Tab. 4.7: Food characteristics in different species of North American and South African Sciuromorpha. Species

Food

Reference

Aplodontia rufa

Forbs, deciduous plants, ferns, shoots. Leaves, berries, needles, tender twigs Seeds, fruits, nuts, green vegetation, buds Seeds, berries, nuts, acorns, rose hips, grass, seeds Seeds, fruit, fungi, roots, subterranean fungi, seldom insects Nuts, seeds, fruits, insects, bulbs, roots Green leaves of different herbs, grazing, fruits, few insects Forbs, grasses, sedges, clover Green grasses, forbs Roots, leaves, seeds of grasses and forbs Roots, bulbs, stems leaves, flowers of grasses, sedges and forbs Leaves, seeds, fruit, stems, flowers, roots of grasses, forbs and sedges More insectivorous (54%), vegetable matter (44%), fresh green foliage Animal matter forms a third of the diet, green plant parts, seeds, roots Seeds, fungi, leaves, flowers, fruits, roots, herbs, grasses Leaves, stems, roots of grasses, weeds, forbs, insects Buds, maple flowers, seeds, fruits, nuts, acorns, mushrooms Pine phloem, small twigs, needle and pollen cones of pine, fungi Acorns, seeds, nuts, insect galls, bark, sap, fungi Generalist, fruits, berries, grains, seeds, buds, insects, some phloem Buds, flowers, seeds, corn, fruits, berries Conifer cones, nuts, buds, flowers, sap fruits, insects, small vertebrates, mushrooms Pine cones, seeds, nuts, fleshy fruits, mushrooms Nuts, acorns, fleshy fruits, seeds, insects, small birds Lichens, buds, leaves, seeds, fleshy fruits, nuts, insects, birds, eggs, carcass conifer seeds, mushrooms, lichens Mainly vegetarian, stems, leaves, herbs, seeds, insects, Mainly vegetarian, plant lice Mainly vegetarian, flowers, leaves, buds, fruits, berries, nuts, insects Nuts, berries, fruits, roots. Leaves, flowers, buds, bark, lichens, insects Mainly vegetarian, flowers, seeds, leaves, berries, fruits, bark, lichens Mainly insectivorous, vertebrates, millipedes, bee larvae Small seeds, green palnt material, insects Seeds, predominantly insectivorous, plant material, fruits

Banfield (1981)

Tamias striatus Eutamias minimus Eutamias amoenus Eutamias townsendii Marmota monax Marmota flaviventris Marmota caligata Spermophilus richardsonii Spermophilus columbianus Spermophilus parryii Spermophilus tridecemlineatus Spermophilus franklinii Spermophilus lateralis Cynomys ludovicianus Sciurus carolinensis Sciurus aberti Sciurus arizonensis Sciurus niger Sciurus niger Tamiasciurus hudsonicus Tamiasciurus douglasii Glaucomys volans Glaucomys sabrinus Glaucomys sabrinus Xerus inauris Xerus princeps Heliosciurus mutabilis Paraxerus palliatus Paraxerus cepapi Graphiurus ocularis Graphiurus platyops Graphiurus murinus

15.3 Gastric anatomy of the Sciuromorpha Gorgas (1967) wrote a most remarkable and insightful publication on comparative anatomical investigations of the digestive tract of Sciuromorpha and Hystricomorpha, as well as the “Caviomorpha”, which are no longer considered as a separate rodent suborder. The species belonging to this “suborder” are now included in the infraorder

Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Murphy and Linhart (1999) Cudworth and Koprowski (2013) Murphy and Linhart (1999) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Banfield (1981) Flaherty et al. (2010) Skinner and Chimimba (2005) Skinner and Chimimba (2005) Skinner and Chimimba (2005) Skinner and Chimimba (2005) Skinner and Chimimba (2005) Skinner and Chimimba (2005) Skinner and Chimimba (2005) Skinner and Chimimba (2005)

Hystricognathi, which, together with the infraorder Ctenodactylomorphi, form the suborder Hystricomorpha. To this impressive study of Gorgas (1967), detailed reference will be made based on the translation of the original German text by the present author. The stomach of Sciuromorpha is always unilocular, as Gorgas (1967) writes. Its shape depends on the contraction or dilatation state of its tunica muscularis. Often,

15 Sciuromorpha 

the fundus ventriculi forms a blindsac or saccus caecus. The author compiled the gastric forms of 12 species of recent sciuromorpha as well as the stomach of a mummified specimen of Citellus glacialis from the late Pleistocene (Vereshchagin and Baryshnikov, 1982, Fig. 4.64). It can be generalised that the stomach is pouch-like with a lesser curvature that is often characterised by a prominent incisura angularis, as has also been described by Bonfert (1928) for the stomachs of Marmota marmota, the Alpine marmot, and Sciurus vulgaris (Eurasian red squirrel) and Sadeghinezhad et al. (2012) for Sciurus anomalus (Caucasian squirrel). Stanojevič et al. (1982) gives some additional information for the stomach of Spermophilus citellus (European ground squirrel): Both the cardia and pylorus possess very strong sphincters and are located in very close proximity to one another. The greater curvature is connected with the spleen by a gastrosplenic ligament. As in the other Sciuromorpha, the entire stomach is covered internally with a glandular mucous membrane, reddish grey in colour. Gorgas (1967) presents aspects that are of great importance in the consideration of comparative anatomy of the stomach (pages 254 and 255, translation from German by

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the present author): The value of the gastric form in comparative anatomical studies has to be taken into account when questions of systematics are covered. Doubtlessly the gastric form within the class Mammalia is influenced by phylogenetic processes, for example, when the multilocular stomachs of the Cetacea and the Ruminantia are taken into account. In unilocular stomachs (as here in the Sciuridae), functional modifiability can change the basic form individually to a strong degree. The stomach form is determined by the degree of filling. In some individuals, the stomach can be strongly dilated, even when it is completely empty. This shows that consideration of the degree of filling does not allow statements about the specific gastric form. In Fig. 4.64, the gastric form of three species of the genus Spermophilus and a fossil species of Citellus are represented, showing the form of the stomach with intermediate filling. Under consideration of the modifiability of the gastric form all statements on specific characteristics have to be made carefully (Gorgas, 1967). According to that author, the internal lining never shows a cornified squamous epithelium. Murphy and Linhart (1999) compared the internal lining in the stomachs of a feeding specialist, Sciurus aberti (Abert’s squirrel) which eats difficult to digest materials during the winter season, such as pine needles. They also studied a generalist, Sciurus niger (Eastern Fox squirrel). The internal surface area of the stomach of Sciurus aberti amounts to 84.6 cm3 and varies significantly from that of Sciurus niger (54.5 cm3). In the tunica mucosa of the Eurasian red squirrel, endocrine cells have been described by Lee et al. (1991), but these authors do not give any functional interpretations of the distribution of these cells. In contrast to this, Vinogradova (1988) gave an interesting account of the mitotic activity of gastric epithelium in the red cheeked ground squirrel Spermophilus erythrogenys. During summer, the mitotic index was low, as well as in the hypothermal state during hibernation. Before functional epithelial cells were needed, mitosis increased drastically during the arousal state in spring.

15.4 Small intestine of Sciuromorpha

Fig. 4.64: Gastric forms of 13 species of Sciuromorpha. The asterisk shows the stomach from a mummified carcass of Citellus glacialis, found in 1948 by Vinogradov deep in the permafrost of the Indigirka River Basin (Vereshagin and Baryshnikov, 1982). Adapted from Gorgas (1967).

Information on the anatomy of the small intestine of sciuromorphs is very limited. Gorgas (1967) identified villi intestinales in the small intestine of Sciuromorpha. According to Ivanovic et al. (1966), the villi intestinales in the ground squirrel, Citellus sp. (Sciuromorpha) are filiform. Enterocytes are 46 µm high, and goblet cells, Paneth cells and leucocytes can be found in the lamina epithelialis. Paneth cells are also differentiated in the epithelium of the crypts.

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15.5 Colon of Sciuromorpha The information on large intestinal anatomy that is available for this suborder varies considerably in extent and quality, but the course of the colon is depicted in the illustrations that represent the results of studies on the rodent suborder Sciuromorpha by Tullberg (1899), Bonfert (1928) and Gorgas (1976) (Fig. 4.65 to Fig. 4.68). The latter author emphasises the difficulties arising when the specificities of the colon configurations have to be studied in situ. For comparative reasons, he brought the colon into a position which allowed the demonstration of colonic coils. The majority of North American species of the genus Spermophilus have a simple hairpin-shaped “double coil” (“Parellelschlinge” in Gorgas, 1976), whereas the majority of species from Europe and Asia have two double coils. In Fig. 4.65, four of his illustrations for the genus Spermophilus are presented (Gorgas, 1976, speaks of Citellus; according to Thorington and Hoffmann, 2005, this is a synonym of the presently valid species name Spermophilus). Despite the variability between species within this genus, the general form (“Grundform” of Gorgas, 1967) is very similar in different species of Spermophilus. In a study on the alimentary canal of the ground squirrel (Spermophilus citellus), Stanojevič et al. (1982) speak of the genus Citellus and write that the colon is composed of three parts: the ascending colon, the transverse colon and the descending colon. It begins its course as dilatation at the base of the caecum, the “infundibulum coli”, which is 8–10 mm in diameter. The initial part of the colon first extends

Fig. 4.65: The large intestine of Sciuromorpha: Sciuridae and Mormotini. Small intestine: grey; caecum: black; colon: white. Modified after Gorgas (1976).

Fig. 4.66: The large intestine of Sciuromorpha. Small intestine: grey; caecum: black; colon: dark grey; rectum light grey. Modified after Bonfert (1928).

cranially from the caecum as ascending colon, followed by a sharp turn. This turn has to be considered homologous to the flexura coli dextra of human anatomy (Gorgas, 1967). In the ground squirrel, this curve is denoted as flexura prima, from which it runs in caudal direction, where it abruptly forms a second coil, the flexura secunda. Having then followed a craniad course, the colon makes a third curve, the flexura tertia, from where it runs in caudal direction. The “double coil of the descending colon is connected by the mesocolon and lies along the right abdominal wall” (Stanojevič et al., 1982, page 213). In Fig. 4.65, the drawing of the gut of Spermophilus suslicus (speckled ground squirrel), which was also originally published by Gorgas (1976), shows a small second coil (sensu Stanojevič et al., 1982). The present author compiled drawings from other species of Sciuridae, which were either modified from Bonfert (1928) (Fig. 4.66) or Tullberg (1899) and Gorgas (1967) (Fig. 4.67), most of which show two hairpin-shaped “double coils”. However, the illustrations of the large intestine of the red squirrel (Sciurus vulgaris) in both illustrations show the double coil very close to the dilatation at the transition from caecum to colon, the “infundibulum coli”; the colon ascendens is very short. In Myosciurus pumilio, the African pygmy squirrel (Fig. 4.67), only one “double coil” can be seen. In Fig. 4.66, a drawing of the large intestine of a forest deermouse, Dryomys nitedula (Bonfert, 1928), does not show any loops and a clear demarcation between the small and large intestines (probable site indicated by

15 Sciuromorpha 

 191

arrow) is missing because a caecum could not be distinguished. This is an unexpected situation because all other sciuromorph guts (Fig. 4.65 to Fig. 4.68) show a caecum, which is marked in black in the illustrations. In relation to the opening of the ileum into the large intestine relative to the position of the beginning of the colon ascendens or “infundibulum coli”, the illustrations of Sciuromorpha demonstrate that the ileum opens into and the colon branches off from the caecum very close to each other. This is comparable to the second example presented by Behmann (1973) (Fig. 4.63) where the opening of the ileum and caecum lie close to each other. Another family of the suborder Sciuromorpha, the pocket gophers (Geomyidae), has also been depicted, both by Tullberg (1899) and Gorgas (1967) (Fig. 4.68). For Botta’s pocket gopher (Thomomys bottae), Gorgas (1967) shows a widened proximal colon – “infundibulum coli” – as well as two hairpin-shaped double coils. The illustration of the southeastern pocket gopher, Geomys pinetis, which was drawn after Tullberg (1899), only shows a dilation (probably the infundibulum caeci) at the site where the caecum joins the colon. A double coil cannot be distinguished in this drawing. Fig. 4.67: The large intestine of Sciuromorpha: Sciuridae. Small intestine: light grey; caecum: black; colon: dark grey. Adapted from Gorgas (1967) and after Tullberg (1899).

Fig. 4.68: The large intestine of Geomyidae. Small intestine: light grey and stippled (in Thomomys b.); caecum: black; colon: dark grey. Adapted from Tullberg (1899) and Gorgas (1967).

15.6 Caecum of Sciuromorpha The caecum as part of the large intestine is a structure that can store digesta, so that they are set-off from the direct aborad flow (Langer, 1988, 1991). The length of the caecum is related with the quantity of digesta that can be stored in the caecum. The fact that digesta are set off from the oral to aboral flow is very well suited for a time-consuming digestive process, especially for microbial degradation of plant cell-wall material. In many rodent species, it is the caecum, which represents an important section of the digestive tract. When stomach, small intestine, caecum and colon are considered in Microtus pennsylvanicus (meadow vole), the caecum contains the relatively heaviest weight of digesta in the tract. This is especially so when a secondary plant cell compound, such as tannin, is present in the digesta (Fig. 4.69) (Breton et al., 1989). In their study on Southern African myomorph rodents, Perrin and Curtis (1980) published data on the length of the small intestine, caecum and colon of 19 species, as well as information on the type of food; they speak of “feeding category”. These data were compiled in three ternary diagrams for granivores/insectivores, omnivores and herbivores (Fig. 4.70). In granivores/insectivores and in omnivores (both groups cannot be clearly separated from each other), the length of the caecum plays only a minor role, but in the herbivores about 25% of the

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Fig. 4.69: Masses of digesta relative to body mass (g/g BM) in compartments of the tract of Microtus pennsylvanicus that were fed rabbit chow (control, hatched) or chow containing 0.3% tannin (dark signature). Raw data are from Brenton et al. (1989).

digestive tract length is represented by the caecum. The functional importance of the caecum is shown in Microtus sp., eating grass, sedges, seeds and bark, when the internal surfaces of the above-mentioned three sections of the digestive tract are considered (Fig. 4.71) (Barry, 1977), more than 10% of the surface is supplied by the mucosa of the caecum. Of the 307 species of the Sciuromorpha (Wilson and Reeder, 2005), only one belongs to the family Aplodontiidae with one species, the mountain “beaver” or sewellel (Helgen, 2005c). Twenty-eight (9%) of the Sciuridae are represented by the Gliridae (dormice), but 278 species (91%) belong to the Sciuridae, Squirrels. Because of their high species number and because some species live close to humans, the Sciuridae represent a well-studied group (for example, Gurnell, 1987). According to this author, the primary food of squirrels consists of tree seeds and fruits. According to Schieck and Millar (1985), the Sciurinae are granivorous, the Xerinae partly granivorous, as well as herbivorous (Fig. 4.62). Foods of less importance include berries, fungal fruiting bodies and also mycorrhizal fungi,

as well as buds, growing shoots flowers, bark and lichens and occasionally even animal food, such as invertebrates, bird’s eggs; sometimes even carrion is taken (Gurnell, 1987). In relation to plant material, this author writes that “squirrels select food with low tannin content and that this preference may be influenced” by the unpleasant taste of tannin (page 40). A triangular diagram depicting the relative weights of the small intestine, caecum and colon (Schieck and Millar, 1985, Fig. 4.72) in seven species of the family Sciuridae (Sciuromorpha) gives some interesting information on the relationship between digestive tract morphology and food. In relation to the weight of the colon, no differentiation between herbivorous and graminivorous species can be found, but in contrast to the granivorous species, there is a tendency to increased caecum weight in the herbivorous animals, which, most probably, eat a food with more cell wall material (fibre) than the granivorous animals. A schematic illustration of the caecum of Sciuromorpha in general, based on Gorgas (1967), has already been given above (Tab. 4.1). Another figure of the caeca of two

Fig. 4.70: Relative length of small intestine, caecum and colon in 19 myomorph rodent species eating different types of food. Adapted from Perrin and Curtis (1980).

15 Sciuromorpha 

Fig. 4.71: Relative surface areas of small intestine, caecum and colon and types of food in Myomorpha. Raw data are from Barry (1977).

Fig. 4.72: Relative weights of small intestine, caecum and colon in herbivorous and granivorous Sciuromorpha. Adapted from Schieck and Millar (1985).

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species of Spermophilus (Fig. 4.73), as documented by Stanojevič et al. (1982) and Cork and Kenagy (1989), presents a simple, bag-like caecal shape and the incoming ileum and outgoing colon ascendens lie closely together. Although the study of Behmann (1973) did not deal with sciuromorph species, his illustration of different types of caeca and of the relationship between the ileum and the colon ascendens presents a situation that can also be found in Spermophilus: Both sections of the gut enter and leave the caecum in direct neighbourhood (Fig. 4.63 B). Gorgas (1976) supplied the illustrations of the arterial supply of the digestive tract. Figs. 4.65 and 4.67 show that the caecum of Sciuridae is supplied by the A. ileocolica, a branch of the A.  mesenterica superior (cranialis). The same supply by the A. ileocolica is shown for a representative of the sciuromorph family Geomyidae, Thomomys bottae, in Fig. 4.68 (lower panel). Stanojevič et al. (1982) mention that a view into the opened caecum shows transverse mucosal folds. Murphy and Linhart (1999) outlined shapes of digestive tracts, including the caecum, for Sciurus aberti and S.  niger. In their text, these authors give the information that Sciuridae are not caecotrophic and do not show the colonic separation mechanism. Gorgas (1976) supplies drawings of the caecal form in Marmotini, which is generally bag-like and shows a very close proximity of the ileal opening into and the colonic exit from the caecum. The same author also depicts caeca of Sciuridae, which are more lengthened and look more cylindrical and tube-like (“Caecum angustius”, Kostanecki, 1926; Jacobshagen, 1937) than those caecal shapes mentioned above. From these findings it has to be concluded that the caecum shows different forms within the Sciuromorpha; from bag-like to lengthened and narrow tubes.

Fig. 4.73: Outlines of the caeca of two species of Spermophilus (Sciuromorpha: Sciuridae). Adapted from Cork and Kanagy (1989), and Stanojevic et al. (1982).

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According to Baecker (1938), the caecum of Alpine marmots (Marmota marmota) is very voluminous and can be called a “caecum amplius”, a wide caecum (Kostanecki, 1926; Jacobshagen, 1937). The marmot caecum has an inner relief consisting of longitudinal and circular folds. In the corpus and the apical region of the caecum, they form a regular meshwork. These folds are formed by a thickened tela submucosa, but in the circular folds circular musculature (stratum circulare) can be distinguished, together with an artery and a vein, both ensheathed into an elastic environment (Baecker, 1938). In their studies, Hume et al. (2002) of Alpine marmots (Marmota marmota) between first emergence from the winter den and midsummer (July), the fresh tissue mass of the caecum increased by 185%, although microbial activity in the caecum was already significant at emergence. The length and fresh mass of the caecum increased in response to ingested food. For the second important family of the Sciuromorpha, the Gliridae, Bonfert (1928) gives a very interesting detail: The author mentions for Dryomys nitedula, the forest dormouse, that a caecum is missing (bottom of Fig. 4.66). It is impossible to give commentaries on this remarkable statement. This absence of a caecum is surprising because D. nitedula can be called an omnivore (Storch, 1978a), with plant material representing the main staple: seeds, small fruits, buds, lichens, leaves, but also considerable quantities of arthropods, eggs, young birds (Görner and Hackethal, 1988; Macdonald and Barrett, 1993; Lange, 1994; Catzeflis, 1995b). Plant food would make the caecum a valuable organ where microbial fermentation could take place.

16 Castorimorpha 16.1 Introductory remarks Detailed information on the Castorimorpha has been made available recently by Helgen (2005b), Patton (2005a, b), Hafner et al. (2007) and Wu et al. (2012). This suborder has three families: the first one is represented by the Castoridae, beavers, with only one genus and two species (Helgen, 2005b). The second family is represented by the Heteromyidae with six genera and 60 species (Patton, 2005a), differentiated into three subfamilies (Hafner et al., 2007), the Dipodomyinae or kangaroo rats and the sister clades Heteromyinae or spiny pocket mice, as well as the Perognathinae or pocket mice. The third castorimorph family is represented by the Geomyidae or pocket gophers, including 6 genera and 40 species (Patton, 2005b). Geomyidae are confined to the New World and spend much of their time underground in a permanent tunnel system (Eisenberg, 1989). Heteromyidae from North, Central

and South America, on the other hand, show adaptations for arid environments, but some species have adapted to moister habitats and have a long association with grasslands (O’Connell, 1982). The families Heteromyidae and Geomyidae separated from each other about 20.5 million years ago, but the base of the Castorimorpha lies approximately 45.5 million years ago (Wu et al., 2012). A fossil species with relationships to heteromyids and geomyids, Eomys querci, from the late Oligocene of Germany, is the oldest rodent with the capacity of gliding capacity (Storch et al., 1996). This type of locomotion can also be found in some recent species of the Sciuromorpha and Anomaluromorpha. The American beaver (Castor canadensis) was also almost completely extirpated in North America because of human exploitation (Hadidian, 2003). However, after 25 pairs of this species were introduced to Tierra del Fuego Island (Chile and Argentina) in 1946, their population has drastically expanded during just half a century over the complete archipelago and “engineers” the area because of its tree-felling and dam-building activities (Anderson et al., 2009). According to Malmierca et al. (2011), North American beavers threaten ecosystems in southern Patagonia and cause significant impacts on biodiversity. From the island of Tierra del Fuego, they have expanded their range to the South American mainland and still progress north (Graells et al., 2015). In Eurasian countries, the beaver (Castor fiber) also has a long history of quantitative breakdown (Halley and Rosell, 2003). Only remnants could be found in Belarus, France, Germany, Mongolia, China, Norway, Russia and Ukraine and in Denmark. Recently, a phase of population growth after reintroductions can be observed in Europe (Hartman, 2003). The Eurasian beaver shows remarkable ability to adapt to periods of drastically changing water levels (Kurstjens and Bekhuis, 2003).

16.2 Food of the Castorimorpha Castor fiber, the European beaver, is a strict plant-eater (Freye, 1978; Allgöwer, 2005a). In Denmark, animals foraged on woody plants in the winter from November to May and on non-woody plant material from June to September (Elmeros et al., 2003). Jones et al. (2003), who investigated beavers in a Scottish enclosure, mention that trees of three genera were felled: Alnus sp., Betula sp. and Salix sp. This material was partly used for building purposes, but also as food. Willow (Salix) species are highly preferred by European beavers and were actively selected for (Elmeros et al., 2003; Jones et al., 2003). Also in the American beaver (Castor canadensis), willow “is important as food and construction material” (Baker, 2003); “Willow leaves are high in protein content and are readily eaten during the

16 Castorimorpha 

summer. The bark of willow stems stored in a food cache accessible from under the ice may be the only source of winter food for beaver that live in climates where surface water freezes during winter; thus, the availability of suitable willow stems can limit beaver populations in cold climates” (Baker, 2003, page 174). In relation to the European beaver, Allgöwer (2005a) speaks of an opportunistic nutritional behaviour, i.e. it uses those plants that are available in the greatest quantities; in the main vegetation period, it can even concentrate on grass and herbs that grow on the edges of open water. However, in winter, the beaver feeds on woody vegetation almost exclusively (Chaney, 2003). Banfield (1981) mentions for Castor canadensis that the cambium layer of branches, leaves, twigs, buds, as well as much herbaceous vegetation, including submerged root stalks, are also taken. To make use of the products of microbial symbionts beavers reingest parts of the faeces (Allgöwer, 2005a). A special material, caecotrophes, which looks different from normal faeces, which is moist and rich in mucous is taken directly from the anus in the morning hours (Richard, 1959). According to their investigations in rabbits, Leiber et al. (2008) state that fatty acid profiles in the caecum indicate that caecotrophs contain products of anaerobic microbial metabolism. It is plausible that the situation in both beaver species is similar. In relation to the type of food, it should be kept in mind that the material eaten by beavers is not characteristic for all Castorimorpha. Sánchez-Giraldo and Díaz (2010) found for the southern spiny pocket mouse (Heteromys australis) from the north of South America that it eats leaves, fruits and especially seeds. About 52% of food remains in cheek pouches of this species were from palm seeds. This is certainly a material of considerably higher quality then the winter food of Castor sp. Haarberg and Rosell (2006) studied foraging of European beavers on woody plant species. They call Castor fiber “central-place foragers” because the animals bring their food to their refuge. This term had already been used by Belovsky (1984b) and Fryxell and Doucet (1991). According to Baker and Hill (2003), woody plant parts constituted 53% of the annual diet (86% in winter and 16% in summer). Even in newly colonised areas, woody plant forages play an important role with periodical changes (Elmeros et al., 2003; Madsen et al., 2007). Deciduous plants represent the most important component of the beaver diet, but conifers are also cut and eaten for building material and food. Studies on the North American beaver, published by Hoover and Clarke (1972), indicate that the caecum and upper colon are the sites of fibre digestion and of VFA production and absorption. The observed cellulose digestion coefficient of 30% in the beaver is lower than the values reported for deer, 40.7%.

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16.3 Gastric anatomy of the genus Castor The stomach of the beaver is divided by a muscular contraction into two portions, which Home (1807a) calls the cardiac and the pyloric one (Fig. 4.74, upper panel, and Fig. 4.75, upper panel). The cuticular lining of the oesophagus terminates at the orifice of the stomach. The length of the stomach (20 cm) of the European beaver has already been given by Tullberg (1899), and was corroborated by Vispo and Hume (1995) for Castor canadensis. The latter authors determined the mass of gastric wet contents, which amounted to 258 g, equivalent to 23% of the total post-oesophageal gastrointestinal tract. Upon the lesser curvature Home (1807a) describes a large oval glandular structure, which is subdivided into different ridges that project into the gastric lumen. This structure has been depicted by Nasset (1953) (Fig. 4.76). It contains secreting tubules, which are lined with parietal cells. This gland reminds of the cardiac gland that was described for Sirenians (Fig. 2.26). Nuhn (1870)

Fig. 4.74: Three outlines of the beaver (Castor) stomach by different authors.

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Fig. 4.76: Three aspects of the cardiac gland in the stomach of Castor canadensis (white dots in a and b). (c) Opened stomach with glandular apertures. Adapted from Nasset (1953).

Fig. 4.75: Gastric forms of four species of Castorimorpha. Adapted from: Tullberg (1899) (A, B, D); C, Gorgas (1967) (C).

16.4 A few remarks on the castorimorph families Geomyidae and Heteromyidae

published an illustration of the cardiac gland in Castor sp. (Fig. 4.74, middle panel). According to this illustration, the gland lies around the distal oesophagus, which is incorrect, as has been shown by Nasset (1953) (Fig. 4.76) and Gorgas (1967). “On the right of the oesophagus, at the lesser curvature of the stomach” of the beaver (Owen, 1868, page 422) “is a gastric gland composed of numerous branched follicles…On the right of these orifices commences the pyloric portion….” In his lecture on comparative anatomy of mammals, Flower (1872) mentions for Castor fiber the remarkably large glandular mass situated on its lesser curvature to the right of the cardiac orifice. Oppel (1896) characterises this structure as an evagination of the glandular mucosa close to the cardia, which contributes to the magnification of the glandular mucosal lining. He also mentions that the total internal gastric surface is lined with glandular mucosa. A schematic illustration has been given by Pernkopf (1937) (Fig. 4.74, lower panel). Digestion of the woody material eaten by beavers is enhanced by caecotrophy, which is a regular process in beavers (Richard, 1959; Buech, 1984). It starts at about sunrise and then lasts for two to three hours. In winter, the time of caecotrophy is subdivided into many small periods extended over the day.

In contrast to the Castoridae much less is known of the digestive tracts of Geomyidae and Heteromyidae. Eisenberg (1989) remarks that Geomyidae gather grasses, seeds, forbs; they are adapted to feeding on the roots of grasses and tubers; about 45% of their food consists of grasses, as Luce et al. (1980) write. Thomomys talpoides, the northern pocket gopher, is a fossiorial rodent that hoards plant parts in the snow or in underground tunnels (Stuebe and Andersen, 1985). From these stored materials, this geomyid species is able to survive adverse seasonal conditions. Heteromyidae, on the other hand, seem to rely on a food of slightly better quality. Heteromys anomalus, the Caribbean spiny pocket mouse, includes some fruit and insects in its food. For example, the food of Heteromys australis (southern spiny pocket mouse) from the Cordillera Central of Columbia consists of 51.51% of palm seeds, grasses are practically not included in the food (SánchezGiraldo and Diaz-Nieto, 2010). Reichman and Price (1993) write that evolutionary differentiation made heteromyids seed specialists and that other resources, such as insects and green vegetation, are more ephemeral. Seeds represent the mainstay of the heteromyid diet. Their teeth and jaw structure, as well as external cheek pouches, are all suited to this type of food (Reichman and Price, 1993). Any

16 Castorimorpha 

influence of the food on gastric anatomy is not mentioned in that publication. Plant seeds constitute a diverse and quantitatively important dietary resource for rodents. In heteromyid rodents, dietary seed components dominate food composition. As a species belonging to the heteromyid subfamily Dipodomyinae, Merriam’s kangaroo rats (Dipodomys merriami) from New Mexico consume grass seeds to a large extent (Hope and Parmenter, 2007). Generally, it can be said that the cardia and pylorus lie close to each other in all Castorimorpha, especially in the Geomyidae and Heteromyidae (Fig. 4.75).

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16.5 Small intestine of Castorimorpha Very little information on the small intestine of Castorimorpha is available. Only arterial supply has been dealt with in some detail by Bisaillon and Larivière (1976). The small intestine receives some blood via the A.  coeliaca, but the majority of the small intestine is supplied via the A.  mesenterica cranialis (Fig. 4.77, upper panel). In Castor canadensis, an anastomosis between A.  coeliaca and A. mesenterica cranialis could be found: The A. pancreaticoduodenalis cranialis forms an anastomosis with

Fig. 4.77: Schematic representation of the arteries of the digestive tract in three rodent species. Anastomoses are represented by connecting lines.

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a cranial branch of the A.  mesenterica cranialis via the A. pancreaticoduodenalis caudalis.

16.6 Colon of Castorimorpha Two papers, by Tullberg (1899) and Bisaillon and Larivière (1976), publish illustrations on the large intestine of the Canadian beaver, Castor canadensis, which – in a modified form – can be found in Fig. 4.78. The drawing published by Tullberg (1899) shows clearly that the colon, with the exception of the terminal part and rectum, has taeniae. These contribute to the formation of haustra and semilunar folds. This differentiation of the colonic wall is an adaptation to effective regulation of digesta transit, which is useful when a food of low in quality and rich in fibrous material is eaten (Langer and Takács, 2004). Two hairpin-like double coils can be found in the illustrations modified from both papers. They lie in the central part of the colon, i.e. in the colon transversum.

16.7 Caecum of Castorimorpha Castor canadensis was studied by Hoover and Clarke (1972) and they determined that the beaver caecum and

Fig. 4.78: The large intestine (caecum dark) of Castor canadensis.

Fig. 4.79: The caecum (dark) of Castor fiber.

its upper colon together form the site of fibre digestion and of production and absorption of volatile fatty acids. Total VFA levels were highest in the caecum and upper colon, averaging 0.498 and 0.419 mEq/g DM, respectively, whereas the total VFA level in the lower colon averaged 0.222 mEq/g DM. The digestion of cellulose by Castor canadensis amounts to 32 to 33% (Currier et al., 1960). The general shape of the fermentation chamber where fibre digestion takes place has been depicted by Tullberg (1899) for the American (Fig. 4.78) and by Gorgas (1967) for the European beaver (Fig. 4.79). In the illustrations by Tullberg (1899) and Gorgas (1967), it can be clearly seen that the proximal part of the organ close to the opening of the ileum is wide and voluminous, but towards the apex it becomes narrow. In this case, Jacobshagen (1937) speaks of a “colon angustius distale”. It should also be mentioned that the proximal parts of the caecum and colon ascendens (ampulla coli, Ac in Figures 4.78 and 4.79 of both beaver species are relatively wide structures. In the arterial vascularisation of the caecum of Castor canadensis (Fig. 4.80) the A.  caecalis sinistra arises from the A.  mesenterica cranialis. It follows the whole left side of the voluminous corpus caeci, but does not reach its apex. The A. caecalis dextra, on the other hand, is the last branch of the A.  mesenterica cranialis before this proceeds as A.  ileocolica. It follows the right side of the corpus caeci and reaches its apex. Both caecal arteries give off branches to the caecal wall. Seven to 10 Rr. caecales branch from the A.  ileocolica along its whole course. The last ones are the A.  colica ventralis dextra and sinistra, which are not marked in this illustration.

17 Myomorpha 

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Fig. 4.80: Arterial supply of the ileo-caecal region in Castor canadensis. Modified after Bisaillon and Larivière (1976).

17 Myomorpha 17.1 General remarks Today 40% of all mammalian species are rodents (Churakov et al., 2010). Beck et al. (2006) acknowledge 113 extant families of placental mammals, but Wilson and Reeder (2005) even list 130 eutherian families and identified 2277 rodent species, grouped in 33 families. Of these, 1569 species in 326 genera belong to the suborder Myomorpha, which comprise about 69% of the total number of rodent species (Wilson and Reeder, 2005). These are subdivided into two superfamilies, the Dipodoidea and the Muroidea. The taxonomy, as well as the phylogeny of the Dipodoidea remains controversial, as Lebedev et al. (2012) remark. Muroid rodents represent the most diverse group of rodents (Catzeflis et al., 1992), according to Wilson and Reeder (2005), there are 1518 muroid species in 310 genera, and the family Muridae is the most diverse one of living mammals, as Jansa and Weksler (2004) write. The subfamilies of muroids are organised into five major lineages (Michaux et al., 2001): One unites the Spalacinae and Rhizomyinae and contains 23 species; the second one includes African taxa with 43 species; the third one comprises only the six species of the genus Calomyscus. The following two clades literally “exploded” into a wide variety of species and dispersed all over the world. For example, in the above-mentioned fourth clade, the subfamily Arvicolinae is one of the most diverse rodent taxa, which inhabit tundra, forest and steppe biomes of the northern hemisphere in great populations and large areas (Shenbrot and Karasov, 2005). The Arvicolinae are extremely abundant and exceptionally fertile, a very successful group in evolution (Chaline and Main, 1979).

Within the suborder Myomorpha, the family Dipodidae are the first to be distinguishable, next are the Spalacidae. The Muridae and Cricetidae – the latter probably with an Asian origin (Gomez Rodrigues et al., 2009) – separate later from each other. This sequence of separation of myomorph families can also be found in publications of other authors: Carroll (1988), Huchon et al. (2002), Jansa and Weksler (2004), Veniaminova et al. (2007), Montgelard et al. (2008) and Blanga-Kanfi et al. (2009). Mice and rats, forming the subfamily Murinae, are an expansive group: According to Lecompte et al. (2008), the first colonisation of Africa by Murinae occurred around 11 Mya and the native rats and mice of Australia came to that remote continent about 4 million years ago (Breed and Ford, 2007).

17.2 Food of the Myomorpha The Myomorpha, which are widely distributed in the world, eat a considerable diversity of food, so that the characterisation of Landry (1970) of the order Rodentia as omnivores can also be applied in the suborder Myomorpha. To obtain an impression of the food of myomorphs, information was compiled from Boitani et al. (1983), Grzimek (1988), Sheng et al. (1999), Kryštufek and Vohralik (2005). In Fig. 4.81 (right section of the graph), black fields indicate presence of respective material in food. Fields with a white “X” indicate reduced importance of a food constituent (i.e. “not so important”). Very widely eaten are seeds, tubers, leaves and stems, as well as arthropods, i.e. insects and/or spiders. Kingdon (1974b) gives information on the types of food eaten by different representatives of the murid family Nesomyidae and his data give the impression that these rodents tend to eat a food of good quality. For example,

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Fig. 4.81: Phylogenetic tree (left), gastric outlines and mucosal lining in stomachs of Myomorpha (centre), as well as a table of food constituents (right). The tree is adapted from Jansa and Weksler (2004); gastric outlines are from Maddock and Perrin (1981) (A); Naumova (1981) (B); Perrin and Curtis (1980) (C); Tullberg (1899) (D) and Vorontsov (1967) (E). Food characteristics are from Boitani et al. (1983), Grzimek (1988), Sheng et al. (1999) and Kryštufek and Vohralik (2005). Black fields indicate use of the respective food material; an additional “X” means that the type of food is less important.

Dendromus melanotis (grey African climbing mouse) eats a mixture of starchy and fatty seeds, but also insects and small vertebrates. D. mesomelas (Brant’s African climbing mouse) feeds on grass seeds and insects. On the other hand, Cricetomys gambianus (northern giant pouched rat) feeds on beans, roots, bulbs and nuts; this species applies coprophagy. Saccostomus campestris (Southern African pouched mouse) lives on dry seeds, berries and occasionally insects, especially termites. In the myomorph family Cricetidae, subfamily Arvicolinae, species eat different types of food (Batzli and Cole,

1979): The prairie vole (Microtus ochrogaster) eats primarily forbs, i.e. soft herbs, but the California vole (M. californicus) and the Siberian brown lemming (Lemmus sibiricus) eat primarily grasses and sedges. Baker (1971) observed that grass-eaters are more selective feeders than seedeaters; they do not eat randomly any grass available. In contrast, seed-eaters may also include seeds, fruits, fungi, and invertebrates in their food, all of which are seasonal, but represent a food of higher quality than material eaten by grass-eaters. In meadow voles (Microtus pennsylvanicus), food choice can be related to the presence or absence

17 Myomorpha 

of alkaloids or tannins (Belanger and Bergeron, 1987), but a clear pattern of association between the presence or absence of alkaloids and tannins and vole food preferences could not be detected. Meadow voles appear to optimise their diets on the basis of protein and secondary antiherbivore compounds simultaneously, as Bergeron and Jodoin (1987) write. Another cricetid species, a member of the subfamily Neotominae, the southern grasshopper mouse, Onychomys torridus, eats almost entirely animal matter with arthropods forming the major component (Horner, 1962, Horner et al., 1965). According to Giannoni et al. (2005), sigmodontine rodents (Cricetidae) from Argentina can either be herbivorous, or omnivorous, or can show a strong tendency towards insectivory. Pearson (1988) describes for Reithrodon, another Argentinian genus, that 90% of the food consists of grasses. This animal consumed almost exactly its own weight in fresh grass each day. Forty-three present of this food was digested. Comparing arvicoline rodents (Cricetidae) with murine species (Muridae) Butet and Delettre (2011) came to a generalising conclusion: Most arvicolines eat mainly green matter of the herbaceous layers of open habitats whereas most murines are able to use a greater diversity of high energetic plant tissues from denser habitats. However, not only in the Cricetidae, but also in the Muridae, considerable variability of food eaten can be observed. For example, diet of four species of Gerbellinae (gerbils) from Israel was studied by Bar et al. (1984). Seeds were the prominent food, plant parts were second and the proportion of insects in the diet was small. The diets consumed by Moravian populations of the yellownecked field mouse, Apodemus flavicollis, seasonally differed by the number of food items consumed; vegetative parts of plants can be of great trophic importance (Holišova and Obrtel, 1980). On the other hand, various invertebrates (above all, insects) could also be the most important component of the diet. Invertebrate food was also eaten by introduced Mus musculus on subantarctic Maquarie Island (Copson, 1986). In addition to invertebrates, the diet of the mouse also consists of seeds and plant material and occasional vertebrate flesh. The roof or ship rat, Rattus rattus, introduced to the same island, eats mainly plant material which is supplemented by invertebrates and vertebrates. Most of the Muridae investigated by Genest-Villard (1980) in Central Africa, seem to be more or less insectivorous. One species, Prionomys batesi (Dollman’s African tree mouse, Family Nesomyidae) is strictly insectivorous, eating only ants. There are also species that are herbivorous, others are almost completely frugivorous. Under differentiation into herbivores, omnivores, granivores, and insectivores digestibi-

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lity can vary widely, as Batzli and Cole (1979) remarked. The above-mentioned and haphazardly selected examples show clearly that it is difficult to attribute well-defined food types to the Myomorpha, but the types of food taken by them is of surprising diversity.

17.3 Gastric anatomy in the Myomorpha 17.3.1 Terminological remarks The diversity of gastric forms in the Myomorpha is considerable and makes a clearly defined nomenclature necessary. In the lower part of Fig. 4.81, it can be seen that the stomach of the myomorph family Dipodidae is completely lined internally with a glandular mucosa. This situation can often be observed in eutherian stomachs, for example, in carnivores or humans. However, a myomorph stomach can also be “composite” (Langer, 1985), which means that part of the organ – starting close to the cardia and extending from there into fornix and corpus, in some cases, even into the pars pylorica – is lined with stratified squamous epithelium (Schaller, 1992), which is free of mucosal gastric glands, representing the “nonglandular” (Langer, 1985) condition. Fig. 4.82 presents different types of cricetine composite stomachs, originally published by Carleton (1973). This graph depicts the possible distributions of non-glandular (black) and glandular mucosa. Listing of species or genus names is not considered to be helpful here. In some cases, a great number of genera is represented in one gastric representation, e.g. in the hemiglandular gastric type with, at least, 24 genera. The overview shows that the extension of the two types of mucosa can be very different. When glandular and non-glandular parts are of approximately identical size, the organ is a “hemiglandular” one, when glandular mucosa is reduced in size, but still relatively extensive, the newly coined term “sub-hemiglandular” is recommended. The pars glandularis can be reduced to small areas (“discoglandular”, Langer, 1985) or can be reduced to a small pouch or blindsac (“diverticular”). By folds or constrictions, the stomach can be subdivided into two or more compartments. In the lower section of Fig. 4.82, two “chambers” can be discerned in three examples that are lined differently by glandular and nonglandular mucosa. Discussing structure, diversity and nomenclature of the mammalian stomach, Langer (1985) writes: “The gastric lumen can be unilocular (undivided) or plurilocular (divided) with two, three, or more chambers (bilocular, trilocular). According to Henderson et al. (1963), a loculus is a small chamber or cavity. The term “locular” has already been used by Pernkopf and Lehner

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 IV Euarchontoglires – 17 Myomorpha connection between inflow and outflow. In their overview of different shapes in sections of the digestive tract, Godon et al. (2013) identify a digestion chamber of this type a “batch reactor”.

17.3.2 General remarks on gastric form, mucosal lining and taxonomic relationships in the Myomorpha

Fig. 4.82: Form and mucosal lining in stomach of different species of Cricetinae. Black: squamous epithelium, light coloured: glandular mucosa. Adapted from Carleton (1973).

(1937), Dorst (1972) and Carleton (1973)” (page 101). Nickel et al. (1973) calls the unilocular stomach “simple”, a term which might be confused with the exclusive lining of the organ by glandular mucosa. On the other hand, “plurilocular” can be considered synonymous with “complex” (Vorontsov, 1967/1979, Langer, 1985). A third – more functional – aspect in the consideration of gastric diversity of the myomorph stomach also has to be kept in mind. It has been discussed in some detail by Langer (1988): Gastric sections can be positioned in-line in the oral-aboral direction of digesta net flow. On the other hand, it is possible that a sort of blindsac is formed, that forces digesta to make a “detour“. Sometimes ingested material can even be retained in these set-off gastric regions. Keeping these latter aspects in mind, an additional definition of bilocularity has to be given: Even when a prominent set-off volume of a stomach is differentiated, for example, when the fornix gastricus becomes long and extended, this organ will be called a bilocular stomach. As has already been indicated above, food passing through this set-off section makes a “detour” from the shortest

Comparison of the stomachs of Myomorpha affords a wider radius than just consideration of the Cricetidae. In Fig. 4.81, the range of six families of Myomorpha is taken into account, based on anatomical information from five publications: Maddock and Perrin (1981), Naumova (1981), Perrin and Curtis (1980), Tullberg (1899), Vorontsov (1967/1979). Non-glandular mucosa is marked black, the other regions are glandular (not further differentiated). This tree of gastric forms of Myomorpha is “clipped” from Jansa and Weksler (2004), but it is derived from a strict consensus tree that follows parsimony analysis, as determined by gene sequences of interphotoreceptor retinoid binding protein (IRBP). The sequence of phylogenetic appearance of families is as follows: Dipodidae are the first to appear (~64 Mya according to Montgelard et al., 2008). Next are the Spalacidae (~53 Mya) and the Muridae and Cricetidae separate considerably later from each other (~34 Mya). Similar sequences of separation can also be found in Huchon et al. (2002), Veniaminova et al. (2007) and Blanga-Kanfi et al. (2009). As has already been mentioned, Dipodidae are the most basic myomorph family. They are characterised by a glandular stomach, completely lined with a tunica mucosa with gastric glands. Vorontsov (1967/1979) mentions that in “a number of forms of Dipodoidea the stomach” is “completely glandular” (page 222 of the English translation, 1979). It can be assumed that the differentiation of gastric forms in Myomorpha started with unilocular glandular stomachs and the differentiation of composite and plurilocular (bilocular in this case) organs followed later. In the Spalacicidae, Myospalax already shows a non-glandular fornix and corpus gastricus. All these already mentioned stomachs of Dipodidae and Spalacidae are unilocular. In the Muridae, the stomachs are composite and generally also unilocular, although slight constrictions can be identified, e.g. in Gerbillus. Bilocular stomachs are characteristic for Nesomyidae and Cricetidae. Some of these (Neotoma, Peromyscus, Dicrostonyx) have a glandular disc in an area with nonglandular mucosa, lined by squamous epithelium. Kohl et al. (2013) investigated the effects of anatomy and diet on

17 Myomorpha 

gastrointestinal pH in rodents. They compared Mus musculus, Peromyscus maniculatus and Neotoma lepida, coming to the conclusion “that bilocular stomach anatomy creates an environment in the proximal stomach that is suitable for microbial growth” (page 225). Myodes (= Clethirionomys) has an extensive pars glandularis. Butet and Delettre (2011) write that “Despite its phylogenetic position among arvicoline rodents, the bank vole (Myodes glareolus) shows morpho-physiological and ecological traits which tend to be more similar to murine species” (page 297). To get an impression of the food on gastric differentiation, information was compiled in a table from Boitani et al. (1983), Grzimek (1988), Sheng et al. (1999), Kryštufek and Vohralik (2005) (fields marked black in Fig. 4.81 indicate presence of respective material in food, fields with a white “X” indicate secondary importance – [“not so important”]). There are herbivores with a uniloculaer hemiglandular stomach (Tatera) and others which are bilocular and sub-hemoglandular (Mystromys, Myospalax) and in one case (Saccostomys) Perrin and Curtis (1980) give the impression that the pars nonglandularis is subdivided into a fornical and a pyloric section. A statement made in relation to the Cricetidae can be generalised: Although systematic position and gastric mucosal lining could possibly be related with each other – see Dipodidae – a clear relationship between food and

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gastric form in general could not be identified for the suborder Myomorpha. As an example for the Cricetidae Sakaguchi et al. (1981) write for Mesocricetus auratus (golden hamster) on page 510: “…the forestomach had no critical nutritional significance for the hamster given a nutritionally adequate diet”. The study of relationships between anatomical form and phylogeny is an interesting aspect. Although the total digestive tract has to be considered when the treatment of ingested food is discussed, it seems to be worthwhile to take gastric shape and mucosal lining together with food habits or trophic category (O’Connell (1986) into account (Fig. 4.83). Information on this aspect was compiled for the New World Cricetidae from seven publications: [1] Banfield (1981), [2] Eisenberg (1989), [3] Eisenberg and Redford (1999), [4] Niethammer (1988), [5] O’Connell (1982), [6] O’Connell (1986), [7] Redford and Eisenberg (1992). A maximum likelihood tree, based on tooth morphology studies (Fig. 4.83), is available (Jansa and Weksler, 2004; Carleton, 1973). The representative illustration of the unilocular hemiglandular organ is shown for sigmodontine genera, for the neotomine genus, Scotinomys, and for the two considered tylomyine genera Nyctomys and Tylomys. Discoglandular stomachs can be found in the unilocular Scapteromys and in two neotomine genera, Peromyscus and Neotoma. In addition to a discoglandular stomach, Peromyscus also has a diverticular organ.

Fig. 4.83: Phylogenetic tree (left), gastric outlines and mucosal lining in stomachs of 19 genera of Cricetidae (centre), as well as a table of food constituents (right). The tree is adapted from Jansa and Weksler (2004), gastric outlines from Carleton (1973). Information on food is from Banfield (1981) (1), Eisenberg (1989) (2), Eisenberg and Redford (1999) (3), Niethammer (1988) (4), O’Connell (1982) (5), O’Connell (1986) (6), Redford and Eisenberg (1992) (7), Matson et al. (2012) (8).

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Considering gastric shape and mucosal lining, the following conclusions can be drawn from Fig. 4.83: Considered Sigmodontinae have unilocular stomachs, which are hemiglandular, sub-hemiglandular or discoglandular. In Rheomys sp., the pars glandularis is completely surrounded by the non-glandular mucosal zone, which extends down to the pylorus (similar to the situation in discoglandular stomachs). In Sigmodontinae, there is considerable variability in mucosal lining, but no separation of gastric form into a bilocular organ. Carleton (1973) was able to demonstrate that the size of the glandular area can vary considerably in the stomach of Thomasomys sp.; therefore, two illustrations referring to that genus are given in Fig. 4.83. In the Neotominae, both form (unilocular and bilocular stomachs) and mucosal lining (hemiglandular, discoglandular, diverticular) vary considerably. In Peromyscus sp., discoglandular and diverticular stomachs can be found in different species (Carleton, 1973). The two considered genera of Tylomyinae have unilocular stomachs hemiglandular mucosal differentiation. Comparing general gastric shape and mucosa within the Cricetidae, the Tylomyinae stand closer to Sigmodontidae and most Neotominae are more distant. This statement is not in accordance with the present tree, published by Jansen and Weksler (2004), but according to Musser and Carleton (2005), the Nesomyinae belong to the family Nesomyidae, which is separate from the Cricetidae, including Sigmodontinae and Tylomyinae. In relation to food, 7 of the 14 genera of the Sigmodontinae with a unilocular and hemiglandular stomach have to be called omnivores, eating a wide range of food types (Fig. 4.83). However, the genus Reithrodon, which also has a unilocular hemiglandular stomach, is a herbivore and granivore. The unilocular hemiglandular type of stomach of the genus Thomasomys, which can also have a sub-hemiglandular organ, eats fruits and seeds. Scapteromys, eating arthropods and non-arthropod invertebrates, has reduced the pars glandularis to a small disc and the insectivorous genus Rheomys also shows considerable reduction of the relative size of the glandular area. In the two genera of the Tylomyinae, a unilocular hemiglandular stomach is found, but – different from the Sigmodontinae – these animals are frugivorous, i.e. they eat a food that is easier to digest than that of omnivores. Peromyscus and Neotoma, two genera of the Neotominae, eat material rich in plant cell-wall material and the formation of a set-off and relatively voluminous blindsac of the fornix gastricus, which is lined with squamous non-glandular mucosa, could increase retention of digesta. The pars glandularis in Peromyscus and Neotoma is reduced

to a small disc or even to a glandular diverticulum. To conclude, a clear relationship among the gastric form, mucosal lining and trophic category cannot be deduced from the available material, but systematic relationships between Cricetidae seems to play a role in the selection of food. Tylomyinae tend to live on a food consisting of fruits and many Sigmodontinae prefer a wide range of food constituents.

17.3.2.1 Remarks on the stomachs of Dipodidae Reference has already been made above to the statement of Vorontsov (1967/1979) that species belonging to the family Dipodidae have unilocular and glandular stomachs (Fig. 4.81). Organs of members of the dipodid subfamilies Cardiocraniidae, Dipodinae and Allactaginae have been illustrated by Naumova (1981). This relative “monotony” of mucosal lining in the Dipodidae does not coincide with a monotonous type of food within this rodent family. Predominant ingestion of seeds (granivory) can be found in different species, for example, in Salpingotus crassicauda (Cardiocraniidae) (Rogovin et al., 1985), as well as in Zapus trinotatus (Pacific jumping mouse, Zapodinae) (Gannon, 1988) or Z. princeps (western jumping mouse, Hart et al., 2004), where berries, fungi or insects represent less than 10% of the food. Within the Zapodinae, Napaeozapus insignis (woodland jumping mouse), seeds, roots and basal parts of plants represent about 70% of the food, but insect larvae, as well as fungi amount to only about 22% (Whitaker and Wrigley, 1972). In Zapus hudsonicus (meadow jumping mouse), Whitaker (1972) determined that insect larvae and beetles represent about half the food and seeds only about 20%. In the Sahara desert, where green vegetation and water are limited, Jaculus sp. (jerboa, subfamily Dipodinae) eats Scarabaeus cristatus beetles to maintain their water balance (Sánchez Piñero, 2007). According to Rogovin et al. (1985), Dipus sagitta (northern three-toed jerboa), another species belonging to this subfamily, is a green plant eater. The same author also mentions that Allacta balikunica (Balikun jerboa, Allactaginae) eats mixed food with green parts, seeds and insects in approximately equal proportions and Allactaga sibirica (Mongolian five-toed jerboa) and Euchoreutes naso (long-eared jerboa) tend to consume more animal food, such as insects and other invertebrates (Rogovin et al., 1985). The differences in chemical composition, as well as of physical characteristics, such as particle size or abrasiveness of gastric contents on the epithelium, do not stimulate the formation of squamous non-glandular mucosa in the stomach. The abrasive activity of the gastric content can be associated with a diet

17 Myomorpha 

including exoskeletons of arthropods, hard seed coats, rough herbage or bark (Horner et al., 1965). A remark of Perrin and Curtis (1980) can only be corroborated: “It is likely that there is no single causal factor in the evolution of stomach complexity and that in different families different selective pressures may have resulted in a diversity of stomach forms for various functions and diets” (page 31).

17.3.2.2 Remarks on the stomachs of Nesomyidae Two species from the total number of 61 (Wilson and Reeder, 2005) of the Nesomyidae have been studied anatomically in considerable detail: Cricetomys gambianus, the northern giant pouched rat, and Mystromys albicaudatus, the African white-tailed rat. The semi-schematic representation of both stomachs can be found in Fig. 4.81. In their study on Cricetomys gambianus, Knight and Knight-Eloff (1987) write that this species has a large, nonglandular fornix plus corpus region, which, according to Camain et al. (1962) together have the form of a lengthened pocket, into which the oesophagus opens. This area is papillated. A fully glandular antrum pyloricum follows. There is a sharp delineation between cornified and glandular mucosa. Both chambers are connected by a short narrow section with an external diameter of approximately 1 cm (Camain et al., 1962). This is not in accordance with the assumption of Knight and Knight-Eloff (1987), who call the stomach of C. gambianus unilocular. It has already been mentioned above that the formation of a voluminous blindsac, which forces digesta to make a “detour”, deviating from the direct oral-aboral flow, should be interpreted as a separate gastric compartment, thus making the organ a bilocular stomach. The squamous epithelium of the first chamber is covered with a layer of microbes. In this pouch, neither glands nor autoenzymatic activity from this gastric mucosa can be found. Knight and Knight-Eloff (1987) believe that the set-off gastric region may be important in the digestion of starch, glucose and nitrate. According to Camain et al. (1962). the pars glandularis consists of fundic or proper gastric glands, as well as of pyloric glands, the extension of which is reduced. From the cited findings it looks probable that alloenzymatic digestion takes place in the set-off gastric section, whereas the glandular part houses autoenzymatic digestion. Perrin and Maddock (1983) write: “Examination of the natural food preferences of Mystromys albicaudatus showed that the rodent selects a diet rich in starch, glycogen and protein. The bilocular stomach of M. albicaudatus

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is well adapted to efficiently digest these dietary components with carbohydrate digestion occurring in the keratinised fornix and protein digestion in the glandular antrum.” “Gastric fermentation is unlikely, but that the forestomach acts as an amylase reservoir. Large populations of amylase-producing bacilli, located on fornical papillae, contribute significantly to high alpha amylase activity in the fornix” (Perrin and Maddock, 1983, page 128). Superficially, the sacculated bilocular hemiglandular stomach of Mystromys albicaudatus (Mahida and Perrin, 1993, 1994) has a “forestomach” that has papillae and a high density of bacteria. Perrin (1987) does not join those many authors who speak or write of “ruminant-like” digestion when alloenzymatic digestion is mentioned. He calls the fornix gastricus of Mystromys albicaudatus and Cricetomys gambianus an amylolytic reservoir, rather than a site for cellulose fermentation. Gastric bacteria sit on the papillae formed by the pars nonglandularis (Maddock and Perrin, 1981), which optimise amylolysis, but not cellulose fermentation. The bacterial community might change its composition when the concentration of soluble sugar is low and that of crude fibre is high. C. gambianus (and its microflora) might be able to detoxify secondary plant compounds in the food (Perrin, 1987), but in M. albicaudatus this cannot be observed. Symbiotic association with numerous bacteria in the set-off section of the stomach of C.  gambianus or M.  albicaudatus implies coevolutionary adaptation between host and microbes (Perrin and Kokkinn, 1986). Ontogenetic development of the gastric microbial populations in M. albicaudatus was studied by Maddock and Perrin (1983). The present author will cite from this publication in some detail: The synchrony of events in gastric development and appearance of papillae, ingestion of solid food and the colonisation of papillae by bacilli, suggest symbiosis between mammal and microbes to intensify the process of alloenzymatic digestion. During gastric morphological development in the whitetailed rat, a microbial succession is apparent, initiated by a bacterial flora established in the gut during the first few days of life. A variety of transitory microbes invades the gut after birth and they colonise the stomach. The microbes are largely facultative anaerobes. During the third postnatal week, after the ingestion of solid food, gastric conditions change and become unfavourable for the juvenile facultative microbial community, but evidently suit the bacilli introduced with the solid food. These bacilli are specific to papillary microhabitats and do not occupy the folded fornical epithelium (Maddock and Perrin, 1983).

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17.3.2.3 Remarks on the stomachs of Cricetidae 17.3.2.3.1 Subfamily Arvicolinae The cricetids in general exhibit the greatest range of variability (O’Connell, 1986) and their subfamily Arvicolinae, including voles, lemmings and muskrats, presents an excellent example of impressive mammalian radiation (Woronzow, 1961; Carleton, 1981, Galewski et al., 2006; Robovsky et al., 2008). The effect of the radiation of the palaeo- and Nearctic Arvicolinae is beautifully documented in an atlas published by Shenbrot and Karasov (2005). To obtain an idea of the variability of the arvicoline types of stomachs, reference is made to the paper of Dearden (1969), as well as to information published by Luppa (1956) (Fig. 4.84). The available illustrations were ordered according to a tree, which was adopted from Robovsky et al. (2008). Already in the 19th century, Retzius (1841) and Toepfer (1891) describe plurilocular and composite stomachs in Arvicolinae. Under consideration of modern studies on phylogenetic relationships some direction of the gastric radiation is indicated: The subhemiglandular stomach of Lagurus lagurus, steppe vole, can be found on the most basic branch and different degrees of discoglandular stomachs are found in the younger branches (Lemmiscus curtatus, sagebrush vole, and Microtus pennsylvanicus, meadow vole). The shape of the discoglandular stomach of Dicrostonyx sp. (collared lemming), a “most basal” arvicoline (Robovsky et al., 2008), is quite different from that of Lemmus sp., a “true lemming”, where the hemiglandular situation can be found. Both genera are not closely related, as has already been suggested by Galewski et al. (2006). It can be seen in all gastric forms shown in the figure that the fornix gastricus is differentiated to a prominent blindsac. This means that the arvicoline stomach has to be called bilocular, especially when a transverse fold separates the pars pylorica from the corpus and fornix gastricus. In the Arvicolinae, the squamous epithelium is widely distributed (Lüthje, 1975), not only in the fornix gastricus. In some cases, it reduces the glandular mucosa to very small fields. According to Lüthje (1975), the squamous mucosa shows a remarkable activity of different enzymes, so that it functions as a transport and absorptive lining; Breton et al. (1989) found in Microtus pennsylvanicus (meadow vole) that secondary plant metabolites, such as ingested phenols and tannins, do not induce clear adjustment in the size of the major absorptive surface. According to Kajigaya and Goto (1980), the stomach of Microtus montebelli, the Japanese grass vole, is divided into two main parts; the “forestomach”, i.e. the fornix or

Fig. 4.84: Gastric forms and phylogeny in Arvicolinae. Gastric shape adapted from Dearden (1969) and Luppa (1956); the tree is from Robovsky et al. (2008).

fundus gastricus and the pars pylorica. Gastric glands can be found in two areas, the discoglandular region on the larger curvature and a few pyloric glands surrounding the pylorus, which are not depicted in Fig. 4.84. The discoglandular mucosal section in Dicrostonyx groenlandicus lies aborad of this fold in the pars pylorica, but in Lemmiscus curtatus and Microtus pennsylvanicus, in the region of the corpus gastricus. The glands of the tunica mucosa in the discoglandular area have parietal cells, as well as proper gastric gland cells (“chief cells”, Golley, 1960). With exception of the gastric gland areas, the stomach is lined with keratinized stratified squamous epithelium. The gastric gland areas are covered by a simple columnar epithelium (Kajigaya and Goto, 1980) and in the tunica mucosa at about 20 days of postnatal age (Kobaru et al., 1988) become mature in relation to gastric wall differentiation (Ohara et al., 1986). Two types of muscle were found in the stomach of Microtus montebelli. One is the smooth muscle, which

17 Myomorpha 

consisted of the most part in the stomach, the other is the striated muscle fibre found in the cardia and oesophageal groove (Dearden, 1966, Kajigaya and Goto, 1980). Striated musculature extends into the fold between corpus gastricus and pars pylorica, called the “corpopyloric fold” by Dearden (1966) or “Grenzfalte” by Toepfer (1891). Ohuchi et al. (1992) described the gastric groove of Microtus montebelli in some detail. According to these authors, microbial fermentation and VFA production take place in the fornix ventriculi and its contents is different from that of the pars pylorica (Kudo and Oki, 1981). A structure that makes bypass of this fermentation region possible seems to make sense. Ohuchi et al. (1992) demonstrate prominent lips formed on both sides of the groove by the innermost muscular layer, the fibrae obliquae, which might separate the bypassing digesta from the bypassed material in the fornix gastricus. In the fundus gastricus of the Japanese grass vole (M. montebelli), Kudo and Oki (1981) demonstrated gastric fermentation. The pH value and amounts of total VFAs were always smaller in the fundic and pyloric regions of the stomach than in the “sac” formed by the fornix and acetic acid was the major fermentation product. More than 106/g aerobic and anaerobic bacteria were present in the fundus gastricus. In addition to Microtus montebelli, which has mainly been investigated by Japanese researchers, other arvicoline species have also been studied and have formed the basis for reflections. For example, Garon and Piérard (1972) speculate that the gastric groove which extends to the pylorus of Ondatra zibethicus, the muskrat, has, “no doubt”, to be explained by the aquatic life of the animal. In most mammals, swallowed liquids pass towards the pylorus without mixing with the gastric contents. The muskrat ingests abundant quantities of water, which, very probably, pass the stomach rapidly. Fermentative or alloenzymatic digestion in the stomach of Arvicolinae can be found in different species. Most arvicolines eat mainly green matter (Butet and Delettre, 2011), and according to Herrmann (2002), food ranges from leaves, seeds, roots and mixtures of these. However, this myomorph subfamily should not be considered as strict herbivores. For example, bank voles (Myodes glareolus [Clethrionomys g.]) are able to exploit a wide spectrum of trophic resources from low energetic lignified tissues to high calorific invertebrate prey. This results in a very diverse diet (Viro and Niethammer, 1982; Burkhardt and Schlund, 2005; Butet and Delettre, 2011). The consumption of animal matter has the potential to

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play a major role in the nitrogen economy, as Campbell and MacArthur (1996 b) showed in muskrats (Ondatra zibethicus). An interesting remark on the significance of alloenzymatic fermentation in the fundus gastricus of voles was made by Manaeva et al. (2012) in a comparative study on Microtus levis (East European vole, in that study as M.  rossiaemeridionalis) and Myodes (Clethrionomys) glareolus. Even when the cellulose content increases in forage plants, alloenzymatic digestion is low in these species because of the brief stay of the food in the fornix, which is insufficient for the development of substantial enzymatic activity of microorganisms. When this relatively low degree of alloenzymatic digestion in the stomach should be followed by low fermentation rates in the large intestine, reingestion of faeces could improve energy availability when food supply is limited. Cranford and Johnson (1989) studied this process of coprophagy in Microtus pennsylvanicus, meadow vole and M.  pinetorum, pine vole. In these investigations, prevention of coprophagy resulted in subsequent decline of body mass. Despite this rather cautious statement, a remark of Perrin and Maddock (1985), based on studies of South African rodents, should be kept in mind: “The evolution of complex gastric anatomy in rodents,…, can only be explained by increased digestive efficiency, an expanded nutritional niche” (page 323).

17.3.2.3.2 Subfamily Sigmodontinae Ellis et al. (1994) studied five species of Sigmodontinae in the pampa of Argentina. Referring to studies of Vorontsov (1960) these authors stated that a low energy and high cellulose food, as compared to a high-energy, high protein or high lipid diet, should be connected, among other aspects, with a small size of glandular mucosa relative to an extensive surface area covered with cornified epithelium. The compilation of information on gastric form, mucosal lining and food constituents of South American representatives of the Cricetidae can be found in Fig. 4.83. The illustration shows for Scapteromys and Rheomys that animal food (high-energy) is related with a relatively small glandular area and extensive squamous non-glandular area. Sigmodontinae usually have a unilocular stomach (Finotti et al., 2012) and in some cases (e.g. Scapteromys) the organ is hemiglandular. They are mostly omnivores, but large differences in proportions of food items were identified. Neither a relationship between food quality and mucosal lining nor between quality and number of gastric chambers could be discerned.

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 IV Euarchontoglires – 17 Myomorpha

17.3.2.3.3 Subfamily Cricetinae In Fig. 4.81 Cricetinae (hamsters) are represented by three genera; Mesocricetus, Cricetulus and Phodopus, all three species are, as the whole subfamily, from the Old World (Asia). They have a prominent fundus gastricus, which is lined by a non-glandular tunica mucosa and their pars glandularis can be of relative variability: It is very extensive in Mesocricetus sp. and relatively small in Cricetulus sp. Nevertheless, all three species are granivorous, but they also eat tubers, as well as arthropods. In an interesting study, Ehle and Warner (1978) removed potential “fermentation chambers” from the digestive tract of living golden hamsters (Mesocricetus auratus). In animals fed nutritionally adequate diets, based either on cereals or alfalfa, the forestomach does not appear to be of critical nutritional significance; hamsters with their forestomach removed performed equally well as intact ones. Sakaguchi et al. (1981) come to the radical conclusion in relation to the fundus gastricus of Mesocricetus auratus that “…the forestomach had no critical nutritional significance for the hamster given a nutritionally adequate diet” (page 510). This view was recently corroborated by Shinohara et al. (2016), who studied the microbial population in the “forestomach” of Tscherskia triton, the greater long-tailed hamster, but found that the bacterial diversity in that gastric region was low; the “forestomach” does not function like the rumen of ruminants. DiBattista and Robillard (1993) believe that the fundus (= fornix) gastricus allows Mesocricetus auratus to consume voluntarily substantial amounts of the disaccharide sugar lactose. Surgical removal of the “pregastric pouch” caused a 40% reduction in total lactose consumption, but the authors do not comment on the biological significance of this unusual behaviour. It has already been mentioned that the fornix or fundus gastricus in hamsters is lined by a squamous nonglandular tunica mucosa, which is superficially similar with the rumen mucosa. In a study on the rat (Muridae, Murinae), Robert (1971) even proposes the term “rumen” for the non-glandular section of the stomach of Rattus norvegicus! Moir (1965) argues that absence of glands and enzymatic activity in a “forestomach” region makes microbial digestion and fermentation probable. However, it should be emphasised that the tunicae mucosae with a squamous non-glandular epithelium can be morphologically and functionally different structures. For example, the enzymatic activities in the ruminant stomach allow active transcellular transport, but in the pars proventricularis of horses, such a transport is not made possible by the squamous epithelium (Schnorr and Wille, 1971). Even the subepithelial capillaries in the proventricular part of

the horse are free of endothelial pores (Wille, 1972) and thus make active transport, as is possible in the ruminal wall, impossible. Returning to Cricetinae: Sakata and Tamate (1976) compared the histology and ultrastructure of the mucosa of the fundus gastricus in the golden hamster with the ruminal mucosa of Ruminantia. Both types of mucosae showed general resemblance. In ultrastructure, the epithelium of the hamster forestomach showed a typical keratinising stratified epithelium. The upper strata of the hamster epithelium suggest that the rate of cell proliferation and postmitotic aging are probably much slower than in the ruminal epithelium. As Mesocricetus auratus is an often used laboratory animals, the arterial supply of the organ (Schwarze and Michel, 1957), as well as the finer adrenergic and a cholinergic nerve distribution in the gastric wall (Stach, 1977) have been studied. To obtain an idea about the ontogenetic development of the non-glandular and glandular section of the stomach, Sakata and Tamate (1979) studied the postnatal ontogeny of the non-glandular mucosa of Mesocricetus auratus. The postnatal preweaning and postweaning increase in weight of this region in the golden hamster was nearly linear during the first 7 weeks (weaning occured at about 3 weeks postpartum) and the weight of the fundus gastricus increased to about half of the glandular part during the first 8 weeks postpartum. The situation of the adult M. auratus is depicted in the semi-schematic illustration of the golden hamster stomach given in Fig. 4.81. Histologically, the forestomach epithelium develops mainly during the first 2 weeks of life, with no further changes after weaning (Sakata and Tamate, 1979). 17.3.2.3.4 Subfamily Neotominae In Fig. 4.83, gastric shapes and mucosal lining are shown for three genera, including Neotominae. In Scotinomys, a unilocular hemiglandular stomach is differentiated, but in the other depicted genera, the relative size of the glandular area is considerably reduced to the discoglandular or diverticulated form. Most differentiated is the diverticulated form of Peromyscus sp. (deermouse) (Vorontsov, 1967/1979). Horner (1962) and Horner et al. (1965) discuss the morphology of the stomach of the southern (Onychomys torridus) and northern (Onychomys leucogaster) grasshopper mice (not depicted), which both are chiefly insectivorous or carnivorous rather than herbivorous; Horner et al. (1965) even speak of “predators”! Eighty-nine percent of the food eaten was of animal (insect) origin. Seeds, fruits and leafy foods are eaten when nothing else is available. The stomach is diverticular. The diverticulum is called “fundic region”, a terminology that is unacceptable

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because this gastric section lies on the greater curvature of the corpus gastricus and not in fornix or fundus to the left of the cardia as dilatation of the greater curvature. Because of a relatively voluminous fundus, the stomach, at least, tends to be bilocular with fundus gastricus and antrum pyloricum. In between lies the corpus gastricum with the above-mentioned diverticle. With the exception of the diverticle, the stomach is lined by non-glandular mucosa with squamous epithelium. At the base of the fold that surrounds the diverticulum lies a small zone of cardiac mucosa (Horner et al., 1965), the remainder of the diverticle is lined by proper gastric gland mucosa. 17.3.2.3.5 Subfamily Lophiomyinae This subfamily contains just one species, Lophiomys imhausi (maned rat). According to Vorontsov (1967/1979), this species has an intensively differentiated stomach within the Myomorpha (Fig. 4.85). The original description of the stomach is from Milne-Edwards (1867) and the following text is based on a translation from the original French (pages 106–107) done by the present author, as well as from the English version of the book of Vorontsov (1967/1979). The terminology, which is generally applied in that text will also be used here: The stomach is well developed, especially in relation to length (Fig. 4.85 C). At the lesser curvature, the oesophagus opens into a curved stomach compartment (I). From the fundus or fornix gastricus, a part of this curved compartment (I), an additional pocket (V), which is lined by a non-glandular squamous tunica mucosa, branches off in slightly dorsal direction. This is reminiscent of a similar formation in swine (Sus), the diverticulum ventriculi (Schaller, 1992). The gastric compartment “I” ends at a narrow isthmus beyond which the gastric tube (II) (very probably representing the corpus gastricum), also lined by squamous epithelium, “descends” to another narrow isthmus where a small diverticle (IV) can be discerned. Beyond this differentiation starts the “ascending” portion (III) of the stomach, which is lined by nonglandular mucosa and ends at the pylorus, where the duodenum begins. The opening leading into the glandular diverticulum ventriculi of the stomach in Lophiomys (IV in Fig. 4.85 C) is so small that food could not pass into this area and proteinaceous food is treated in the gastric regions II and III with the gastric juice secreted by the glandular diverticulum ventriculi, which is, in fact, a large gland. The stomach has an intestinal aspect, but Milne-Edwards (1867) comes to the surprising conclusion that the spread-out stomach is unilocular. We may assume, on the basis of the stomach structure, that cellulose food plays an exclusive role in the nutrition of this species. Vorontsov (1967/1979) speculates

Fig. 4.85: Stomach of Lophiomys imhausi. The roman numerals mean: I: first gastric compartment; II: gastric tube, “descending” portion; III: gastric tube, “ascending” portion; IV: diverticle of gastric tube; V: fornical diverticle. Adapted from: Milne-Edwards (1967) (A, B) and Vorontsov (1967/1976) (C).

that the stomach in Lophiomys represents the extreme degree of adaptation to cellulose nutrition. However, the food of Lophiomys imhausi consists of leaves, fruit and shoots (Kingdon, 1974b), which do not seem to be extremely rich in cellulose. 17.3.2.3.6 Subfamily Tylomyinae These rodents are primarily frugivores (Eisenberg, 1989), as well as on seeds and insects (Hunt et al., 2004). In Fig. 4.83, a unilocular and hemiglandular stomach is shown, so that it can be assumed that food of good quality, as fruits are, can be well handled by this type of stomach.

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17.3.2.4 Remarks on the stomachs of Muridae Almost half of the genera 150 (= 46%) and species 730 (= 48%) of the Myomorpha are represented by the Muridae. Despite this large number, the gastric anatomy is known in detail only in very few species. The two murid species that are often used as laboratory animals, Mus musculus, the house mouse, and Rattus norvegicus, the brown rat, have been intensively investigated – in many cases as the easily available “rat or mouse model” in clinical studies and not as objects of basic research on form and function. Careful investigations of gastric anatomy on related species are available. In the following, reference will also be made on Meriones unguiculatus (Mongolian jird) (Schendel and Wissdorf, 1973) and Acomys spinosissimus (Southern African spiny mouse) (Boonzaier, 2012), as well as on Australian rats and mice that were investigated by Breed and Ford (2007). The stomach of Rattus norvegicus has been described in detail by Hebel (1969b) and is depicted in Fig. 4.86. The following description is from page 256 of that text and was translated from German and adapted by the present author. The stomach lies transversally to the longitudinal axis of the abdomen, mainly extra-thoracically in the left anterior part of the abdominal cavity. The lesser curvature is very short and is directed craniodorsally. The greater curvature is directed to the left and caudoventrally. Viewed from the outside, the stomach is subdivided into two sections. Starting from the oesophageal opening, a clearly marked line can be followed over the corpus gastricum almost perpendicular to the longitudinal axis of the stomach. On the side towards the fundus gastricus, the gastric wall is thin and seems to be almost transparent and forms a clear blindsac, extending craniodorsally. Towards the pylorus, the stomach narrows and the beginning of the duodenum is marked by a prominent constriction, the pylorus. The tunica mucosa of the oesophagus extends on the gastric wall into the fornix gastricus. A squamous and non-glandular zone of the tunica mucosa extends from the cardia and lines the blindsac to the “margo plicatus”, which represents the above-mentioned “margo”, ridge or small fold of non-glandular squamous mucosa. In this non-glandular section, the gastric wall is just half as thick as the glandular section in the distal corpus gastricum and the pars pylorica. The fact that the wall of the fundus gastricus is very thin has functional consequences. Under the influence of physiological investigations on cats by Schulze-Delrieu et al. (1998) and on humans by Schwizer et al. (2002), Liao et al. (2005) studied the rat stomach. The “proximal stomach” volume, i.e. the fundus gastricus, increased more than the “distal stomach”, the pars pylorica,

Fig. 4.86: Internal aspect of the opened stomach of Rattus norvegicus with gastric regions. Adapted from Hebel (1969b).

during food intake. The volume of the lumen of the nonglandular stomach can increase from the 70 to 145% of the glandular stomach volume and the non-glandular section deforms more than the glandular stomach. Confusion is produced by Brümmer (1876): This author calls the section of the murid stomach that is internally lined by a squamous non-glandular mucosa the “Muskelmagen” (muscular stomach), but does not show massive musculature for that compartment. According to that author, this gastric section is followed by the “Drüsenmagen” or glandular stomach, a term that is clear and correct. It seems to be a problem with laboratory rodents that “private terminologies” are applied, which do not consider comparative aspects. For example, in a general description of the stomach of Rattus norvegicus Oehmke (1963) calls the fold between squamous non-glandular and glandular mucosa, which is, in fact, the margo plicatus, “plica circularis” and names the fundus gastricus “pars cardiaca”, but mentions that the tunica mucosa of that section is a continuation of the oesophageal lining. Describing the stomach of Meriones unguiculatus (Mongolian jird) Schendel and Wissdorf (1973) use descriptive terms for two of the gastric sections that do not refer to comparative anatomical considerations, but which are relatively “neutral”. The stomach of that species is unilocular and composite and has a large “pars proventricularis” (= fundus gastricus) and a smaller “pars intestinalis” (= pars pylorica). Both sections touch each other without externally visible constriction. In a recent study, Boonzaier (2012) investigated the stomach of Acomys spinosissimus, the Southern African spiny mouse. This organ is U-shaped with well-developed greater and lesser curvatures and a spacious corpus region in the centre. On one side of the corpus gastricum lies the

17 Myomorpha 

fundus gastricus and on the other the pars pylorica. The fornix and pyloric regions lie close to one another because the incisura angularis is “sharp” and deep. Internally, the fornix of A.  spinosissimus is lined with stratified squamous epithelium around the oesophageal entrance. The fornix or fundus gastricus is demarcated from the glandular gastric epithelium by a “limiting ridge/line”, the margo plicatus. This ridge crosses the lesser curvature at the angular incisure and the greater curvature at a point opposite the angular incisure. The gastric glands in the corpus of the stomach appeared tubular. Numerous parietal cells (triangular shaped) were present in the isthmus and neck of the glands, as well as several peptic cells at the base of the gland. Few neck mucous cells were observed in the corpus of the stomach of A. spinosissimus. In their book on the native rats and mice of Australia, Breed and Ford (2007) deal with the diet and gastrointestinal tract morphology of four species of Murinae, Notomys mitchelli (Mitchell’s hopping mouse), Melomys cervinipes (fawn-footed melomys), Uromys caudimaculatus (giant white-tailed uromys) and Hydromys chrysogaster (common water rat) (Fig. 4.87). The stomach in all four species is subdivided into two regions, which are clearly demarcated from each other. In three species, a hemiglandular stomach can be identified, but in Hydromys chrysogaster, the area with the non-glandular mucosa is reduced (Speight et al., 2016) to the fundus gastricus, whereas in the other three species, this area descends down to the corpus gastricum in a situation which is similar to that already depicted in Fig. 4.86, where the borderline between the pars nonglandularis and the pars glandularis can be followed as margo plicatus over the corpus gastricum. The fundus and corpus are lined by several layers of a stratified squamous epithelium, whereas the second half of the stomach, the pars pylorica, has a simple columnar glandular epithelium and secretes proteolytic enzymes for digestion of proteins. The function of the fornix gastricus and distal corpus gastricum has been an area of debate, but according to Breed and Ford (2007), its most likely function is to prolong the period of time that amylases, which are secreted by the salivary glands and mixed with food in the mouth, can act to break down starch and glycogen. These authors consider the possible relationship between food and gastric differentiation. In Notomys mitchelli, characterised by the authors as an omnivore, about half of the stomach is composed of the corpus region and the other half represents the antrum (Fig. 4.87). In the more herbivorous species, Melomys cervinipes, the corpus and the extended diverticulum, formed by the fundus or fornix gastricus, probably store nonfibrous plant material. The frugivorous and herbivorous Uromys caudimaculatus

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has a large stomach with the pars nonglandularis making up around 65% of the total gastric surface area and extending into the corpus gastricum. In addition, Uromys c. has a gastric sulcus that passes from the base of the oesophagus to the antral region of the pars pylorica and may allow food to be selectively passed to either the corpus of the stomach or antrum. By contrast, in the carnivorous Hydromys chrysogaster the stomach has a much larger pars glandularis and pars pylorica, which extends into the fornix region. Although Uromys c. and Hydromys c. have similar body weights, the stomach of the latter is smaller. Furthermore, only about 25% of its volume is made up of the pars nonglandularis, with the rest being composed of a typical glandular lining. This is a markedly smaller relative volume of the fornix gastricus than in the herbivorous or even omnivorous, native rodents. The histology of the murine stomach has been mainly studied in Rattus norvegicus and Mus musculus. Many of the investigations are descriptive texts with little or no consideration of functional aspects: For example, Dawson (1948) described argentaffin and argentophile cells of the fundic mucosa of Rattus norvegicus, but was not able to assign a function to these cells. Pipan (1968) investigated keratohyaline granules in cornified mucosa of the mouse

Fig. 4.87: Mucosal lining in four species of Australian Murinae. Non-glandular tunica mucosa in black. Scale-bars represent 1 cm. Adapted from Breed and Ford (2007).

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fornical region, but a clear picture of cornification and granules could not be obtained. The glandular mucosa of the mouse was intensively studied, often as a “mouse model”. Karam and Leblond (1993) published excellent illustrations of a proper gastric glandular tube in mice with different cell populations in its basal, neck, isthmus and foveolar section, as well as the surface mucosa which lines the gastric lumen. In the adult mouse, it is the glandular isthmus which represents the generative zone for cell replacement in the gastric glandular tubes (Takeoka and Kataoka, 1986). A large number of mitoses found in the foveolar and mucous neck cells after refeeding, following a fasting period, is believed (Hunt, 1957) to replenish not only surface cells, but also parietal and possibly zymogenic cells. Kantani-Matsumoto and Kataoka (1987) concentrated on the number of secretory granules in the epithelial cells of the foveolae gastricae. At the end of the weaning period, histogenesis of the mucosa of the gastric pars pylorica of the mouse was observed by Takeoka and Kataoka (1986), indicating that the mucosa had to be adapted to nutritional conditions during adult life. Chief and parietal cells can be distinguished in the gastric glands one day after birth (Kammeraad, 1942). The glands increase immensely in length during the first 15 days of postnatal development and by the 25th day, the distribution of the chief and parietal cells reaches the adult condition. Prospective chief and parietal cells of the rat stomach can be demonstrated on day 16 after conception and the differentiation of the mucoid surface cells extends from day 17 to day 19. In the gastric mucosa of rat foetuses, the mucoid neck cells differentiate as the last cell type. The interrelationship between weaning on postnatal days 15–20 and increase in the number of endocrine cells producing gastrin density was studied in rats by Ekelund et al. (1985). Along the lesser curvature of rat and mouse stomachs, a “small portion of the mucosal epithelial cells lining the gastrointestinal tract exhibit several unique features; these polarized cells have a narrow apical pole with a tuft of numerous strait microvilli that…contact the gut lumen” (Breer et al., 2012, page 15). These chemosensory cells might be able to “taste” digesta constituents. The arterial supply via the truncus coeliacus, an unpaired branch of the aorta abdominalis, is very variable within rat and mouse, as Firbas et al. (1972) documented. The gastric terminal vessels, the mucosal capillaries, are fenestrated and pass in close proximity to the gastric glands (Gannon et al., 1982). Because of the close proximity of the fenestrated mucosal capillaries to the parietal and other mucosal epithelial cells secretion and general

cellular metabolism is enabled. In relation to the number of intramural ganglionic cells, Schardt and van der Zypen (1974) did not differentiate between the pars nonglandularis and glandulares, but were able to show the difference between general gastric wall and the region of the pyloric sphincter: In the stomach, there are about 26 × 103 ganglia/cm3, but in the pylorus, about 46 × 103 cells/cm3; in the following duodenum, the number decrease to about 5000 ganglia/cm3. However, not only the differentiations in the gastric wall, especially the pyloric sphincter, play a role in gastric emptying, but events occurring at the level of the intestine govern this process in rats (Vachon and Savoie, 1987). Having seen the wide range of the gastric internal surface that is lined in Murinae with a non-glandular squamous tunica mucosa, the question concerning the functional significance of that region, has to be asked, not only for this subfamily, but also for the rest of the Myomorpha with this type of gastric differentiation. Kunstýr et al. (1976) dealt with this problem in rats. From this publication, it is worth to cite verbally: The forestomach “has a reservoir function which has special importance for dietary carbohydrates. In the forestomach, a continuous process of amylolysis takes place, with the resultant formation of simple sugars, important for the intense energy metabolism of these small rodents” (page 170). For Gärtner and Pfaff (1979), the pars nonglandularis or “forestomach” of rats and mice is simply “a food store without bacterial protein digestion”, as they write in the title of their publication. To proceed with the considerations of Kunstýr et al. (1976): “In contrast to ruminants, in which the rumen has a multiplicity of functions, it appears that amylolysis is about the only digestive function of the rat forestomach. Therefore, the large population of microflora seems to play a rather detrimental role. The real functions, particularly those of the lactobacilli on the wall of the forestomach and yeasts on the muscous membrane of the glandular stomach, are not yet understood” (page 170). It is an interesting aspect, also mentioned by Kunstýr et al. (1976), that rats with a surgically removed “forestomach” lived without complications for more than 1 year. Despite the wide opening between the pars nonglandulares and glandulares, Peters (1973) states for Rattus norvegicus that the pH of the filled “forestomach” is not affected by secretions from the glandular stomach. However, the values in the pars nonglandularis (pH 4.3) of normal rats and in the pars glandularis (pH 3.2) are characteristically different (Browning et al., 1984). The mucosal protection of the glandular mucosa against luminal acid develops, as Dial and Lichtenberger (1986) found, only after the first several

17 Myomorpha 

weeks of life. Mucins are high-molecular-weight glycoproteins. They are also produced in the stomach of rats. “The most remarkable property of mucin is its ability to form a gel, a viscoelastic semisolid material that adheres to the epithelial surface and provides a physical barrier between the underlying cell surface and lumen; it is termed the first line of defence against potential luminal insults. Therefore, an increase in mucin content at the mucosal surface, produced by dietary fibre, could impair the rate of nutrient absorption” (Satchithanandam et al., 1990, page 1182). There are two main criteria that might influence the developmental differentiation of the gastric wall: dietary bulk, as well as short-chain fatty acids. Sakata (1986) investigated the stomach of the laboratory rat, Rattus norvegicus. Under the influence of bulk the absolute weight of the pars nonglandularis (Sakata speaks of “forestomach”) increases and the weight of the pars glandularis (“hindstomach”) relative to body weight decreases significantly. The influence of the short-chain fatty acid (SCFA) could not be shown. Based on his detailed knowledge of ruminant physiology, Sakata (1986) comes to the conclusion that the absolute increase of “forestomach” weight resembles the situation in ruminants where bulk promoted the development of the muscle of the forestomach musculature. Although there is a coevolutionary process between muroid rodents and their endosymbionts, these animals depend less on the activity of their endosymbionts than ruminants do (Naumova, 1990). As that author writes, the stomach and the whole digestive tract adapt not only to particular feeding habits, but also to the symbionts, which are the primary consumers of food entering the forestomach and simultaneously producers of valuable nutrients for the host. In addition to the function of the pars nonglandularis as digesta reservoir, it particularly deals with the carbohydrate in the diet. Peters and Gärtner (1973) mention a continuing process of amylolysis and formation of simple sugars made available for the energy metabolism of Rattus norvegicus. To conclude this paragraph on the Muridae, the process of coprophagy should be mentioned, which was so impressively treated by Hörnicke and Björnhag (1980). It can be found in the two well-investigated murine species Mus musculus and Rattus norvegicus. Ebino et al. (1988) shows what he calls the innate behaviour of coprophagy in the laboratory mouse. Cree et al. (1986) discuss it in Rattus: Fermentable components are completely digested by the microflora during the first passage through the lower bowel and no additional fermentation occurs with subsequent reingestion. However, bodies of microbes can be used as additional protein sources when they are reingested with the faeces.

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17.3.2.5 Remarks on the stomach of Spalacidae A discussion of the evolutionary history, speciation and population biology, but no information on the anatomy of the Spalacidae has been published by Savić and Nevo (1990). Velichko (1939) mentions that striated musculature extends into the cardiac region of the stomach; further details are not given. Ilgün and Özkan (2012) write that a deep incisura angularis extends from the lesser curvature of the organ. Because of lack of other anatomical information on gastric anatomy of the Spalacidae, reference will mainly be made in the following to the only publication on that subject known to the present author, the English translation of Vorontsov (1967/1979). This author gives a detailed description of Myospalax myosplax, the Altai zokor. A related species, Eospalax fontanierii, the Chinese zokor, is described by Zhang and Liu (2003) as highly specialised herbivore with a fossorial mode of life, living in underground burrow systems. According to Vorontsov (1967/1979), the Myospalax’s stomach structure sharply differs from other spalacids. Savić and Nevo (1990) write on page 132 of their paper about Spalacidae: “The phylogeny and systematics of the family has been largely intractable since the establishment of the family. This is true from the familial down to the specific level and no consensus is yet in sight”. Another clear statement, of Norris (2009), presents the actual view of the problem: “Recent molecular studies have concluded that the genus Myospalax evolved from within the rodent subfamily Cricetinae. […] Based on our analyses, Myospalax appears to be sister to a clade containing the subfamilies Spalacinae and Rhizomyinae, and all three of these lineages appear to be basal to the superfamily Muroidea. Based on the position of these three lineages, we suggest that they be placed in a distinct family, the Spalacidae, rather than subsumed as subfamilies in the family Muridae”. (page 139). The stomach of Myospalax is one-chambered (Vorontsov (1967/1979)), but a deep fold on the lesser curvature partially separates the pylorus from the fundus (Fig. 4.88). It was first described and depicted in a monograph by H.  and A.  Milne-Edwards (1868–1874), who mention the genus Siphneus, which is an obsolete synonym of Myospalax (Musser and Carleton, 2005). The fundus gastricus and corpus gastricum are lined with squamous non-glandular epithelium. The blindsac of the fornix is lined with multiple villi (1 in the illustration), reaching a height of 5–7 mm. The presence of villi in the stomach of Myospalax sp. is a peculiar feature of this rodent. Villi considerably increase the wall area of the “fermentation chamber”. A squamous non-glandular, but smooth, epithelium follows aborad (2). This non-papillated zone widens from the oesophageal opening towards the greater

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Fig. 4.88: The stomach of Myospalax myospalax. Significance of numbers: 1. Papillated fornix gastricus, 2. Non-papillated corpus gastricum, 3. Glandular pars pylorica. Adapted from: Milne-Edwards (1868–1874) (A, B); Vorontsov (1967/1979) (C).

gastric curvature. The margo plicatus separates squamous non-glandular mucosa from the glandular portion (3), which stretches caudad of this ridge and represents the pars pylorica. Vorontsov (1967/1979) states that the stomach of Spalax sp. highly resembles those of Arvicolinae and Cricetinae and seems to be adapted to cellulose nutrition. Spalax giganteus (giant blind mole rat), Sp. microphthalmus (greater blind mole rat) and Sp. leucodon (lesser blind mole rat) have a similar stomach structure divided by a deep isthmus into two chambers and the non-glandular squamous epithelium lines the entire fornix gastricus, whereas the glands are concentrated only in a small portion in the pars pylorica. Gorgas (1967) speaks of a bilocular stomach in Spalax leucodon, of which the main section is lined with a non-glandular cornified squamous epithelium.

17.4 Small intestine of Myomorpha The publication of Lemaire et al. (1980) presents a remarkably simple situation in the duodenum of the Norway rat, Rattus norvegicus. Three sections are mentioned. They

can be correlated with the pars cranialis and its ampulla duodeni, pars descendens and pars ascendens, but anatomical names are not given in that paper. In the Mongolian gerbil, Meriones unguiculatus, Schendel (1972) differentiated three sections of the duodenum from each other, the partes cranialis, descendens and ascendens, separated from each other by the flexura duodeni cranialis and flexura duodeni caudalis. At the flexura duodenojejunalis, the duodenum passes into the jejunum. The length of the small and large intestines, relative to the total intestinal length, is variable. Recent comparative studies of the situation in Hydromys chrysogaster, the common water rat, which is carnivorous, showed a comparatively long small intestine, which represents approximately 90% of the total intestinal length. This is much longer than in other more omnivorous and herbivorous Australian myomorphs where the small intestine contributes about 60 to 70% to the total intestinal length (Speight et al., 2016). The authors believe that this increase in length is an adaptation to a carnivorous protein-rich diet. Mouse, rat and golden hamster are all representatives of the rodent suborder Myomorpha and are used in many laboratories as experimental animals. The villi intestinales in the duodenum of Rattus norvegicus have a length of 1 to 5 mm. They are orientated in a zigzag course transversally to the longitudinal axis of the gut (Hebel, 1969). Towards the jejunum the length and width of the villi decreases. Only in the first 6 to 8 mm of the tela submucosa in the duodenum, Hebel (1969) found Brunner’s glands and irregularly arranged Peyer’s patches. The villi intestinales in a healthy duodenum of Norway rats are finger-shaped and have a smooth surface (Madge, 1974). The study of Winne (1975) gives an interesting comparative illustration of the villi intestinales of the rat, rabbit and cat. According to Stenling and Helander (1981), the mucosa of the small intestinal mucosa in the rat is characterised by its large transport capacities. An increase of absorptive capacity in aboral direction is related with the number of villi intestinales per area of mucosal surface and the size of duodenal villi intestinales. In the yellow-necked mouse, Apodemus flavicollis, the villi are smallest in the duodenum and biggest in the jejunum (Wilczynska, 1999). The structure of absorptive cells in the small intestine of rats during starvation (up to 21 days!) was investigated by Sohma (1983). The basal parts of the enterocytes showed remarkable changes. The apical section of the enterocytes was not structurally changed, so that the cell would be able to absorb nutrients when these become available again. In the investigation of the mouse, Mus musculus, by Potten and Loeffler (1987), the postmitotic migration of epithelial cells starting from the crypts of the small intestine is demonstrated and the development of villi intestinales is described together with the

17 Myomorpha 

differentiation of the total tunica mucosa by Kammeraad (1942) and Mathan et al. (1976). Wilczynska and Przystalski (1996) indicate that the different sections of the tunica mucosa in mice change in thickness with increasing age. Regional distribution and relative frequency of endocrine cells was studied in Microtus montebelli, the Japanese field vole, by Ohara et al. (1986), but the functional significance of the findings could not be explained by these authors. Kurohmaru et al. (1983) present an interesting point concerning the villi intestinales of the small intestine of Microtus montebelli. In the duodenum of adult animals, a net-like arrangement of folds, running mainly transversally, can be discerned. The authors describe that at birth, these villi are differentiated, but at 20 days of postnatal age, the duodenal villi become “wide” and fuse with each other to form the above-mentioned folds, which also differ in shape from those in the jejunum, where they follow a wavy course. It is assumed by the researchers that the existence of fused villi in the small intestine is related to a herbivorous habit, but a convincing explanation for this assumption is not given. When only the tunica mucosa is considered, the transition from stomach to duodenum is gradual in Microtus sp. (Golley, 1960). A simple columnar epithelium is found in the duodenum. Villi intestinales are short and broad. Few goblet cells lie in the villus epithelium. Below the lamina epithelialis mucosae Brunner’s glands are differentiated. These glands form a ring in the submucosa. Caudad the glands of Brunner decrease in height, but maintain their continuity around the duodenum. In Mesocricetus auratus, the golden hamster, Kurohmaru et al. (1979) describe the prenatal development of villi intestinales. At birth, each of these absorptive cells has a structure almost similar to that in adult.

17.5 Colon of Myomorpha Within the myomorphs, the relative functional importance of the colon can be variable. This is probably related with the different types of food the different species eat: For example, according to Green and Millar (1987), prairie voles (Microtus ochrogaster) respond to decreasing diet quality by retaining more ingesta in the caecum than in the small intestine or colon. The food of Microtus ochrogaster consists of a wide variety of green forbs and grasses in summer and stored bulbs, rhizomes, and seeds in autumn. In winter, tubers and bulbs are eaten (Banfield, 1981). Retention of digesta in the caecum gives enough time for microbial degradation of the food. On the other hand, deer mice (Peromyscus maniculatus) retain more ingesta in the small intestine than in the caecum and colon. According to Banfield (1981), Peromyscus maniculatus is an omnivore, it

 215

eats the seeds of a wide variety of grasses and forbs. It takes berries, cherries, wild apple, as well as mushrooms and buds. Besides this vegetable diet, deer mice are very fond of insects, eggs, larvae, cutworms, caterpillars, and spiders. As compared with the prairie vole, deer mice eat food of high quality. This allows effective and sufficient digestion of food and absorption of nutrients in the small intestine, where digesta spend extended time. Schieck and Millar (1985) presented data on the weight of different sections of the gut and its contents, which can be taken as a representation of the volume of the small intestine, caecum and colon. For this chapter, the data for 11 species of the subfamily Muroidea were compiled, for which these authors also presented data on the type of diet these species generally eat (Fig. 4.89). It is evident from the ternary diagram that omnivores have a large small intestine; it represents more than 50% of the total volume. This percentage can be reached by herbivores, but most cases the small intestine represent less than 50%, but the caecum can be relatively large. In this context, it is of interest that the colon in the Muroidea is of relatively small size. In the superfamily Dipodoidea (Tullberg, 1899; Behmann, 1973), the large intestine of three species is depicted (Fig. 4.90). The great jerboa (Allactaga major) and the lesser Egyptian jerboa (Jaculus jaculus) eat a food with approximately 110 g CF/kg DM and the southern birch mouse (Sicista subtilis), a material that is of better quality and with lower crude fibre contents (~63 g CF/kg DM). According to Behmann (1973), the ileum in Allactaga major opens into a widened ampulla coli, which is not only characterised by an extended diameter but contributes to the formation of a parallel loop. Close to the right colonic flexure, another parallel loop can be formed, and at the end of the colon transversum another parallel loop can be differentiated. It has to be assumed that the first parallel loop functions together with the caecum and allows degradation of food of intermediate quality with the help of microbes. The description by Tullberg (1899) of the large intestine of Jaculus jaculus (the author speaks of Dipus aegypticus) shows similarities with the previous species (Fig. 4.90), but also specific differentiations: In the beginning, directly following the caecum, the colon forms a paracaecal loop (“Paracaecalschlinge”). After this, the colon ascendens forms two parallel loops, the first one being larger than the second. Immediately after the second parallel loop, the colon transversum begins, which then passes into the colon descendens. In Sicista subtilis (Fig. 4.90), Behmann (1973) could not find special differentiations in the simple colon, nor did he detect taeniae in the colonic wall. However, the illustration, which is adapted from a drawing presented by Behmann (1973), shows a widened region where caecum and colon

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Fig. 4.89: Relative weights of small intestine, caecum and colon (including contents), presented for 11 species of the myomorph subfamily Muroidea. Omnivores are represented by open diamonds, herbivores by black dots. Raw data from Schieck and Millar (1985).

ascendens join, forming an ampulla caecocolica. It is unclear what the functional significance of the colonic and caecal areas with extended diameter in a species which eats a food of relatively low crude fibre contents might be. Are these sections of the large intestine of importance during a “colonic separation mechanism”, as it has been described by Björnhag and Snipes (1999) not only for lagomorphs and caviomorphs, but also for Myomorpha? In this rodent order, the colon has internal differentiations. Does the ampulla caecocolica contribute to this separation? Behmann (1973) gives an instructive compilation of differentiations in the proximal colon of Myomorpha (Fig. 4.91). Comparable structures will also be described in the section on Hystricomorpha. The colonic tube can form a hairpin- or U-shaped loop (A), the branches of which are tightly coupled to each other by a mesenterial ligament. For this type of colonic differentiation, the term “parallel loop” is applied. A second type of loop is, in fact, a double or W-shaped loop (B), characterised by the fact that both loops have a parallel course. A third type of differentiation demonstrated by Behmann (1973) is the simple spiral with one turn (C). In the Myomorpha, a further differentiation can be the spiral cone with centripetal turns to the apex of the cone and centrifugal turns away from it (D). The cone is, of course, a threedimensional structure.

According to Groves (2005), the Myomorpha differentiated 326 genera, 310 of which belong to the superfamily Muroidea. This group is to be treated in the following with a few examples. In Fig. 4.92, the large intestines of seven species are depicted. In the representatives of the Arvicolinae (voles), the food is generally very rich in crude fibre, which means that this material is difficult to digest, most probably with the help of microbial symbionts. In Gymnuromys roberti from Madagascar, information on the quality of food could not be obtained; Cricetomys gambianus, the northern giant pouched rat, on the other hand, tends to be a more omnivorous feeder. Gymnuromys roberti has a voluminous caecum, which opens into a paracaecal loop of the colon, which, according to Tullberg (1899) is rather small. Two parallel loops on the right side of the abdominal cavity are differentiated, but it is not clear whether they are parts of the colon ascendens or transversum. The following colonic sections do not show remarkable differentiations. In Cricetomys gambianus, the proximal colon emerges from the ampulla caeci (Knight and Knight-Eloff, 1987) and then forms two colonic parallel loops. In the left hypogastric abdominal region of the Eurasian water vole, Arvicola amphibius, Behmann (1973) describes a voluminous ampulla caecalis, which is joined with the ampullar widening of the proximal colon. An extensive, well-developed colonic double spiral follows,

17 Myomorpha 

 217

Fig. 4.92: First illustration of the large intestine of myomorph Muroidea (caecum black). Combined from six groups of authors.

Fig. 4.90: Large intestine of myomorph Dipodoidea (caecum in black). Adapted from Tullberg (1899) and Behmann (1973).

Fig. 4.91: Differentiations of the proximal colon in Myomorpha. The arrows indicate the passage of digesta through the colon. Species are identified as follows: (A) Meriones and Micromys; (B) Reithrodontomys and Apodemus; C: Cricetulus and Napaeozapus; D: Microtus. Modified after Behmann (1973).

which has about three internal and external turns or windings. The following free section of the colon ascendens can be followed craniad to the flexura coli dextra.

It generally contains digesta pellets. The short colon transversum does not differentiate parallel loops, nor does the descending colon. In the lemming (Lemmus lemmus), the beginning of the proximal colon is the ampulla coli, which is the short wide part from the entry of the ileum to the base of the prominent colonic spiral (Sperber et al., 1983; Björnhag and Snipes, 1999). The first part of this, the inner spiral, is made up of about four windings or turns which are held together by an axial structure (Fig. 4.93). At the apex, the inner spiral is continued by the outer spiral which runs down towards the base, leaves the colonic spiral and after a short distance changes into the distal colon. The windings of the outer spiral are attached to the axial structure by fairly wide mesenteries. Two hairpin-shaped parallel loops can be differentiated in the drawing (Fig. 4.93), which was originally published by Sperber et al. (1983). Behmann (1973) writes that the colon of the lemming starts with a U-shaped ampulla coli, which proceeds into the colonic spiral, consisting of five inner and five outer turns. It is extremely well developed (“extrem entwickelt”). From the outer windings of the colonic spiral proceeds the short colon ascendens to a sharp flexura coli dextra (Fig. 4.92) in Lemmus lemmus. After this, the colon transversum forms a first parallel loop and after another 3 cm a second long hairpin-shaped parallel loop is formed. After further 2.5 cm, a third parallel loop is differentiated, which proceeds into the colon descendens.

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Apex

Ileum

Ampulla coli

Caecum

* Narrow channel of spiral turns Fig. 4.93: Longitudinal section of the colonic spiral in Lemmus lemmus. The narrow channel of spiral turns is marked by asterisks. Modified after Sperber et al. (1983).

Following Golley (1960), the small intestine in the meadow vole, Microtus pennsylvanicus, enters the caecum at a right angle and is separated from the three distinct colic loops by a short isthmus. The colon, extending from the colic loops to the anus, averages approximately 156 mm in length and is generally narrower in diameter than the small intestine. Faecal pellets are formed approximately midway between the colic loops and the anus. A taenia coli is differentiated, but not depicted in the illustration originally published by Golley (1960). In his description of the large intestine of Microtus agrestis (field vole), Snipes (1979a) speaks of the proximal colon. After spiralling around the ampulla ceci in the form of an ansa spiralis coli, this colonic section runs cranially under the corpus caeci, dorsal to the distal ileum. It crosses the midline and ascends towards the right body side making a small half loop before ascending on the right lateral body size (colon ascendens) in an arched course medial to the descending duodenum. The transverse colon crosses the body cavity from right to left under

the stomach. It descends (colon descendens) on the far left body side lateral to the caecum. The rectal portion approaches the body midline below the caecum. Fig. 4.94 presents information on the large intestine of Cricetidae (hamsters and their kin), a family of the Muroidea. Their food is of intermediate or higher quality with low content of crude fibre. For the eastern wood rat, Neotoma floridana, Tullberg (1899) mentions that the colon is larger than the small intestine; this species as an omnivore generally eats a food of intermediate quality. At its beginning, the colon forms a paracaecal loop, which can be clearly seen on his illustration. It is not clear whether two parallel loops are formed by the colon ascendens or transversum. The descending colon does not show remarkable differentiations. In another representative of the Cricetidae, Oxymycterus sp., the “Hocicudo”, according to Eisenberg and Redford (1999) and Wilson and Reeder (2005), the caecum is of approximately constant diameter and relatively short (Behmann, 1973) (Fig. 4.94). An isthmus separates it from an ampulla coli, after which a slight spiral is formed close to the flexura coli dextra (not clearly visible in the illustration originally published by Behmann, 1973). Internal oblique folds can be found in the colon transversum; the colon descendens is straight and free of these folds. This species lives mainly on invertebrates (Eisenberg and Redford, 1999). The large intestine of the common hamster (Cricetus cricetus) is depicted in an illustration, which was originally

Fig. 4.94: Second illustration of the large intestine of myomorph Muroidea (caecum black). Combined from four authors.

17 Myomorpha 

published by Bonfert (1928). Directly ventral to the opening of the ileum into the caput caeci the colon ascendens forms a spiral, the apex of which is directed caudad and dorsad. The spiral has one centripetal and one centrifugal turn or winding. From the centrifugal turn a straight section of the colon originates in cranial direction. Below the stomach it makes a sharp bend, forming a parallel loop with an apex that shows to the right side. The distal branch of this loop proceeds into the colon transversum, which also forms a short parallel loop, after which the short colon descendens begins. Snipes (1979b) studied the large intestine of the striped desert or Sungarian hamster (Phodopus sungorus). The distal ileum enters the ampulla ceci medially, close to the point of transition from the ampulla into the proximal colon, which then forms a small colonic spiral. The proximal colon courses from the caecum in the lower portion of the abdomen to the right where it forms a long loop, the arms of the loops being held together by the mesentery. The colon ascends to the level of the stomach, where it forms the colon transversum, which crosses from the right body side to the mid-abdomen and descends dorsad as colon descendens. Three of the four species depicted in Fig. 4.94 (Oxymycterus sp., Cricetus cricetus, Phodopus sungorus) have a simple colon with a small colonic spiral; all three eat a food which contains considerable amounts of animal matter and a small percentage of crude fibre contents. Six species, which are representatives of the family Muridae, are depicted in Fig. 4.95. In the illustrated species, the general architecture of the colon is very simple. For example, in the Congo forest rat, Deomys ferrugineus, the short colon begins at the very small caecum and does not show a parallel loop (Gorgas, 1967). The ventral aspect of the ampulla coli of Meriones unguiculatus (Mongolian jird) covers the caecocolical junction Snipes (1982b). The diameter of the colon is smaller than the ampulla: The colon runs to the right lateral side, making a parallel loop before ascending, lying ventral to the descending portion of the duodenum. It then runs in a transverse direction to the left. After another bend the descending colon runs slightly left and lateral to the midventral line. As a whole, the large intestine of this more omnivorous species is quite simple, especially the colon. The illustration of the colon of the piscivorous common water rat, Hydromys chrysogaster, which was originally published by Tullberg (1899), is surprisingly simple. The caecum is small and the colon shows little differentiation: It does not have a paracaecal loop, nor parallel loops (and internal oblique mucosal folds are missing). The following three illustrations in Fig. 4.95 inform about the general layout of the large intestine in two

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Fig. 4.95: Third illustration of the large intestine of myomorph Muroidea (caecum black). Combined from five publications.

laboratory rodents, the house mouse, Mus musculus, and the Norway rat, Rattus norvegicus. Snipes (1981) describes the colon of the mouse. The exit from the caecum lies ventrally on the caecum, the entry of the ileum to the caecum is dorsal to it. The colon ascendens courses directly to the right side of the body, makes a loop in the mid-dorsal abdominal area, passes to the right before going over into the transverse portion, and then descends mid-abdominally into the descending colon. No ansa spiralis coli (colonic spiral) was seen in the present material. However, Bonfert (1928) in the same species observed a loop directly on the caecum, which follows a course similar to a “W” (not discernible in Fig. 4.95). From this structure arises the short colon ascendens with a wide lumen. The remaining colon ascendens has a length of 4–5 cm. At the lower part of the arcus costalis, it proceeds into the colon transversum (1 cm), which in a slightly curved line that proceeds to the left dorsal abdominal wall and from there directly caudad as colon descendens (1.5 cm). Bonfert (1928) also mentions that the caecum of Rattus norvegicus, compared with other rodents, is small. From the caput caeca, the colon ascendens arises, which is surprisingly simple (“für einen Nager auffallend einfach”, Bonfert, 1928), only forming an S-shaped loop at its beginning. From here it runs straight upwards (9 cm) to the right costal arch, proceeds into the

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slightly bent transverse colon (7 cm), turns into the colon descendens, and ends after 6 cm in the rectum. The last illustration that will deal with the Myomorpha illustrates the large intestine in Spalacidae (Fig. 4.96). In the drawings, the voluminous caecum is obvious in all three cases. According to Tullberg (1899), the caecum of Spalax microphthalmus (Greater blind mole rat) has an internal spiral fold. A spirally formed paracaecal loop follows, which proceeds into a wide colon with a prominent right parallel loop of intermediate size. This loop is formed by the transverse colon (Behmann, 1973). A voluminous ampulla caecocolica in Spalax sp. is followed by a simple colonic spiral with two turns is formed. According to Behmann (1973), this spiral is very similar to that in Cricetus sp. (see above). The following section of the colon ascendens is short. After having passed the flexura coli dextra there is a parallel loop in the colon transversum; the descending colon is unspecialised. In the lesser blind mole rat (Spalax leucodon), the colon ascendens starts with an ansa spiralis coli with 3 to 4 turns or windings. In the illustration copied from Gorgas (1967), this spiral is not shown because the large intestine has been opened and laid out. The author notes that such a spiral is typical for Cricetinae, Gerbillinae, Muridae and Microtinae. A parallel loop follows in the colon transversum (?), and the descending colon is short and undifferentiated. The

Fig. 4.96: Fourth illustration of the large intestine of myomorph Muroidea: Spalacidae (caecum black). Combined from three authors.

colon shows two types of differentiation, namely, the ansa spiralis caeci of the ascending colon and a parallel loop in the colon transversum.

17.6 Caecum of Myomorpha 17.6.1 Muridae The Myomorpha represent the rodent suborder with a great number of publications dealing with the caecum and its function. Hebel (1969), who investigated the Norway rat, showed the extensive caecal mesentery and therefore the caecum can change its position in the abdomen. Generally, it lies to the left and caudal in the abdominal cavity. The rat caecum is of kidney shape and has an ampulla caeci (“Caecumkopf” according to Hebel, 1969) (Fig. 4.95). At this border between corpus and ampulla, the ileum enters the caecum. This situation can assure a sorting mechanism (Snipes, 1981), whereby foodstuff can pass directly from the ileum through the ampulla to the colon or be delayed in the caecum by passage from the ileum through the ampulla into the corpus ceci. The appearance of musculature in the area of the ileocaecal and caecocolical junctions acting as sphincter-like structures could conceivably aid in this directional flow. The “colon is somewhat narrowed with respect to the ampulla” (Snipes, 1981, page 459). In some cases, the ampulla narrows before gradually passing into the colon. In the opposite direction, both in rat and mouse, the corpus caeci diminishes in diameter to the apex caeci; taeniae and haustra are not present in the caecum of these two species. In both species, the entry of the ileum and the colon exit from the ampulla caeci are in close anatomical proximity, as depicted originally by Behmann (1973) (Fig. 4.63 B). According to Snipes (1981), this architectural situation of the entry and exit into and from the caecum (ampulla ceci) is seen in a large number of rodents. According to Meyer (1975), the length of the caecum in the laboratory rat is approximately 5 cm, the diameter of the organ measures about 1.5 cm in the laboratory mouse Meyer (1975) measured a caecal length of 2.9 cm and a diameter of about 0.7 cm. At weaning, i.e. at the time when milk is replaced by solid food, the caecum should be able to handle and degrade the new food material. After weaning, the mass growth of intestinal segments, including the caecum, becomes smaller (Sakata and Satoyama, 1997). The caecal wall is considerably thinner than other sections of the gut (Hebel, 1969). However, leaf-, tongueor finger-like villi were observed by Ono (1980) on the

17 Myomorpha 

caecal mucosa of rats at and shortly after birth, but after the 6th day of age, the villi gradually decreased in number and in length. The villi were not observed in rats over 10 days of age. According to Gustafsson and Maunsbach (1971) and Ishikawa et al. (1989), the caecal volume of germ-free Rattus norvegicus is four to six times as large as in conventional animals. The enlargement of the caecum is paralleled by a change in the crypts of Lieberkühn and their epithelia. It has been demonstrated that microbial inoculation rapidly reverses the caecal enlargement of germfree animals (Ishikawa et al., 1989). It is the caecum that is adapted to accommodate microorganisms (Gustafsson and Maunsbach, 1971), possibly the crypts of Lieberkühn in this organ might be the crucial structures, which are most important for symbiotic relations. Ambuhl et al. (1979) and Itano (1984) removed the caecum from the abdominal cavity of laboratory rats connecting the ileum directly with the colon ascendens. Caecectomy removes the major pool for mixing and retention of digesta in the gut distal to the stomach. Caecectomised rats had greater food intake than shamoperated rats and decrease in absorptive surface due to caecectomy is responsible for the increase in faecal water because of reduced absorption (Ambuhl et al., 1979). There was increase in faecal output in animals after caecectomy. Propulsive activities of the digestive tract without caecum are accelerated, resulting in a larger amount of contents being transferred into the colon. As a consequence of this, the size of the scybala increases (Itano, 1984). Schendel and Wissdorf (1973) write that the caecum of the Mongolian jird or gerbil (Meriones unguiculatus) is hook-shaped and subdivided organ (depicted in the second row of Fig. 4.95). The ampulla ceci is slightly dilated. The corpus ceci decreases gradually in diameter to the blind-end, the apex ceci. A half ring-fold limits the entrance to the proximal colon from the ampulla. A wideopened communication exists between the ampulla and the corpus ceci. The caecum is lined internally by a tall columnar epithelium displaying a well-developed microvillar border (Snipes, 1982b). Schendel (1972) and Schendel and Wissdorf (1973) give a description of the intraabdominal position of the caecum: It lies in the left ventral quadrant of the abdomen, craniad of the stomach. When it is intensively filled it can extend to the right side of the abdominal cavity. As has already been shown for Sciuromorpha and Castorimorpha, the caecum obtains its arterial blood from the A. mesenterica superior via 8 to 10 branches caeci in

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the mouse, but in the rat, there are four to seven branches (Snipes, 1981). According to this author, but in another publication, the caecum of Meriones unguiculatus, the gerbil, is supplied via a branch of the A.  mesenterica superior, a situation similar to most other rodents (Snipes, 1982b). Individual branches from this main artery supply the initial portion of the proximal colon, the distal ileum, the ampulla ceci, and neighbouring portion of the corpus ceci. One branch runs along the mesenteric side of the caecum to the apex, giving off smaller rami to the distal two-thirds of the corpus and apex. Infusion of volatile fatty acids into the caecum of Rattus norvegicus increased the relative weight of the mucosa and submucosa, crypt size and mitotic index in the caecum (Ishikawa and Sakata, 1997). Lange and Staaland (1970) found that sodium, potassium and water are absorbed over the course of the large intestine of the rat, including the caecum, but potassium absorption is small. The caecum of rat or mouse is populated by microbes. The mucosal surface in normal and germ-free mice does not principally differ from each other (Geissinger and Abandowitz, 1977), but Bhalla and Owen (1982) have demonstrated accelerated cell turnover and increased mucus secretion due to microbial populations. Microorganisms in the caecum may stimulate accelerated production of goblet cells. In laboratory rodents – especially in mice – the relationship between the caecum of the mammalian host and microbes has been intensively studied. “Among the viable bacteria in the digestive tract…the strictly anaerobic bacteria are the most numerous. They belong to more than 10 different genera and the number of species described increases steadily. Some of these bacteria are very sensitive to atmospheric oxygen” (Raibaud et al., 1982, page 21). According to the same authors, strictly anaerobic bacteria only appear in the mouse at weaning, in the hare they become established from the first day, whereas in the human baby, their establishment takes place immediately after that of facultatively anaerobic strains. Savage (1978) gives a clear description of the inoculation of the caecum and the large bowel in general: Oxygen-intolerant anaerobic bacteria colonise the large bowels of laboratory rodents after the tracts have been colonised by facultative and other oxygen-tolerant bacteria. The oxygen-tolerant microbes may produce end products required as nutrients by the oxygen-intolerant microbes. Another hypothesis is that the oxygen-tolerant microbes lower the oxygen tension and the oxidation-reduction potential to a level at which the oxygen-intolerant anaerobes can survive and grow. During this “succession”, oxygen-intolerant anaerobes

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colonise the epithelium of the large bowel when the animal begins to sample solid food (Savage, 1978). In addition to other aspects, Koopman et al. (1982) studied the influence of microflora on gastrointestinal parameters in Mus musculus. Less oxygen-sensitive bacteria grow rapidly and “protect” the inoculation with strict anaerobes, which are extremely sensitive to oxygen. The bacteria found in the crypts of caecal mucosa of mice are probably true symbionts. Henrikson (1973) indicates that there is a symbiotic relationship between the gastrointestinal system and some of its resident microorganisms.

17.6.2 Cricetidae, Genus Microtus In the myomorph family Cricetidae, the subfamily Arvicolinae very often eats a food rich in fibre. It can be expected that the caecum plays a considerable role in their digestive process and is morphologically differentiated. For example, in Microtus oeconomus, the root vole, “The caecum plays a special role in the digestion of high cellulose content food, that is, food peculiar to the root vole. Variations in the length and weight of this part of the alimentary tract are thus directly connected with the animal’s diet” (Gebczynska and Gebczynski, 1971, page 367). Golley (1960) writes that the caecum in the meadow vole, Microtus pennsilvanicus, “is the dominant structure of the digestive tract” (Page 92). Breton et al. (1989) corroborates this statement for the same species. According to him, the caecum has the highest mass of all four regions of the tract (stomach, small intestine, caecum, and colon). When tannins are added to the food of vole the greatest amount of digesta per body mass can be found in the caecum (Fig. 4.69). Tannins generally reduce microbial protein degradation (Püschner and Simon, 1983; OwenSmith, 2002) and depress food intake (Arnold, 1985). High-fibre diets, on the other hand, cause the caecum and large intestine of Microtus ochrogaster, the prairie vole, to increase in size (Hammond, 1993). An excellent presentation of caecal anatomy (and its arterial blood vessels) in the field vole, Microtus agrestis, was published and illustrated (Fig. 4.97) by Snipes (1979a). “The very large caecum occupies the major portion of the middle to lower abdomen. It extends in its length transversely across the abdominal cavity” (page 183). In the meadow vole, Microtus pennsilvanicus, described by Golley (1960), the caecum fills the posterior half of the abdominal cavity. The terminal portion of the organ is “tightly coiled”, but on the right body side of the field vole, the corpus bends in a caudal direction and ends in the apex, which is situated sagittally in the body cavity

(Snipes, 1979a). Following this author, the corpus caeci is slightly sagittally placed and, close to its caudal end, has an ‘S’-shaped segment. Following the ampullar end of the caecum lies the ansa spiralis coli. “The inner coil of the ansa spiralis is the extension of the ampulla ceci, the distally running proximal colon being coiled around it for two turns” (Snipes, 1979a, page 183). That author revealed that the caecum of the vole forms a spiral fold in the corpus ceci of M. agrestis, the field vole. For the field vole, Golley (1960) describes internal caecal folds, into which the stratum circulare of the tunica muscularis continues, deloping plicae circulares which can be branched. According to Golley (1960), the outer muscle layer may be expanded to form taeniae, which are neither mentioned nor depicted by Snipes (1979a) for the field vole. He mentions that the mucosa covering the caecal wall possesses short, wide-opened crypts and fine structural observations suggest the caecal epithelium to be capable of active absorption. It has already been mentioned above that the caecum and colon play an important role in coprophagy, which helps to handle a food rich in fibre. For example, Lee and Houston (1993) studied Arvicola amphibius (water vole), Microtus agrestis (field vole) and Myodes glareolus (bank vole). Digestive efficiencies in voles can reach 70%, which is very high because coprophagy provides voles with the advantage of microbial symbionts in the caecum to assist with cellulose breakdown because the products of this fermentation can pass through the stomach and small intestine. It is a surprising fact that the mean retention of food in the gut of bank voles (Myodes [Clethrionomys] glareolus) is the same for animals on a seed or leaf diet. This species is able to adapt the length of its digestive tract

Fig. 4.97: Outline and arterial supply of the caecum of Microtus agrestis. Adapted from Snipes (1979a).

17 Myomorpha 

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to the type of food. When they are feeding on a leaf diet rather than of seeds, they have a longer gut and eat more food, but they also recycle more faeces, which they have to subject to coprophagy (Lee and Houston, 1993). Probably because of active coprophagy the nitrogen-fixing activity in the caecum of Microtus arvalis (“rossiae-meridionalis” in the paper of Meshcherskii et al., 2004) was three times that in the stomach.

17.6.3 Cricetidae, Genus Ondatra Landry (1970) considered the Rodentia to be omnivores. In the muskrat, Ondatra zibethicus, Campbell and MacArthur (1996b) demonstrated that meat of fish and of mammal cadavers is eaten. The authors believe that the consumption of animal matter plays a role in nitrogen metabolism of muskrats and might be more widely spread than was previously thought. Bisaillon et al. (1988) depicts the caecum of the muskrat (Fig. 4.98). It is a wide bag-like blindsac, a caecum amplius according to Kostanecki (1926) and on one side is fixed by the ligamentum caecocolicum (Luppa, 1961); according to that author, the tip or apex of the caecum is spirally curved and there is a band of longitudinal muscles on the mesenterial side (the ligamentum caecocolicum), forming the taenia obtecta, as well as a taenia libera on the antimesenterial side (Luppa, 1961). The caecum has a wide connecting area towards the colon, the capud caeci, but a widened ampulla coli cannot be distinguished. The first part of the colon ascendens is coiled and forms the ansa spiralis coli. According to Luppa (1961), the internal loops have a wide lumen and run centripetally to the apex of the spiral, whereas the external narrow coils have a centrifugal course. The apex of this pyramid of coils is pointed caudodorsally (Luppa, 1961). The tunica mucosa of the caecum of Ondatra zibethicus has crypts which are also called caecal glands. In the middle part of these crypts, a considerable number of goblet cells can be found in higher number than in the neck of the crypts. The superficial cells on the surface show microvilli (Luppa, 1961), which indicate an absorptive function of the caecal wall. Bisaillon et al. (1988) give information on the arterial supply of the caecum of the muskrat. The ramus caecalis and the ramus colicus are terminal branches of the A. ileocolica. The ramus caecalis extends to the apex of the caecum and on its way many collaterals branch off to the caecum. Some of these branches anastomose and form arcades. Virgil and Messier (1992) studied the ontogeny of the muskrat digestive tract. During the preweaning period

Fig. 4.98: The caecum of the muskrat, Ondatra zibethiscus. Adapted from Bisaillon et al. (1988).

caecum mass, as well as the total gut mass, increased more rapidly than body mass, but after weaning the growth rate of the digestive tract decreased. The authors speculate that the relatively large proportion of digestive tract tissue (caecum and intestine) at weaning probably enables plant cell material to be effectively processed by increasing both fermentation capacity and absorptive surface area.

17.6.4 Caecum of Myomorpha, Cricetidae, Genus Mesocricetus The caecum of Mesocricetus auratus, the golden hamster (Fig. 4.99), may play a more important role in food utilisation than the stomach, especially when a high-fibre diet is eaten (Sakaguchi et al., 1981). The caecum contributes to the energy metabolism in the hamster given a diet rich in fibre. Microbial protein synthesised in the large intestine may be utilised by coprophagy. Considerable amounts of microbial protein must be synthesised in the caecum amplius with a rounded apex. An externally clearly separated ampulla coli can be seen on the left aspect of the caecum in Fig. 4.99 A. In addition, the two figures identify the arterial supply of the caecum. The A. ileocaecocolica is an end branch of the A.  mesenterica cranialis and proceeds itself towards the apex of the caecum giving branches towards the organ.

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 IV Euarchontoglires – 17 Myomorpha

Fig. 4.99: Left (A) and right (B) sides of the caecum in Misocricetus auratus with arterial supply. Adapted from Schwarze und Michel (1957).

17.6.5 Caecum of Myomorpha, Cricetidae, diverse genera Captive water voles, Arvicola amphibius, that were fed high-fibre diets, had significantly longer and heavier digestive tracts – especially the caecum – than voles fed a low-fibre diet (Woodall, 1989). Also in the North American deermouse, Peromyscus maniculatus, an omnivore feeding on particulate foods like seeds and insects (Green and Millar, 1987) increasing dietary cellulose increased the weight of the caecum relative to wild, naturally fed animals, when food quality of the deermouse was decreased by adding powdered cellulose to the food (Fig. 4.100). The Eurasian water vole, Arvicola amphibius, responded to enhanced energy needs by retaining more ingesta in the caecum (Woodall, 1989); the material from the caecum and colon was reingested during coprophagy and the frequency of this reingestion increased significantly in animals on a high-fibre diet (Woodall, 1989).

A careful description, together with illustrations of the caecum of the dwarf hamster, Phodopus sungorus, has been published by Snipes (1979b). The caecum can be divided into an ampulla caeci, ‘a small bulbous segment into which the ileum enters and from which the proximal colon emerges” (page 230) in an ileocaecal orifice, which is surrounded by a fold. This fold cannot be seen in Fig. 4.101 and is different from the situation in Mesocricetus auratus (Fig. 4.99). The ampulla caeci of Snipes (1979b) seems to be homologous with the ampulla coli of Schwarze and Michel (1957). The second part is the corpus ceci (Fig. 4.101), “the much larger and more voluminous portion of the caecum which extends from the ampulla to its blind end (apex ceci). The corpus is mostly of equal diameter from the ampullar end to the apex and shows nonpermanent strictures of its wall” (Snipes, 1979b, page 230/1). Sperber et al. (1983) supplied an outline illustration of the caecum of the Norway lemming, Lemmus lemmus

Fig. 4.100: Relative weight increase of small intestine, caecum or colon in Peromyscus maniculatus under the influence of addition of powdered cellulose that decreases food quality. Raw data are from Green and Millar (1987).

Fig. 4.101: The caecum and its arterial supply in Phodopus sungorus. Adapted from Snipes (1979b).

17 Myomorpha 

(Fig. 4.102). The proximal colon of this species is able to separate most of the bacteria in the colonic contents from the food residues and returns bacteria back to the caecum. The indigestible parts of the food pass the colon rapidly, whereas the digestible material, such as the bacteria, are retained in the caecum, which shows higher nitrogen concentration than both stomach and distal colon. On the other hand, it should be kept in mind that a post-caecal colonic spiral (ansa spiralis caeci) can be found in the lemming and could be in important section of the digestive tract for important metabolic functions, such as absorptive processes (Lange and Staaland, 1970). Voge and Bern (1949) present information on two species of the cricetid subfamily Arvicolinae the red tree vole (Arborimus longicadatus) and Palaearctic collared lemming, Dicrostonyx torquatus (Voge and Bern, 1955). Both species have villus-like filaments in the caecum. Structurally and functionally these filaments in Arborimus basically resemble villi of the small intestine, and the absorptive surface of the caecum is greatly increased by their presence (Voge and Bern, 1949). In Dicrostonyx, these villi show an occasional occurrence of branching (Voge and Bern, 1955). 17.6.6 Caecum of Myomorpha, Spalacidae and Nesomyidae A very interesting caecum has been described and was depicted by Snipes et al. (1990) (Fig. 4.103). These authors studied the Middle East blind mole rat, Spalax ehrenbergi, which has a voluminous caecum, most probably with fermentation-vat function. A spiral fold, the position of which can be seen from outside, runs through the entire caecum and is based on a fold of the tunica muscularis. This spiral fold increases the surface area of the caecum by a factor of two-fold. A representative of the myomorph family Nesomyidae, is the white-tailed rat, Mystromys albicaudatus. According

 225

Fig. 4.103: Outline of the caecum of Spalax ehrenbergi. Adapted from Snipes et al. (1990).

to Mahida and Perrin (1994), this species is essentially a hindgut fermenter; the VFA content of the caecum is greater than in the forestomach. Knight and Knight-Eloff (1987) investigated the digestive tract of another species of the Nesomyidae, the African giant rat, Cricetomys gambianus (Fig. 4.104). Their ampulla caeci and the ampulla coli of Schwarze and Michel (1957) seem to be homologous structures, but further investigations are necessary. “The ampulla ceci, into which the ileum enters and from which the corpus ceci and proximal colon exit, appears to act as a sorting chamber for digesta directing it in either direction. The several folds, in association with the ileocaecal orifice and ampulla ceci, conceivably aid in directing or restraining this flow of digesta” (page 19, Knight and Knight-Eloff, 1987). In their comments on the caecal tunica mucosa, they write that the “caecal mucosal form differs from the rest of the intestine. The open crypts are thought to enhance absorption through enlargement of the surface area” (Snipes, 1979b), “while the fewer goblet cells correlate with the lack of intestinal content flow and abrasion” (page 20). 17.6.7 Concluding remarks on caecal digestion The species ingesting a high quality material, namely, seeds, insects, fruits or acorns, are characterised by a colon and caecum with low internal surface. In the two myomorph

Colon

Caecum Ampulla coli

Fig. 4.102: Outline of caecum and ansa coli in Lemmus lemmus. Adapted from Sperber et al. (1983).

Fig. 4.104: Outline of the caecum and proximal colon in Cricetomys gambianus. Modified from Knight and Knight-Eloff (1987).

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 IV Euarchontoglires – 18 Anomaluromorpha

Fig. 4.105: The amount of sodium, potassium and water absorption in the lumen of caecum and distal colon in the Norway lemming (Lemmus lemmus) and the brown rat (Rattus norvegicus). Raw data are from Lange and Staaland (1970).

species, the Norway lemming (Lemmus lemmus) and the brown rat (Rattus norvegicus), Lange and Staaland (1970) present direct data on the functional importance of the caecum within the large intestine. In both species, sodium, potassium and water are absorbed over the course of the large intestine, but mainly in the caecum (Fig. 4.105).

18 Anomaluromorpha 18.1 General remarks Anomaluromorpha containing four genera and nine species in two families, the Anomaluridae (Flying squirrels, Anomalurus, Idiurus, Zenkerella) (Kingdon, 1974b; Dieterlen, 2005b) and Pedetidae (Spring hare, Pedetes) (Kingdon, 1974b; Dieterlen, 2005c), but according to Honeycutt (2009), their placement is not yet well resolved. Romanenko et al. (2012) write that the evidence for the recognition of Anomaluromorpha is not really persuasive. The taxon is poorly studied at a chromosomal level, but Anomaluromorpha, together with Hystricomorpha, Myomorpha and Castorimorpha, form a single clade, separated from the Sciuromorpha. This view had already been indicated by Adkins et al. (2003). Montgelard et al. (2008) state that the suborder Anomaluromorpha forms a “monophyletic assemblage” together with Myomorpha and Castorimorpha. Gorgas (1967) and Kingdon (1974b) mention that the food of Anamalurus derbianus (Lord Derby’s scaly tailed squirrel) is composed of bark, soft wood and fruit, but also of flowers, leaves, green nuts, other unripe fruits and insects. However, records of the feeding behaviour of anomalures are rare (Julliot et al., 1998). Idiurus zenkeri (pygmy scaly tailed flying squirrel) eats a more nutritious food and is mainly frugivorous; it feeds on fruits, nuts and insects. Feeding observations of Julliot et al. (1998)

demonstrated bark peeling and ingestion of phloem sap. They observed that sap flow sites were also used by insects and could be revisited by anomalures to eat these insects together with the sap. The great amount of insects found in the stomach of Anomalurus derbyanus suggests that insects were probably actively hunted and not just eaten opportunistically. As a representative of the family Pedetidae the South African spring hare, Pedetes capensis, feeds on stems, roots and storage bases of grasses (Gorgas, 1967; Kingdon, 1974b), as well as on new sprouts, foliage, herbs, fruits and insects, Skinner and Chimimba (2005) call Pedetes capensis a “grazers” that utilises at least 20 plant species.

18.2 Gastric anatomy of the Anomaluromorpha In her study on systematics and biography of anomalurids Schunke (2005) mentions the visceral anatomy of these animals just in passing and refers to an old study of Alston (1875) without going into further detail. It was Tullberg (1899) who published gastric outlines and some length measurements, but no further morphological details (Fig. 4.106). According to that author, Pedetes caffer, the South African spring hare, has a “rounded” stomach and the fundus gastricus is not prominent; the length of the organ is 100 mm. The oesophagus in this species extends into the gastric lumen with a short, round valva oesophagea (Gorgas, 1967) and a constriction in the middle section makes the stomach bilocular. However, the incisura angularis does not extend over the whole gastric wall, down to the curvatura major. Contrary to the statement of Tullberg (1899), the fundus gastricus, according to Gorgas (1967), has a voluminous blindsac and reduces its circumference towards the corpus gastricum. After a constriction between the angulus and the greater curvature, the gastric

18 Anomaluromorpha 

 227

Fig. 4.106: Outlines of the stomachs of two species of Anomaluromorpha. Adapted from Tullberg (1899).

lumen widens and forms the antrum pyloricum, which reduces its circumference towards the pylorus. A clear pyloric valve can be found before the duodenum. In addition to the above family Pedetidae, Tullberg (1899) describes the stomach of Anomalurus peli (Pel’s scaly tailed squirrel) as “rather lengthened” with a length of 90 mm; in A.  beechcrofti (Beechcroft’s scaly tailed squirrel) the length of the stomach is 95 mm in males. In his impressive study on the comparative anatomy of the digestive tract in rodents, Gorgas (1967) deals with Anomalurus derbianus (he writes A. fraseri) (Lord Derby’s scaly tailed squirrel). In this species, the stomach is baglike and dilated and the fundus gastricus very prominent. The antrum pyloricum is short and separated from the bulbus duodeni by a constriction. In another anomalurid rodent, Idiurus macrotis (long-eared scaly tailed flying squirrel), the fundus gastricus forms a voluminous blindsac, the pars pylorica is short and ends at a circular fold. On the internal lining of the stomach, Gorgas (1967) comments that it is smooth; no further details on characters of mucosa or epithelium are given. At the cardia, the oesophagus has an oval valva oesophagea. The total length of the stomach is 16 mm.

18.3 Small intestine of Anomaluromorpha On this section of the intestinal tract of flying squirrels and spring hare, no information is available.

18.4 Colon of Anomaluromorpha Tullberg (1899) demonstrated that the proximal colon of Beechcroft’s scaly tailed squirrel (Anomalurus beechcrofti) is fixed to the curved caecum with a mesentery. It forms a prominent parallel loop (Fig. 4.107). This author refers to Anomalurus pelii in his description of A.  beechcrofti,

Fig. 4.107: Large intestine of Anomaluromorpha. Caecum black, colon grey. Adapted from Tullberg (1899).

indicating a great similarity between the large intestines of both species. A valvula coli separates this section of the gut from the caecum and ileum. The colon ascendens forms a parallel loop. Transverse and descending colon have a long mesentery, but special differentiations could not be found. The most proximal section of the ascending colon is fixed to the caecum and its following free section forms two parallel loops. The following transverse colon also forms a small parallel loop, but cannot be clearly identified in Pedetes capensis. The descending colon lies slightly to the left of the vertebrate column.

18.5 Caecum of Anomaluromorpha The caecum of the spring hare (according to Mills and Hes, 1997; Skinner and Chimimba, 2005, Pedetes capensis) is very voluminous and the beginning of the caecum has a valvula coli, similar to that in Anomalurus sp. (Tullberg, 1899). This author depicts the total digestive tracts of Anomalurus beechcrofti (Fig. 4.107). The caecum of this species does not have taeniae. According to Gorgas (1967), it is extraordinarily long and slender. It has a spiral shape and becomes longer towards the apex. It lies in the middle section of the hypogastrium. A short ligamentum ileocaecale connects the corpus caeci with the ileum (not depicted in Fig. 4.107). The apex caeci of Anomalurus beechcrofti is bent backwards (hairpin-like) and is free of the mesentery. Interestingly, spiral folds can be found in anomaluromorphs (Gorgas, 1967); Anomalurus sp. has an internal spiral fold and is thus comparable to Spalax ehrenbergi (Snipes et al., 1990) (Myomorpha) and lagomorphs. In Anomalurus beechcrofti, the valva spiralis caeci has about 19 windings and a height of 3 to 10 mm.

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 IV Euarchontoglires – 19 Hystricomorpha

Tullberg (1893) mentions and depicts a caecal spiral fold also for Anomalurus pelii (Pel’s scaly tailed squirrel). In the long-eared scaly tailed flying squirrel, Idiurus macrotis, the long-eared scaly tailed flying squirrel, Gorgas (1967) found a caecum without taeniae, but with a valva spiralis caeci that has about 10 windings, as well as a fold partly separating ileum and caecum, the valva ileocaecalis. The caecum forms a spiral-shaped structure and lies caudally in the left dorsal part of the abdominal cavity. As chitinous insect exoskeletons could be found in the stomach and in the caecum of Idiurus macrotis, Gorgas (1967) speculates that the food might have a higher content of insects than of plant material, but in a related species, Idiurus zenkeri, pygmy scaly tail flying squirrel, this species eats the pulp of oil-palm fruits, as well as nuts and traces of insects. For the second family of the suborder Anomaluromorpha, Pedetidae (Dieterlen, 2005c), very little anatomical information on the caecum is available. As a medium-sized mammal, the spring hare, Pedetes capensis is small enough to exploit nutritious, short, sparse grasses (Butynski, 1997). A minimum of 20 plant species is utilised in Northern Cape Province (Skinner and Chimimba, 2005). Eight grass species contributed 76% of the diet. Seeds of grasses, green grass stems, leaves, bulbs, roots and rhizomes are dug from the ground or new sprouts, foliage, herbs and fruits are taken from the surface (Kingdon, 1974). Fig. 4.107 presents an illustration of the digestive tract of Pedetes capensis, based on a drawing published by Tullberg (1893). This author mentions that the caecum is very wide and does not have a spiral fold, but a valvula coli can be found at the entrance of the caecum. According to Gorgas (1967), the caecum in Pedetes capensis is much more voluminous that in Anomalurus sp. and he agrees with Tullberg (1893) that this species does not have a valvula spiralis caeci.

19 Hystricomorpha 19.1 General remarks The order Rodentia (Cao et al., 1994, deBry and Sagel, 2001) is clearly monophyletic. Rodents originated around 61.7–62.4 Ma, shortly after the Cretaceous/Paleogene boundary, and diversified around 57.7–58.9 Ma (Wu et al. (2012). The first suborder separating from the other rodents were the Hystricomorpha. They comprise two infraorders, the Ctenodactylomorphi with only four genera and five species, as well as the Hystricognathi with 73 genera and 285 species (Wilson and Reeder, 2005).

Three main branches of rodents were differentiated by Churakov et al. (2010), namely, a “mouse-related clade”, including Myomorpha, Anomaluromorpha and Castorimorpha and the “squirrel-related clade” or Sciuromorpha; both clades have already been dealt with in previous sections. The third clade Ctenohystrica (Wilson and Reeder, 2005, write “Ctenohystricha”, page 1538) represents a taxonomic group uniting the two infraorders Ctenodactylomorphi and Hystricognathi (Huchon et al., 2002). An interesting map, published by Fabre at al. (2012), showed highest species richness of Hystricognathi in South America, especially in Amazonia and in the Atlantic coastal forests of Brazil. Practically the whole continent is occupied by them with the exception of the western deserts along the Pacific coast. On the other hand, the Ctenodactylidae can be found in northern Africa and Sub-Saharan Africa. The Palaearctic and most of the Nearctic regions, Arabia, Madagascar, New Guinea, New Zealand and Australia are not settled by Ctenohystrica. Mares and Ojeda (1982) present maps illustrating the geographical distribution of 122 species in the infraorder Hystricognathi, forming a very diverse rodent fauna on the South American continent (Alho, 1982). The distribution of the suborder Hystricomorpha in southern Africa is depicted by maps in Skinner and Chimimba (2005). Kingdon (1974b) informs about hystricomorph distribution in East and Central Africa. As has been demonstrated by Fabre et al. (2012), the number of hystricomorph rodents living in regions other than South America and South Africa, is small. For North America one species, the North American porcupine, Erethizon dorsatum, is documented (Banfield, 1981; Kays and Wilson, 2002); for the Near East Qumsiyeh (1996) mentions the Indian crested porcupine, Hystrix indica, which is also listed for the Indian subcontinent by Gurung and Singh (1996), together with Hystrix brachyura, the Malayan porcupine. Sheng et al. (1999) mention this latter porcupine species for southern China, as well as the Asiatic brush-tailed porcupine, Atherurus macrourus.

19.2 Form and function of the gastric region in Hystricomorpha As the Hystricomorpha – generally speaking – can be classified as colon or/and caecum fermenters, the anatomy of the stomach has not found as much attention as, for example, in the Myomorpha. Fleischmann (1891)

19 Hystricomorpha 

characterised the stomach as a simple organ, which is pouch-shaped. In the following, the present author will first deal briefly with the Ctenodactylidae of northern Africa, followed by the discussion of African, American and Carribean Hystricognathi. It will soon become obvious that the material available for different species is extremely unbalanced in quantity and quality.

19.2.1 Infraorder: Ctenodactylomorphi 19.2.1.1 Family: Ctenodactylidae In his still important paper on rodent taxonomy, Tullberg (1899) publishes an outline of the stomach of Ctenodactylus gundi, the common gundi (Fig. 4.108 A and B), which, according to Gorgas (1967), is unilocular and has a fundus gastricus, which is not prominent. The latter author gives a total length of the organ of 63 mm. Gorgas (1967) mentions that squamous gastric epithelium is not differentiated in Ctenodactylus gundi, i.e. the stomach is glandular, not hemiglandular, as in many Myomorpha.

Fig. 4.108: Outlines of the stomachs in four families of Hystricomorpha. Adapted from different authors.

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19.2.2 Infraorder: Hystricognathi African and Eurasian hystricognath families 19.2.2.1 Family: Bathyergidae 19.2.2.1.1 Food of some bathyergid species In their book on the Southern African mammal fauna, Skinner and Chimimba (2005) comment on nutritional characteristics of Bathyergidae. For Bathyergus suillus, Cape dune mole rat, they even apply a superlative, calling its diet the “most catholic vegetarian…of all species” (page 82). Roots, bulbs, green forbs and grass and independence of water characterise this species. According to Bennett et al. (2009), 60% of the diet of this species consists of above-ground herbs, grasses, sedges; bulbs, corms and tubers are also eaten. Interestingly, glycosides, which can be found in the food of the Cape dune mole rat, are not toxic to Bathyergus suillus, but to other mammals. Another species of this genus, the Namaqua dune mole rat, B. janetta, eats subterranean plant storage organs and pulls above-ground vegetation underground (Skinner and Chimimba, 2005). These authors also inform about the food characteristic of three species of Cryptomys: C. hottentotus, Southern African mole rat, C.  darlingi, Mashona mole rat and C.  damarensis, Damaraland mole rat. All three live on succulent underground parts of plants, such as fleshy roots, bulbs, tubers and succulent underground stolons of grasses. For the Damaraland mole rat, Bennett and Jarvis (2004) mention that the diet includes various species of Curcubitaceae. As has already been mentioned above for Bathyergus suillus, some of the underground reserve organs are toxic to other mammals, but not to Cryptomys damarensis. The Cape mole rat, Georychus capensis, eats plant storage organs, such as bulbs, corms and tubers (Bennett et al., 2006) and about 6% of the stomach contents consist of above-ground plant parts (Skinner and Chimimba, 2005). 19.2.2.1.2 Remarks on the gastric anatomy of some bathyergid species In a detailed study on the comparative anatomy of the abdominal digestive tract, Kotzé et al. (2010) treat six species of bathyergids, most of them already mentioned in the above lines: Bathyergus suillus, Cryptomys hottentotus, C.  damarensis and C.  mechowi, as well as Georychus capensis and Heterocehalus glaber. Kotzé et al. (2010) show in a graph that the stomach contributes only a quarter of the surface to the total gastrointestinal tract. The organ is depicted as an outline illustration for Georychus sp. (Fig. 4.109) by Tullberg (1899); in G. capensis,

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 IV Euarchontoglires – 19 Hystricomorpha 19.2.2.2 Family: Hystricidae

Fig. 4.109: Outlines and mucosal lining in three genera of the hystricognath family Bathergidae. Adapted from Tullberg (1899) and Gorgas (1967).

the stomach has a length of 33 to 53 mm (Gorgas, 1967). For Bocage’s mole rat (Cryptomys bocagai), that author mentions of the unilocular stomach (length 53–59 mm) that a prominent fundus (fornix) gastricus is differentiated. On the other hand, the unilocular stomach of the silvery mole rat, Heliophobius argenteocinereus, has a rounded fundus gastricus and the pars pylorica is of conical shape; length of whole organ 56–57 mm (Gorgas, 1967). Only very few remarks have been made on the mucosal lining of the stomach in Bathyergidae. In the stomachs of two species, as depicted by Vorontsov (1960, 1967/1979), Georychus capensis and Heliophobius argentocinereus (Vorontsov writes Myoscalops argenteus), the tunica mucosa is exclusively glandular. However, that author also presents an illustration of the stomach in Cryptomys damarensis, which has a fornix gastricus covered with cornified epithelium and villi. “Apparently the function of this portion consists of trapping the soil particles entering the stomach along with food,…” (page 224 and Figure 122 of the English translation of Vorontsov, 1967/1979). The digestion coefficient for bulbs, corms and tubers in Cryptomys damarensis amounts to values between 85 and 95% (Bennett and Jarvis, 2004). This value can probably be reached because coprophagy is practised by bathyergids, for example, in the naked mole rat, Heterocephalus glaber (Jarvis and Sherman, 2002), which eats a lowquality, high-fibre diet. Symbiotic microorganisms are active in an enlarged caecum.

19.2.2.2.1 Remarks on the gastric anatomy of some hystricid species, combined with short notes on food Describing Hystrix africaeaustralis, Barthelmess (2006) stated that the glandular unilocular stomach is relatively large for a herbivorous rodent, mean maximum volume 1.019 cm3. This value can also be found in the paper of van Jaarsveld (1983). The Cape porcupine is predominantly vegetarian, it eats bulbs, tubers, roots and is characterised by “catholic dietary habits” (Skinner and Chimimba, 2005). Most of the published information on the hystricid stomach is based on species belonging to the genus Hystrix. Gorgas (1967) was able to study Atherurus macrurus, the Asiatic brush-tailed porcupine, but mentions that the stomach is similar to that of Hystrix. In that species, the tunica mucosa at the pylorus is thickened and the organ has a length of 105 mm. Both Tullberg (1899) and Gorgas (1967) present drawings of the crested porcupine stomach (Hystrix cristata) (Fig. 4.110 A and B). Both authors show a prominent fornix gastricus and a surprisingly voluminous distal zone of the stomach, formed by the corpus gastricum together with the pars pylorica. All gastric sections form a continuous cavity (Gorgas, 1967) in that species and the length of the stomach is 175 mm. A circular

Fig. 4.110: Outlines of stomachs in hystricomorph families Hystricidae, Erethizontidae, Octodontidae. Adapted from: Tullberg (1899) (A); Gorgas (1967), (B, E); Van Jaarsveld (1983) (C); Vispo and Hume (1995) (D).

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pyloric fold separates stomach from ampulla duodeni. No cornified epithelium is present in the stomach of the crested porcupine. In Hystric africaeaustralis, a simple, glandular, unilocular stomach (Fig. 4.110 C) with a thickened tunica muscularis in the pars pylorica can be found. When van Jaarsveld and Knight-Eloff (1984) compared all layers between the corpus gastricum and the pars pylorica, only the three muscular sheets, the lamina muscularis mucosae, stratum circulare and stratum longitudinale, increase drastically in aborad direction, i.e. towards the pylorus. This is especially true for the stratum circulare, which indicates that the pars pylorica is the gastric region that regulates digesta transport into the duodenum. 19.2.2.2.2 Arterial supply of the stomach of Hystrix cristata Anatomical data on the stomach and surrounding organs in Hystricomorpha are often limited. Because of this deficiency it is very much appreciated that Atalar and Yilmaz (2004) published a description – with illustrations – of the branches of the coeliac artery in the crested porcupine, Hystrix cristata. The information they present does not elucidate the arterial supply uncontroversially. For example, they write that the A.  gastrica dextra as first branch of the A. hepatica “disposed to the facies parietalis of the cardia ventriculi” (page 53). However, their illustration of the parietal aspect of the stomach shows clearly that the vessel they call A. gastrica dextra runs to the anatomical left and is, in fact, the A.  gastrica sinistra. This latter interpretation is in accordance with results of comparative investigations, for example, with information on the human distal oesophagus, as supplied by Lippert and Pabst (1985). These authors write: “The abdominal part of the oesophagus is supplied by 2–3 branches from the left gastric artery” (page 17). Keeping these aspects in mind, the present author produced a schematic diagram (Fig. 4.111) of the arterial supply of the Hystrix stomach, which is based on a figure of Atalar and Yilmaz (2004). There are two main branches of the aorta abdominalis and the situation considered to be “normal” in humans with three branches (A. gastrica sinistra, A. splenica and A. hepatica communis, all three forming the Tripus Halleri, Lippert and Pabst, 1985), was not present in the crested porcupine. 19.2.2.3 Family: Petromuridae This family contains only one species, Petromus typicus, the dassie rat. This species eats a highly variable plant diet

Fig. 4.111: Arterial supply of the stomach in Hystric cristata. Adapted from Atalar and Yilmaz (2004).

(Skinner and Chimimba, 2005). Hypsodont cheek teeth are adaptations to chew lignified grasses, but leaves of dicotyledons and wild cucumbers are also relished. Rathbun and Rathbun (2005) state that dassie rats in Namibia feed on a wide variety of plants with a preference for fresh leaves and stems, fruits, and flowers and avoid relatively few plants and plant parts. According to George (1981), the stomach of Petromus typicus is simple; the diet consists of shrubs and herbs. Mess and Ade (2005) go into more detail and a short passage will be cited verbally: “The stomach is…markedly curved, almost U-shaped. It has no transversally-running folds or septa producing proventriculus-like structures without glands as, e.g. in murids…There is a continuous layer of glands present as judged from gross morphological analysis” (page 47) (Fig. 4.112). 19.2.2.4 Family: Thryonomyidae In this small hystricomorph family, there are just two species, Thryonomys gregorianus and T.  swiderianus. All information presented here is from Thryonomys swinderianus, the greater cane rat. It is a herbivorous species, eating roots, shoots, stems of grasses, and reeds (Skinner and Chimimba, 2005), i.e. a food of low quality. Efficiency of digestion of low-fibre diets may be ascribed to changes in large intestinal capacity (van Zyl et al., 1999). However, this needs further investigation as little is known of the mechanisms involved in fibre digestion in cane rats.

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Fig. 4.112: A photo of the opened stomach of Petromus typicus. The oesophagus had been resected and its course is indicated by the right arrow. Adapted from Mess and Ade (2005).

Coprophagy is practised by greater cane rats, as van Zyl and Delport (2010) mention. This process increases the digestibility of food as seen in the higher protein concentration and energy content in the soft faeces, which are swallowed into the stomach. This organ is unilocular and glandular in Thryonomys swinderianus (Fig. 4.108 C). The incisura angularis is shallow and the fornix gastricus prominent (van Zyl et al., 2005). American hystricognath families 19.2.2.5 Family: Erethizontidae This family has 5 genera and 16 species; the genera Chaetomys, Echinoprocta and Erethizon are monospecific; Sphiggurus, has nine species. Coendu, on the other hand, comprises four species (Wilson and Reeder, 2005). However, the numbers for Iberoamerican species, given by other authors, are variable (Woods, 1982, Mares and Ojeda, 1982) and a statement of Mares and Ojeda (1982) should be kept in mind: A taxonomic

scheme is, at best, only an approximation of reality (page 394). The thumb in the hystricomorph family Erethizontidae is replaced by a broad movable pad, and the sole of the hind foot is wide. According to Eisenberg and Redford (1999), this demonstrates adaptation for an arboreal life. For example, Echinoprocta rufescens, the stump-tailed porcupine of the mountain areas of Columbia, is arboreal, as Delgado and Tirira (2008) write. Generally speaking, all porcupines are at least partly arboreal, and they variously eat fruit, nuts, leaves, and bark (Simpson, 1980). Smythe (1986) writes (page 174): “The ancestors of the New World hystricomorph rodents reached South America in the Eocene or early Oligocene and underwent a rapid adaptive radiation, spreading into diverse niches in South America. In the late Pleistocene or more recently, they spread through Middle America to North America. Only one genus has survived in nontropical North America: Erethizon”. Presently, Erethizontidae are distributed from northern Canada south to northern Argentina (Redford and Eisenberg, 1992). The South American species are mostly less spiny than the North American porcupine. One species of the New World porcupines survived in North America, Erethizon dorsatum, and it is still widely present there (Simpson, 1980). Banfield (1981) presents information about the food of porcupines during different seasons: In summer, porcupine food in Canada consists of a wide variety of lush green leaves of forbs, shrubs, and trees, such as aspen and white birch. In winter, they feed on the cambium layer and inner bark of trees as well as on the new twigs and buds and in spring they eat the unfolding poplar and basswood leaves. Different species of the genus Sphiggurus (dwarf porcupines) feed on fruit, ant pupae, vegetables and roots in Suriname (Redford and Eisenberg, 1992; Leite and Patterson, 2008). According to Eisenberg (1989), this genus has a distribution from Mexico south over the Isthmus of Panama across much of northern South America into Amazonian Brazil. The poorly known Chaetomys subspinosus, the thin-spined porcupine, eats, according to DeSouto Lima et al. (2010), a diet consisting of leaves for more than 70%, followed by flowers and fruits. Chaetomys is a folivore and highly selective (Fernandez Giné et al., 2010), perhaps the most folivorous amongst the Erethizontidae. Acording to these latter authors the food contains high levels of protein and fibre and symbiotic nitrogen-fixing bacteria are established, not in the simple and unilocular small stomach, but in the large intestine. The unilocular stomach of the Erethizontidae has the shape of a hook (Fig. 4.110 D) because of a strong bend

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between the fundus gastricus and the corpus gastricum plus pars pylorica (Gorgas, 1967) in Erethizon dorsatum and Coendu prehensilis. Vispo and Hume (1995) speak of a horn-shaped organ. Its wet contents of digesta amounts to 167 g or 17% of the total tract mass. In the North American porcupine, a circular pyloric fold separates the stomach from the ampulla duodeni and the length of the stomach reaches 160 mm, in Coendu prehensilis, the stomach has a length of 180 mm. The total length of the gut in Erethizon dorsatum amounts to 8.5 m (Woods, 1973). This species does not practise coprophagy.

19.2.2.6 Family: Chinchillidae Under reference to the taxonomy used by Wilson and Reeder (2005), three genera have to be attributed to the Chinchillidae: Chinchilla (2 species), Lagidium (3) and Lagostomus (2). Because of its fine pelt, species of the genus Chinchilla have been ruthlessly hunted and caught. The overexploitation ended in the extinction of C.  chinchilla, the short-tailed chinchilla in many areas (Jiménez, 1996). It is now bred in captivity (D’elia and Ojeda, 2008). Chinchilla lanigera, the long-tailed chinchilla, is now vulnerable. Despite current protection measures, populations in Chile are continuing to decline (D’elia and Teta, 2008). The plant material eaten by C. lanigera varies considerably between seasons. Sixty-five percent of the food is made up of fibre. The high contents of fibre can, according to Cortés et al. (2002), originate from bark, woody stems of shrubs and succulent agaves. The seed component in the chinchilla food is minor – almost absent during wet years. Wild chinchillas eat, as Spotorno et al. (2004) mention, up to 24 plant species, mainly herbs and grasses with seasonal changes. In summer, succulents are taken. It was already Tullberg (1899), who published an illustration depicting the gastric outline of Chinchilla lanigera (Fig. 4.113 A). Gorgas (1967) mentions that the gastric form in that species can vary, but generally the stomach is unilocular, has a roundish bag-like unilocular form with a prominent fornix gastricus (B). Spotorno et al. (2004) call the stomach form pyriform and he gives a length of 63 mm and a greatest breadth of 44 mm. The gastric length given by Gorgas (1967) lies between 56 and 78 mm and its volume is 33.5 cm3; according to Bickel (1981), the stomach contains 60 cm3 and lies mainly on the left side of the animal below the diaphragm. The internal mucosal lining of the organ seems to be completely glandular. In the following two chinchillids, Lagidium peruanum, northern mountain viscacha, and Lagostomus maximus, plains viscacha, Gorgas (1967) found cardia and

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Fig. 4.113: Outlines of stomachs of the hystricomorph family Chinchillidae. Adapted from: Tullberg (1899) (A) and Gorgas (1967) (B).

pylorus closely lying together because the corpus, fornix and pars pylorica form a roundish unilocular sac. The gastric volume in L. peruanum amounts to 65.0 cm3 (length of the stomach, 90 to 122 mm) and in L. maximus, 79.0 cm3 (153–160 mm). This latter species is herbivorous and coprophagous, and Jackson et al. (1996) describe the situation in Argentina, where 16 of the 20 plant species available to L. peruanum were grasses. The area around an area inhabited by viscachas resembles a closely mowed lawn. This food is difficult to digest and this species practises coprophagy (Clauss et al., 2007). 19.2.2.7 Family: Dinomyidae This is a monospecific family, which is represented by the pacarana, Dinomys branickii, a heavily built nocturnal rodent, eating palm and other fruits, leaves and tender stems (White and Alberico, 1992). Anatomical data on the gastric region are not available to the present author. 19.2.2.8 Family: Caviidae In this family, three rodent species are well-known to the general public: The subfamilies Caviinae, Dolichotinae and Hydrochoerinae will be discussed. The guinea pig, Cavia aperea f. porcellus, which is often found as a pet or laboratory animal; the mara, Dolichotis patagonum, that can be seen ranging on the lawns of many European zoological gardens, and, third, the capybara, Hydrochaerus hydrocaeris, the largest surviving rodent. Cavia sp., the guinea pig, is a rodent species (Cao et al., 1994; Sullivan and Swofford, 1997), a fact that has surprisingly been questioned by Graur et al. (1991) and Li et al. (1992). Following Hückinghaus (1960, 1961) the domestic guinea pig is called Cavia aperea f. porcellus by Zumbach (1998), a descendant of Cavia aperea, the wild cavy (Asher et al., 2004). Some subspecies have also been described, for example, by Schliemann (1982). About 3000 to 6000 year ago, guinea pigs were domesticated in South America, as Herre and Röhrs (1990) write. Despite this, Wilson and Reeder (2005) list C.  aperea and C.  porcellus as separate species but call C.  porcellus “domesticated guinea pig”.

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According to Sachser (1998), social interactions between individual guinea pigs have changed during domestication: A great tolerance towards conspecifics can be observed in the domestic form, which cannot be found in C.  aperea. Additionally, experiments undertaken by Furnari (2006) identified behavioural barriers between wild and domestic forms, “which are probably due to the domestication process and can well generate partial reproductive isolation” (page 9). Hydrocoerus hydrochaeris lives in shrubby swamps, forests and wet grasslands (Tomazzoni et al., 2005). They are selective grazers in different types of South American wetlands (Arteaga and Jorgenson, 2007, Desbiez et al., 2011) and choose forage plants of highest protein contents and digest nutrients with high efficiency (Mones and Ojasti, 1986). According to Borges et al. (1996), the digestive efficiency of Hydrochoerus hydrocharis is comparable to that of ruminants eating a similar diet. On the average, five grass species represent 80% of the diet of the capybara (González-Jiménez, 1977), or alternatively, six species represented 64% of total capybara diet (Desbiez et al., 2011). Although the habitat in Southeast Brazil contained a large number of dicotyledons (do Valle Borges and Colares, 2007), the capybaras showed a preference for grasses (Arteaga and Jorgenson, 2007). The nutritional value of plant species selected by the capybara is higher than that of avoided ones (Corriale et al., 2011). For example, the animals select plant species according to caloric energy content. The wetlands in the centre of the South American continent, the Pantanal, is ideal habitat for the capybara, “where groups of 15 to 25 individuals can be seen grazing in flooded habitats” (Alho, 1982, page 157). According to Desbiez et al. (2011), most species consumed by Hydrochoerus hydrocharis were selected and were not the most abundant species in the paddock. During the wet season, an increase in available resources allows the animals to be more selective and thus choosing the more profitable food items whereas in the dry season, niche breadth increases as pastures around the pond dry out. To digest its food effectively, the capybara applies hindgut fermentation, and its digestive efficiency is comparable to that of ruminants due to coprophagy (Desbiez et al., 2011). The stomach of Cavia aperea f. porcellus is unilocular and glandular. The tunica mucosa is smooth and free of cornified epithelium. Illustrations by Tullberg (1899) (Fig. 4.114 A) and Gorgas (1967) (B) show clearly that cardia and pylorus lie close together. The rounded fornix or fundus is not very prominent. The incisura angularis on the lesser curvature can be deep. The length of the

Fig. 4.114: Outlines of stomachs of the hystricomorph families Caviidae and Echimyidae. Adapted from: Tullberg (1899) (A, E); Gorgas (1967) (B, C, D, F, G).

adult stomach lies between 90 and 108 mm; its volume is 8.5 cm3. The digestive process in the guinea pig is enhanced by caecotrophy, a term coined by Harder (1950a). Special faeces, which are produced in the caecum are reingested into the stomach. Frank et al. (1951) studied this process in Cavia sp., but did not differentiate between caecotrophy and coprophagy, as was originally done by Hörnicke and Björnhag (1980). A description of the gastric mesentery, published by Junqueira et al. (1987) does not deal with unusual differentiations; it identifies structures that are normal for the gastric omentum, as described in detail for humans by Liebermann-Meffert and White (1983). The guinea pig mesentery is a uniform membrane that is not pierced by naturally occurring holes and consists of a sheet of connective tissue which is covered on both surfaces by a single, continuous mesothelial layer that rests on a conspicuous basal lamina. This mesothelium is formed of flattened polygonal cells. Sensory information from distal regions of the digestive tract inhibits motor activity of more proximal gut regions. This is accomplished because the majority of afferent pathways from the gastrointestinal tract to the coeliac ganglion originate from the guinea pig large intestine (Messenger and Furness, 1992). On the other hand,

19 Hystricomorpha 

efferent pathways from the coeliac ganglion run to the stomach and other organs. It may be that the enteroenteric pathways via the sympathetic ganglia permit a region of the gastrointestinal tract to monitor volume and composition of the contents it receives, and if necessary inhibit proximal activity to reduce digesta flow into distal gut sections. Great numbers of studies on the domestic guinea pig are available, but some limited information is also available for wild cavies. For example, Tognelli et al. (2001) deals with the food eaten by Microcavia australis, the southern cavy. Leaves, shoots, fruits and flowers are taken and desert plants represent the most frequently eaten food. In this species, Gorgas (1967) found a deep incisura angularis separating the pars pylorica from the rest of the organ. It can be speculated that such an incisure and fold regulates transit of difficult to digest digesta through the stomach. The length of organ amounts to 82–85 mm and the gastric volume is 10.9 cm3. The medium-sized Patagonian mara, Dolichotis patagonum (body mass between 8 and 16 kg, Silva and Downing, 1995) is the second largest caviid rodent, a cursorial, endemic rodent from central south Argentina (Rodríguez and Dacar, 2008). It is a highly efficient herbivore (Kufner and Durañona, 1991), eating mainly green vegetation, but also fruits (Campos et al., 2001a). Puig et al. (1999, 2010) characterise Dolichotis patagonum as grazer. Perennial grasses had a relative frequency in food of 46.8% (Rodríguez and Dacar, 2008). This has the consequence that this species competes with domestic livestock (goat and cattle) when food resources become scarce (Kufner et al., 1992). In autumn and winter, when grasses become senescent, the importance of low shrubs as food items increases, so that maras at this time can be called “mixed feeders”. According to Bonino et al. (1997), it eats 30 species of plants, but only four plant species represent major food sources. There is controversy regarding the proportions of grasses and shrubs in the diet. Maras show preference for grasses, although grasses are less available than shrubs and forbs (Sombra and Mangione, 2005). Digestion of these materials is accomplished with the help of coprophagy, as Campos et al. (2001a) write. The smaller chacoan mara, Dolochotis salinicola, weighs between 1 and 2.7 kg (Redford and Eisenberg, 1992). According to a table published by Campos et al. (2001b), on the other hand, D.  patagonum does not eat arthropods, fruits and seeds in the wet season. Maras show preference for grass, despite these are less available than shrubs. This preference remains constant even during seasonal changes (Sombra and Mangione, 2005). About half of the plant species present in the habitat are eaten

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by maras (Puig et al., 2010). Bonino et al. (1997) state that in general shrubs accounted for about half of the maras’ diet. Rodríguez and Dacar (2008) emphasise that the mara has to be considered as a generalist and opportunistic herbivore. It is an interesting “side-effect” that Rodríguez (2009) mentions that Dolichotis patagonum prefers habitats in the Monte desert of Argentina that were created by human activities, such as grazed, burned and crop areas. As a mammal that is used as a laboratory animal, Cavia sp. has been intensively studied. Eisenberg and Redford (1999) state that the domesticated form, Cavia porcellus, is included within C.  aperea. “The guinea-pig (Cavia porcellus) was domesticated by native Americans of the Andes region from Venezuela to Chile, and although it is distinct from wild species, it appears to be closest to Cavia aperea” (Lord, 2007, page 55). It has already been mentioned above that Herre and Röhrs (1990) published a detailed discussion of the guinea pig’s domestication and apply the full name Cavia aperea f. porcellus, indicating that C. porcellus was domesticated from C. aperea (MüllerHaye, 1984). In a short remark on gastric anatomy, Gorgas (1967) states that the stomach of Dolichotis patagonum has a length of 123 mm and is similar to that of Kerodon. In this species, the organ is unilocular and 71 mm long. It has a voluminous, but not prominent fundus gastricus (Fig. 4.114 C). Weissengruber (2000) supplies some information on the branching mode of the A.  coeliaca in the mara, which supplies the stomach. From the illustration and the accompanying description, a semi-schematic diagram was drawn by the present author (Fig. 4.115). From the A.  coeliaca branches a “Tripus Halleri” with A. gastrica sinistra, A. hepatica and A. lienalis, as it has also been described for human gastric arteries (Lippert and Pabst, 1985).

Fig. 4.115: Arterial supply of the stomach of Dolichotis patagonum. Adapted from Weissengruber (2000).

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A detailed anatomical description of the stomach of Dolichotis patagonum was published by Weissengruber (2000). It is worth being cited extensively, translated, with only a few omissions, by the present author from pages 88 and 89: “The unilocular stomach of the Patagonian mara touches the liver with its parietal face. The opening of the oesophagus can be found slightly left of the median plane on the lesser curvature. The tunica mucosa of the oesophagus extends for about 1 to 2 mm from the pyloric opening into the stomach.…On the left, the whole space caudal of the liver is filled by the fornix gastricus together with the corpus gastricum.…Dorsomedially the stomach has a clearly visible incisura angularis, which separates the pars pylorica from the corpus gastricum. This incisure is responsible for the formation of a semilunar fold, which has a width of approximately 10 mm and extends into the gastric lumen. The pars pylorica consists of the antrum pyloricum (length 20 mm) which is followed by a short canalis pyloricus. In the pyloric region the thickness of the gastric wall increases; the M. sphincter pylori is well differentiated. The internal mucosal lining of the stomach is differentiated by many longitudinal plicae gastricae. These folds can be found in the area of the lesser curvature, as well as in the fornix gastricus. Most of the folds tend to spread from the cardia; they are completely absent in the area of the greater curvature. Although they are numerous on the curvatura minor, they are not prominent, but on the adjacent side walls of the stomach they can be as high as 4 to 6 mm.…In the area of the pyloric antrum they are once again prominent, primarily longitudinal folds that narrow the lumen on its end towards the corpus gastricum. The craniocadal extension of the intermediately filled stomach is 50 mm and the curvatura major is 190 to 220 mm long. The length of the curvatura minor is 25 mm, the latero-lateral width of the stomach lies between 70 and 110 mm” (Weissengruber, 2000).

Hydrochoerus hydrochaeris, the capybara, shows an extremely wide distribution in South America (Mares and Ojeda, 1982). It inhabits the complete zone northeast of the Andes from the Isthmus of Panama, down to northeastern Argentina, south of the La Plata River. Capybaras show a preference for monocotyledons. Do Valle Borges and Colares (2007) mention that just 14.8% of available herbaceous plants are eaten. According to them, aquatic plants constitute important forage, at least in the southern Brazil. However, Mones and Ojasti (1986) state that Hydrochoerus hydrochaeris is not a species eating swamp and water plants, but has to be called a grazer. It has a daily food intake of 70 g of grass per metabolic body weight (g0.75). Escobar and Jimenez (1976) name sweet grasses (Poales) and sedges (Cyperales) as food. Diet selection by capybaras, according to Corriale et al. (2011) is only partly related to nutritional quality. Fed low quality food, animals practise caecotrophy, but Borges et al. (1996) indicate that coprophagy and caecotrophy seem to be not clearly separated in Hydrochoerus hydrochaeris, i.e. “normal” faeces and special caecal faeces are both

reingested. With commercial interest in the background tropical agronomists are interested in comparative aspects of digestive utilisation of different feedstuffs. For example, González Jiménez and Escobar (1975) compared digestion in capybara, rabbit and sheep. The digestibility of pelleted forage was equivalent between sheep and Hydrochoerus; the use of increasing quantities of concentrate was highest in the rabbit, high in the capybara and lowest in the sheep. Gastric capacity, according to deBarros Moraes et al. (2002), in the capybara lies between 850 and 2010 mL, with a mean of approximately 1500 mL. The authors found that the antrum pyloricum is separated from the corpus gastricum by an incisura angularis on the lesser curvature and a constriction of the greater curvature. Such structures cannot be seen in the illustration, which was originally published by Gorgas (1967) (Fig. 4.114 D). According to that author, the fornix and corpus in H. hydrochaeris are of approximately identical volumes; the length of the organ is 110 mm. The architecture of the tunica muscularis deserves careful studies (Pernkopf, 1930, 1937, Pernkopf and Lehner, 1937). These considerations were completely neglected by deBarros Moraes et al. (2005). The textbook knowledge that three muscular layer can be found in the gastric tunica muscularis (stratum longitudinale, stratum circulare and fibrae obliquae from outside to inside) is not considered in their study of the capybara. In contrast, they write on page 54: “Generally speaking, all the four muscular layers (external longitudinal, external oblique, internal oblique and circular) run approximately at right angles to each other”.

19.2.2.9 Families: Dasyproctidae and Cuniculidae The rodent family Dasyproctidae contains two genera, Dasyprocta (agouti) with 10 species and Myoprocta (acouchi) with two species (Partridge, 1992; Wilson and Reeder, 2005). The two species belonging to the family Cuniculidae, the paca (Cuniculus paca) and the mountain paca (C. taczanowkii) are similar; only few data are available. Dasyprocta punctata, the Central American agouti, is classified by Smythe (1978) as a frugivorous animal that also browses and eats seeds. In the stomach of Dasyprocta leporina, the red-rumped agouti, five food elements could be found (Henry, 1999): seeds, fruit pulp, fibre, leaves and animal matter. The seasonal variability in this species is remarkable. Dubost and Henry (2006) compared feeding preferences of the two dasyproctids, Myoprocta exilis (acouchy) and Dasyprocta leporina (agouti), with the paca, Cuniculus paca. All of them are primarily frugivores, but Dasyprocta eats more insects than the two other species. Myoprocta prefers a higher level of fruit and because of this its dietary diversity is only half that of the other two

19 Hystricomorpha 

species. Comparative studies of Dasyprocta spp. and Cuniculus paca, were presented by Govoni and Fielding (2001). According to these authors, both species are mainly folivores, eating seeds, fruits, stalks, leaves and roots. As has already been mentioned above, Dasyprocta eats insects occasionally. It is also able to handle and eat hard fruits. Wild Dasyprocta leporina (red-rumped agouti) eat fruits from 40 species of trees and shrubs, as well as four species of herbs and grasses (Brown-Uddenberg et al., 2004). Anatomical data in the literature on the stomach of Dasyprocta sp. are limited and have been published by only a few authors. Garcia et al. (2000) present some information on the gross anatomy of the digestive system of Dasyprocta leporina, including gastric anatomy. The stomach is piriform-shaped and has a mean length of 13.8 cm with a lesser and a greater curvature. Four regions of the stomach can be differentiated, the cardia, the fornix or fundus, the body and the pylorus. According to Garcia et al. (2000), the fundus forms a conspicuous bulge in the rostral end of the stomach. It has a mean width of 5.6 cm. The body has a diameter of 5.6 cm and is funnel-shaped. The pylorus forms the dilated caudal end section of the stomach. It is thick-walled and has a mean diameter of 3.2 cm. The pyloric sphincter separates stomach and duodenum from each other. The mucosa is lined by simple columnar epithelium. Many chief cells are differentiated, but only a few parietal cells can be found. Mucussecreting cells are rare. The tuncia muscularis consists of inner circular and outer longitudinal muscles, but Garcia et al. (2000) do not mention the fibrae obliquae. Brown-Uddenberg et al. (2004) published valuable measurements of the width of three gastric regions: Fornix gastricus: 5.5 ± 1.3 cm, corpus gastricum: 5.6 ± 1.2 cm, pars pylorica: 3.2 ± 0.6 cm, in Dasyprocta leporina. The weight of the stomach as percentage of total gastrointestinal tract had also been determined by these authors: 13.01%. The length of the stomach, as compared with the total gastrointestinal tract, which has a length of 13.38 cm: 1.62%. In Dasyprocta azarae (Azara’s agouti), the stomach has a prominent fornical blindsac. In his valuable paper, Gorgas (1967) describes a circular constriction between the angulus and the greater curvature that seems to separate the stomach into a bilocular structure; however, this is probably the result of extreme constrictions of the tunica muscularis. The organ ends with a conical pars pylocia. On the other hand, the same author was not able to find a sharp incisura angularis in the unilocular stomach of the red acouchi, Myoprocta acouchy, which has a wide fornix gastricus and is 90 mm long. The paca, Cuniculus paca, is an “opportunistic” feeder (Pérez, 1992), which is mainly frugivorous, but with seasonal variation. Only occasionally it feeds on leaves, buds and blossoms. Gorgas (1967) and Pérez (1992) give

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some basic information on the paca stomach, which has a length of 180 mm (Gorgas, 1967) or 152 mm (Pérez, 1992). The organ has a prominent fornix gastricus and a short and conical pars pylorica (Fig. 4.108 D from Gorgas, 1967) with a circular pyloric fold (Gorgas, 1967), so that the pyloric sphincter is well defined (Pérez, 1992). The discrepancy between description, on the one hand, and illustration, on the other, could show the high variability of the organ. In histological studies Matamoros and Pashov (1982) found that the tunica mucosa is internally lined by a columnar simple epithelium, but on the other hand, these authors describe the fundic or proper gastric glands as formed mainly by parietal cells. Obviously, they mean that the histological structure of all gastric layers in Cuniculus paca is similar to that of most other mammals. 19.2.2.10 Family: Ctenomyidae This family has 60 species, all belonging to the genus Ctenomys (Wilson and Reeder, 2005). Ctenomys mendocinus, Mendocino tuco-tuco, is herbivorous and feeds mainly on grasses, forbs and succulents, as Rosi et al. (2005) write. Digestion of this partly rough material is enhanced in Ctenomys pearsoni (Pearson’s tuco-tuco) by reingestion of faeces. Altuna et al. (1998) mention coprophagy, but not caecotrophy. By the process of reingestion, assimilation of nutrients is improved and B and K vitamins, as well as amino acids synthesized in the large intestine and water can be used by the mammal. Only an outline illustration (Fig. 4.108 E) of the stomach of Ctenomys magellanicus (Magellanic tucotuco) has been made available by Tullberg (1899). 19.2.2.11 Family: Octodontidae This South American family contains 13 species with 8 genera (Wilson and Reeder, 2005). For four of these species, information on the gastric anatomy and the digestive process is available: Spalacopus (Fig. 4.110 E), Octodon, Octomys, and Tympanoctomys. Octodon degus, the degu, eats mainly herbage, bark, green grass (Woods and Boraker, 1975), i.e. a relatively low quality food. Bozinovic (1995) even states that Octodon degus has a pronounced preference for food containing low fibre. However, when degus feed on grass in the wild, containing nearly 60% of fibre during summer, this is the consequence of necessity rather than choice (Caceres and Bozinovic, 1994; Bozinovic, 1995). The viscacha rat, Octomys mimax, which is endemic in lowland deserts of western Argentina, is strictly herbivorous, as Sobrero et al. (2010) write. Main food constituents of this species include leaves, fruits, seeds, and pods. Octomys mimax even feeds on Cactacea. Spalacopus cyanus, the cururo, is a strict herbivore and is specialised to feeding underground on tubers and

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plant stalks and bulbs (Torres-Mura and Contreras, 1998). By its digging activities, this species creates a homogenous soil and influences the growth of plant underground storing organs positively. According to Contreras et al. (1993), these plant structures are the favourite food of cururos. A species specialising on halophytic (high salt) vegetation is the red viscacha, Tympanoctomys barrerae (Diaz et al., 2000), a strictly herbivorous species. The stomach of Octodon degus has a length between 65 and 66 mm and a volume of 9.9 cm3 and an incisura angularis (Gorgas, 1967). Gneiser (2006) describes the degu stomach. Her text was translated from German by the present author: The stomach lies in the regio hypochondriaca sinistra, sometimes, when intensively filled, it extends over this region. It has the form of a bent sac with a greater and a lesser curvature. The facies parietalis of the stomach and the curvatura minor touch the liver and the diaphragm. The visceral face of the stomach is directed to the left and touches the pancreas, as well as the descending duodenum. During certain life periods, the proportions of the stomach can change. For example, in lactating females, the size, contents and dry weight of organs of the gastrointestinal tract – including the stomach – is greater than in non-lactating animals (Naya et al., 2008). The stomach of Spalacopus cyanus is 45 mm long, unilocular and has a conical, large fornix gastricus (Gorgas, 1967; Torres-Mura and Contreras, 1998) (Fig. 4.110 E). It is assumed by Torres-Mura and Contreras (1998) that the “simplicity” of the digestive system, including the stomach, should reflect ingestion of a diet low in cellulose that can easily be digested. Ventura et al. (1996) published a valuable account of the arteries that supply the stomach of Octodon degus. Four schematic drawings of the branching patterns were

published by these authors and have been transformed here into semi-schematic diagrams that allow good comparison of the four modifications (Fig. 4.116). Whenever possible, it was tried to bring homologous arteries on the same level in all four diagrams. Common origins of the truncus coeliacus and the A. mesenterica cranialis, from a truncus coeliacomesentericus (panel B and C) have been found, in addition to the well-known situation, also found in humans, that a truncus coeliacus is the central branch supplying the cranial abdomen with the stomach (panels A and D). Variation of the arterial branching pattern cannot only be found in comparisons between orders, but also within species and orders. Bozinovic et al. (1997) gives an interesting account on the changes of stomach and total gastrointestinal tract dimensions as reactions to intake of secondary plant metabolites, which are produced by plants in an enormous variety (Karasov and Martínez del Rio (2007). For example, when the food of Octodon degus was rich in tannins and fibre, the absolute and relative gastric size was large. The degu seems to compensate for nutritionally poor food by high gut content volume (Fig. 4.117) (Bozinovic et al., 1997). Is this observation related with the results of experiments described by Caceres and Bozinovic (1994). When food quality is changed experimentally in Octodon degus from a low-fibre to a medium-fibre diet, the pH in the cardiac and pyloric region is reduced considerably and acid lysis increases? When fibre was reduced, but tannins remained high, absolute and relative gastric size were still relatively large (Bozinovic et al., 1997). An unambiguous explanation for this effect cannot yet be given. Karasov and Martínez del Rio (2007) react sceptically to the notion that tannins are general digestibility reducers and general effects in in-vitro experiments

Fig. 4.116: Four possible branching patterns of the first branch of the Aorta abdominalis in Octodon degus. Adapted from Ventura et al. (1996).

19 Hystricomorpha 

Fig. 4.117: Absolute (left columns) and relative (right columns) weight of contents of the stomach, small intestine, caecum and colon under influence of four types of food in Octodon degus. Raw data are from Bozinovic et al. (1997).

“do not translate to general effects on digestion in vivo” (page 501). The effects of tannic acid and other tannins on nutrient absorption and thus digestion in general are very complex. It is possible that they may reduce nutrient uptake by enterocytes (Karasov et al., 1992). 19.2.2.12 Family: Abrocomidae This is a relatively small family with two genera, distributed in 10 species. The chinchilla rats (Abrocoma sp.), native to the southern cone of South America, feed on shoots and young leaves of endemic trees (Tarifa et al., 2009). Gorgas (1967) gives short information on the stomach of Abrocoma bennetti (Bennett’s chinchilla rat), which has a prominent blindsac by the fornix gastricus and a total gastric length of 100 mm. It forms a slightly bent sac-like structure. 19.2.2.13 Family: Echimyidae This family of South American spiny rats consists of 90 species, including 21 genera (Groves, 2005), six of these will be mentioned in the following. The family started to differentiate about 22.4 million years ago (Galewski et al., 2005). As a group, the echimyids seem to be mixed feeders. For example, the common Punaré, Thrichomys apereoides, is often classified a frugivore-herbivore, but according to Lessa and Costa (2009) arthropods, especially hymenoptera (wasps and their kin) and isoptera (termites), are an important food source. Emmons (1981) describes a similar food for Dactylomys dactylinus, the Amazon bamboo rat, which is an omnivore, eating fruit, browse and insects. It strips bark from green bamboo stems and eats the inner pulp. A similar behaviour has been observed in the Bolivian bamboo rat, Dactylomys boliviensis (Dunnum and

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Salazar-Bravo, 2004), which strips the bark from green bamboo stems to eat the internal material. Anatomical descriptions for species belonging to this family are not detailed. For example, Emmons (1981) mentions for Dactylomys dactylinus that its stomach is simple. This can also be said for the Guyenne spiny rat, Proechimys guyannensis, for which Tullberg (1899) published an outline illustration (Fig. 4.114 E). It is a rounded, bag-like unilocular structure, just as the stomach of the red-nosed armoured tree-rat, Makalata didelphoides, which has a gastric form that is voluminous, 90 mm long and has a rounded fornix gastricus (Gorgas, 1967, Fig. 4.114 F). Also for Thrichomys apereoides Gorgas (1967) describes a unilocular stomach, which reminds of a funnel, because fornix gastricus and corpus gastricum narrow towards the pars pylorica. The length of this organ is 75 mm. In the Atlantic bamboo rat (Kannabateomys amblyonyx), the unilocular stomach with a length of 50 mm looks bag-like (Fig. 4.114 G) because the fornix is rounded and has only a short blindsac (Gorgas, 1967). 19.2.2.14 Family: Myocastoridae This monospecific family is intimately nested within the previous family Echimyidae (Galewski et al., 2005). Myocastor coypus, the coypu or nutria, is naturally a species living in the southern cone of South America (Mares and Ojeda, 1982), but is now widely distributed in Europe (Stubbe, 1982, Macdonald and Barrett, 1993), Asia (Sheng et al., 1999) and North America (Banfield, 1981). However, hard winters have had detrimental effects on nutria habitat expansion in Europe (Allgöwer, 2005c, Borkenhagen, 2011) – especially in its northern section (Baagøe, 2007) – and set limits to the distribution of this species (Kohli, 1995). 19.2.2.14.1 Food of the nutria (Myocastor coypus) In South America, this species has a daily intake between 700 and 1500 g, i.e. about 25% of their body mass, of green matter (Woods et al., 1992). A great variety of plants is eaten, mainly aquatic vegetation, also stems, leaves, roots and bark. Food of the nutria in Europe is almost exclusively vegetarian (Macdonald and Barrett, 1993); grasses play an important role in food. In summer, shoots and basal parts of sedges are eaten. In autumn, they feed on fruits, and in winter, on tubers, rhizomes, roots, sugar beet, cabbage and occasionally mussels. 19.2.2.14.2 Anatomy of the nutria stomach The stomach of Myocastor coypus is unilocular, as Wagner (1963) depicted. According to the same author, a deep transverse incisure subdivides the greater curvature; Gorgas (1967) calls this incisure in the stomach (length: 150–195 mm) “prominent”. According to Lereboullet

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(1845), the fornix is prominent (Fig. 4.118). The distance from the cardia to the pylorus is 7 cm, and from lesser to greater curvature, 10 cm (Lereboullet, 1845). The nutria stomach is unilocular and lies transversally in the upper abdomen, touching right and left body wall. Wagner (1963) describes the volume of the stomach as about 600 cm3, whereas the diameter of the organ is approximately 115 to 120 mm at its widest point. The organ lies on the left of the intrathoracal part of the abdominal cavity and cranially it touches the liver. Dorsal to the stomach lies the colon transversum, and ventral, the loop formed by the caecum and ileum (Koch et al., 1953; Wagner, 1963). Macroscopically, the gastric tunica mucosa has been described by Wagner (1963): The mucosa of the stomach is usually reddish, and at the oesophageal end, there are prominent folds, whereas the fornix or fundus exhibits a smooth surface almost to the pyloric sphincter. The latter is folded, and due to the arrangement of the underlying muscles, the orifice leading into the duodenum has a diameter of about 30 mm. “The stomach exhibits cardiac, fundic and pyloric regions. The chief and parietal cells are present but not particularly prominent. The muscularis externa consist of an inner circular and an outer longitudinal layer of smooth muscle” (Wagner, 1963, page 324). Stahl (1987) informs about the glandular types distributed in the tunica mucosa; he describes an unspectacular situation, which is similar to that found in many mammals, including man: The glandular stomach has a cardiac gland zone, a proper gastric gland zone and a pyloric gland zone. This situation has been described by Wagner (1963) and depicted by Otto (1954) (Fig. 4.118). The fornix gastricus is lined by a zone of cardiac glands and oesophageal mucosa ends at the cardia within this zone of cardiac glands. The proper gastric glands lie within the corpus gastricum and pyloric glands can be found in the pars pylorica. However, the terms “Cardiadrüsen” and “Fundusdrüsen” are incorrectly applied by Otto (1954). His “cardiac glands” can be found in the fornix (or fundus)

gastricus and his “fundic glands” (= proper gastric glands) lie obviously in the corpus gastricum. During the last decade, careful studies of the arterial supply of the nutria stomach have been undertaken by Culau et al. (2008) and Campos et al. (2013). It was found that the truncus coeliacus “presented a trifurcation after a short path” (Campos et al., 2013, page 1), producing the A. gastrica sinistra, the A. lienalis and the A. hepatica communis in 83.7% of 30 investigated specimens (Fig. 4.119). From the illustration of the latter authors a semi-schematic diagram was drawn (Fig. 4.119). The terminology according to TA (1998) was applied.

Fig. 4.118: External and internal aspects of the stomach of Myocastor coypus. Adapted from Lereboullet (1845) and Otto (1954).

Fig. 4.119: Arterial supply of the stomach of Myocastor coypus. Adapted from Culau et al. (2008) and Campos et al. (2013).

Caribbean hystricognath families 19.2.2.15 Family: Capromyidae This family of hystricomorphs, also called hutias, inhabits Cuba and Hispaniola, as well as smaller Caribbean islands. The family comprises 8 genera with 20 species (Wilson and Reeder, 2005), many of them vulnerable and on the brink of extinction or already extinct. A statement made by Witmer and Lowney (2007) can be generalised for all capromyids: Relatively little is published on Capromys pilorides (Desmarest’s hutia). This species is nocturnal and rests in trees during the daylight hours. It weights between 4 and 7 kg and has a total length between 55 and 60 cm, of which 15 cm belong to the tail. It feeds on bark, stems, leaves, flowers and fruit (Witmer and Lowney, 2007). The food of the Jamaican hutia, Geocapromys brownii, is similar, as Anderson et al. (1983) describe. This species forages on roots, bark, shoots, fruits and foliage.

19 Hystricomorpha 

Gorgas (1967) states clearly that Mysateles prehensilis (prehensile-tailed hutia, he writes Capromys) has a unilocular stomach with a prominent fornix gastricus. The illustration supplied by Gorgas (1967) (Fig. 4.120 B) depicts a sac-like organ with a rounded fornix. He mentions that the gastric length is 90 mm. The stomach of Capromys pilorides is of similar shape and has a volume of 45.7 cm3. Interestingly, Gorgas (1967) writes about the gastric anatomy (length 81 mm) of Plagiodontia aedium, the Hispaniolan hutia, that the pars pylorica is separated from corpus by a clear incisura angularis, which cannot be clearly discerned on Fig. 4.120 C. In Mesocapromys melanurus (black-tailed hutia), the pars pylorica is clearly separated from the corpus gastricum (Gorgas, 1967) and the blindsac of the fornix gastricus has conical shape; the total stomach has a length of 99 mm. Dobson (1884) supplies a detailed illustration of the stomach of this species (Fig. 4.120, A), which shows a tri-locular stomach. Between the cardia and the pylorus, there are constrictions which partially divide the stomach into three compartments; the first of these is the cardiac blindsac, the fornix gastricus. Here the mucosal lining has prominent long parallel ridges, in the second and third the mucous membrane is smooth and thick. The situation in the black-tailed hutia, as depicted by Dobson (1884) tends to coincide with the statement of Gorgas (1967), who writes that the pars pylorica (he writes “Antrum pyloricum”) in Mesocapromys melanurus is separated from the corpus gastricum.

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19.3 Hystricomorpha, small intestine Information on the small intestine of hystricomorphs is very limited. Only short comments can be made. In Chinchilla lanigera (Hystricomorpha), the ductus choledochus opens into the duodenum about 1 cm below the pylorus on a papilla duodeni. The ductus pancreaticus minor leads the pancreatic secreta into the gut about 2 cm caudad of the papilla duodeni. The duodenum then forms an S-shaped loop on the right wall of the abdomen, forms the flexura prima duodeni (fl. duod. cranialis) and proceeds from there caudally and medially as the duodenum descendens. Close to the caudal pole of the right kidney, the flexura secunda is formed, from where the pars transversa crosses the median plane to the left and proceeds via a flexura tertia into the duodenum ascendens. At the cranial edge of a peritoneal fold, the plica duodenocolica, the flexura duodenojejunalis terminates the duodenum. Hebel (1969a) describes that in relation to the diameter of the duodenum in the long-tailed chinchilla, Chinchilla lanigera, the villi intestinales of this section of the small intestine are extremely long. The epithelium contains many goblet cells and the lamina propria mucosae is rich in glands of Lieberkühn. The first 3.5 cm of the duodenum are characterised by a layer of Brunner’s glands, which lie in the tela submucosa. Caudad, these glandulae duodenales dim out. Peyer’s plaques and lymph nodules can also be discerned in the submucosa. Glandulae duodenales in the tela submucosa of the nutria, Myocastor coypus, can be found and Paneth cells lie in the crypts of Lieberkühn (Wagner, 1963).

19.4 The colon of Hystricomorpha

Fig. 4.120: Outlines of the stomachs from three species of Capromyidae. Adapted from Dobson (1884) (A) and Gorgas (1967) (B, C).

As has already been mentioned in the introductory “General Remarks”, the rodent suborder Hystricomorpha consists of two infraorders, the Ctenodactylomorphi with one family, the gundis or Ctenodactylidae, including 5 species, and the second infraorder are the Hystricognathi, which have 30 Old World species and 255 American ones (Wilson and Reeder, 2005). Generally, following the systematic order applied in the volume of these latter authors, the colonic region will be described and illustrated in the following. The original drawings are of different quality and historical age. Those published by Gorgas (1967) are presented here almost unchanged, but in all other sources the illustrations have been adapted by deletion of stomach and small intestine from the drawings presented here. In Fig. 4.121, the digestive tract of Ctenodactylidae, Hystricidae and Ctenomyidae are shown, rodent families where only one illustration and description was available.

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The illustration of the tract from Gorgas (1967) of Ctenodactylus gundi, the common Gundi, is presented. The beginning of the colon ascendens in this species is widened and passes, in a relatively long course, into a spiral loop. The transverse colon follows the spiral and proceeds into the descending colon. As will be demonstrated below, the colonic spiral is a structure that can only be found in a few families of the Hystricomorpha. For example, it is not developed in Hystrix cristata, the crested porcupine, a species where the colon ascendens is characterised by a relatively long parallel loop (Tullberg, 1899). Also in the following transverse colon a smaller parallel loop is differentiated. It can be found in the illustration, but is not mentioned in the description of that author. For Ctenomys magellanicus (tucotuco), however, Tullberg (1899) mentions that a long parallel loop cannot only be found in the ascending colon, but in addition the transverse colon also has a small parallel loop. For the hystricomorph families Erethizontidae, Abrocomidae and Capromyidae, only the large intestine of one species is illustrated and described (Fig. 4.122). In the North American porcupine (Erethizon dorsatum), the colon ascendens arises at the lesser curvature of the caecum (Bonfert, 1928). According to the illustration published by this author, the proximal section of the colon ascendens adheres to the caecum and can therefore be called a paracaecal loop. However, the majority of the length of the caecum remains free of the colon. After having left the

paracaecal course, two parallel loops are formed by the colon. The first one is directed to the right and craniad, and the second, caudad and to the left, ending at the pelvic entrance. From the distalmost branch of the second loop, the colon ascendens runs craniad and passes into the colon tranversum. The following descending colon has a curved course and forms many loops. In the pelvic cavity, it passes into the short rectum. Tullberg (1899) published an illustration of the digestive tract of Bennett’s chinchilla rat, Abrocoma bennettii, which was modified to demonstrate the situation of the large intestine. The right parallel loop of the ascending colon is large, and also the parallel loop, which Tullberg (1899) attributes to the transverse colon, is of remarkable length. The author mentions the very wide mesentery that connects the colon descendens with the dorsal abdominal wall. Gorgas (1967) was able to investigate the intestinal tract of the Cuban Hutia, Mysateles prehensilis, where the colon ascendens forms a right parallel loop. A clearly discernible colon transversum is not mentioned by the author, but the section of the colon that follows the parallel loop shows an intensively winding course. The following illustration (Fig. 4.123) gives information on three species of the Bathyergidae, but for all of them the descriptions are very short and not very informative. The drawing which is adapted from Tullberg (1899) shows a parallel loop, most probably in the transverse colon, another small parallel loop can be

Fig. 4.121: 1. Illustration of the large intestine of Hystricomorpha (caecum black). Adapted from Tullberg (1899) and Gorgas (1967).

Fig. 4.122: 2. Illustration of the large intestine of Hystricomorpha (caecum black). Adapted from Tullberg (1899), Bonfert (1928) and Gorgas (1967).

19 Hystricomorpha 

distinguished at the border between the transverse and descending colon of the Cape dune mole rat, Bathyergus suillus. However, an explanatory text of the author is missing. For Bocage’s mole rat, Cryptomys bocagei, Gorgas (1967), states that a right parallel loop is differentiated in the beginning of the colon. This is quite a prominent structure, whereas the colon descendens is short and its mesentery small. The same author also briefly mentions that the colonic configuration in Heliophobius argenteocinereus, the silvery mole rat, is identical to the situation in Cryptomys. A drawing published by Gorgas (1967) (Fig. 4.124) of the colon of Makalata didelphoides (Echimys) (red-nosed armoured tree rat) shows a relatively wide proximal colon ascendens, which starts from the corpus of the caecum and forms a right parallel loop, which is followed by a second, but considerably smaller, parallel loop. The descending colon is intensively winding, long and has a broad mesocolon. In his illustration of the hairy Atlantic spiny-rat (Trinomys setosus), Tullberg (1899) demonstrates a right parallel loop, but the parallel loop in the transverse colon is very small and inconspicuous. The descending colon has a wide mesentery. In the third species belonging to the Echimyidae (tree rats) that is shown in the illustration, Gorgas (1967) shows a winding course of the proximal colon in Kannabateomy ablyonyx, the Atlantic bamboo rat, followed by a right parallel loop. A second parallel loop is not differentiated and the colon descendens is relatively short. Illustrations of the large intestine of the long-tailed chinchilla, Chinchilla lanigera, are available from three

Fig. 4.123: 3. Illustration of the large intestine of Hystricomorpha (caecum black). Adapted from Tullberg (1899) and Gorgas (1967).

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Fig. 4.124: 4. Illustration of the large intestine of Hystricomorpha (caecum black). Adapted from Tullberg (1899) and Gorgas (1967).

authors, Hebel (1969a), Tullberg (1899) and Gorgas (1967) in Fig. 4.125. The colon is 1.5 times the length of the small intestine. The ampulla coli cannot be clearly distinguished, but the following colon ascendens forms a paracaecal loop that is fixed to the caecal convexity by a mesenterial ligament (Tullberg, 1899). According to Hebel (1969a) and Tullberg (1899), there is no paracaecal loop, but a parallel loop is formed immediately behind caecocolic transition. In general structure, the proximal colon resembles the caecum with two taeniae and haustra. Between these muscular bands are developed. The taeniae end close to the apex of a second parallel loop where the colonic diameter decreases considerably. The parallel loop is very long and its base is connected with the caecal corpus by a ligamentum caecocolicum. The paracaecal loop is strongly haustrated and has, on its mesenterial side, two prominent (muscular?) bands (Gorgas, 1967). Tullberg (1899) and Gorgas (1967) demonstrate in their illustrations that the parallel loop in the ascending colon forms a very long parallel loop. Both the transverse and descending colon are long and have a wide mesocolon. The drawings originally published by Hebel (1969a) and Tullberg (1899) do not present a paracaecal loop, which has been depicted by Gorgas (1967). On the other hand, the latter authors just show one parallel loop, whereas two of these structures are shown by Hebel (1969a). Gorgas (1967) supplies drawings of two of the species belonging to the hystricomorph family Chinchillidae, Lagidium peruanum (northern mountain viscacha) and Lagostomus maximus (Argentine plains viscacha)

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 IV Euarchontoglires – 19 Hystricomorpha

Fig. 4.125: 5. Illustration of the large intestine of Hystricomorpha (caecum black). Adapted from Tullberg (1899), Gorgas (1967) and Hebel (1969a).

of the colon ascendens is fixed to the caecum by a ligamentum caecocolicum. The colon ascendens forms a prominent ampulla caeci and then follows the convexity of the caecum (Gorgas, 1967). According to Bonfert (1928), the ascending colon of Cavia sp. consists of two sections, one that is fixed to the curvature of the caecum and the second part that forms a U-shaped parallel loop. This remarkable parallel loop, which clearly belongs to the colon ascendens (Gorgas, 1967), is U-shaped and bent on itself, i.e. the U-shaped parallel loop is bent again into a U, the branches of which are formed by two section of the parallel loop. The centrifugal branch of the spiral passes into the colon transversum, which lies in loose loops. Snipes (1982a) mentions that the proximal colon runs parallel to the corpus caeci, being connected to it by a mesenterial ligament (see also Fig. 4.127 after Elliott and Barklay-Smith, 1904). The middle portion of the corpus caeci runs under the proximal colon, crossing the body midline, and curves cranially, dorsal to the loops of the small intestine. The proximal ascending colon after leaving the area of the caecum courses to the right lateral side and in its course forms a parallel loop, which is bent on itself; the authors speaks of an incomplete spiral. The colon then transverses the upper abdomen in a slightly contorted course Snipes (1982a). At the upper left quadrant of the abdomen immediately cranial to the caecocolical region, the colon forms a number of loops similar in appearance to the small intestinal configuration. The terminal portion of the colon descends from this area running to the rectum. The colon transversum and descendens have a wide mesentery similar to the small intestine. In the descending colon, which passes into the rectum, the mesocolon becomes suddenly small. Sander (1990)

(Fig. 4.125). In both species, a paracaecal loop is differentiated, which is strongly haustrated and shows two longitudinal (muscular?) bands. At the end of the paracaecal loop, a parallel loop follows, which is relatively short in Lagostomus maximus. The colon transversum is short and cannot be clearly delineated in both species. The descending colon with its winding course is very long! In his study on longitudinal muscular bands (taeniae) in the large intestine, Vau (1934b) mentions for the domesticated guinea pig (Cavia porcellus), three taeniae of the caecum in that species, which belongs to the hystricomorph family Caviidae, proceed to the colon where they first become broader and start to form a continuous longitudinal muscular layer along the antimesenterial side of the colon. Under the fixation of the mesocolon to the colon, longitudinal musculature cannot be found. In this region, haustra are formed. In an illustration that was originally published for Cavia sp. by Tullberg (1899) (Fig. 4.126), a caecal taenia is depicted. Here, again, the proximal part

Fig. 4.126: 6. Illustration of the large intestine (caecum black) of Cavia sp. (Hystricomorpha). Adapted from Tullberg (1899), Gorgas (1967), Bonfert (1928), Snipes (1982a) and Sander (1990).

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 245

Fig. 4.127: Large intestine of the Guinea pig. Adapted from Elliot and Barkley-Smith (1904). Fig. 4.128: 7. Illustration of the large intestine of Hystricomorpha (caecum black). Adapted from Gorgas (1967).

makes a clear distinction between colonic regions of Cavia: The border between the proximal and transverse colon is projected on the apex of the colonic spiral. The distal colon starts on the right angle formed by the colon on the level of the left costal arcus. The colon transversum is short, the colon descendens is widened (Gorgas, 1967). The descending colon passes to the entrance of the pelvis and proceeds into the rectum, which has a length of about 5 cm. Three species of the Caviidae, other than Cavia sp., are shown in Fig. 4.128 by Gorgas (1967). According to this author, the colonic configuration in Kerodon rupestris (rock cavy), a species of the subfamily Hydrochoerinae, is as in Cavia. The parallel loop is U-shaped, i.e. it is bent on itself and shows a tendency towards the formation of a spiral. Good illustrations of the large intestine of the largest living rodent, which belongs to the family Caviidae (Wilson and Reeder, 2005) or Hydrochaeridae (Macdonald, 2004), the capybara (Hydrochoerus hydrochaeris), a member of the subfamily Hydrochoerinae (Wilson and Reeder, 2005), are not available to the present author. In an article on the digestive physiology and feeding of capybaras, González-Jiménez (1977) publishes a photo of a laid-out digestive tract, which gives very little information on the colon. Neither colonic spiral nor a parallel loop can be discerned, and not anatomical description exists in the text. The author fully concentrates on the caecum, which is an important site of microbial degradation of the plant food eaten by the capybara. Gorgas (1967) makes an interesting remark on the colonic spiral in Hydrocoerus hydrochaeris. It forms a flat disk (“flache Scheibe”), which – in relation to its anatomical position – corresponds with the U-shaped loop (“U-förmigen Schlinge”) in the Caviidae.

It has already been remarked above that this structure is U-shaped and bent on itself, i.e. the U-shaped parallel loop itself is bent again into a U. The ileum of the southern mountain cavy, Microcavia australis, opens between the taeniated caecum and the colon (Fig. 4.128, upper panel). Along the mesenterial side of the colon two longitudinal (muscular?) bands can be found. Formation of scybala, faecal pellets, begins in the distal branch of the parallel loop. In Dolichotis patagonum, the Patagonian mara, colonic configuration is as in other Caviinae, but it has a very long colon descendens. Weissengruber (2000) gives a detailed, but insufficiently illustrated description of the colon for Dolichotis patagonum. The beginning of the colon ascendens either lies caudad of the caecum on the right side of the abdomen or it can lie along the left abdominal wall. It begins with a wide diameter of approximately 30 mm. The colon is connected with the caecum by a plica caecocolica and follows the course of the caecum in a curved line. During this course, its diameter decreases to about 15 to 20 mm. From the convexity of the caecum, it turns up cranio-dorsally. This is a thickwalled section of the colon ascendens with a diameter of about 10–15 mm. On the right body wall, it turns ventrally forming a U-shaped double loop, which means that two “U” follow each other. The two section of the double loop lie in a plane close to the right body wall. This structure can also be considered as a spiral. In this region, the diameter of the lumen has decreased to 7–10 mm. On the mesenterial side of the colon ascendens, two parallel longitudinal folds can be seen from internally, but from the outside, they cannot be distinguished because of the fixation of

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 IV Euarchontoglires – 19 Hystricomorpha

Fig. 4.129: 8. Illustration of the large intestine of Hystricomorpha (caecum black). Adapted from Gorgas (1967) and Bonfert (1928).

the mesocolon. These longitudinal folds end in the first U-shaped loop before the second “U” begins. The length of the colon ascendens from the ostium caecocolicum to the beginning of the colon transversum in Dolichotis is 64 cm. Cranial of the A. mesenterica cranialis, the colon transversum starts, which passes into the colon descendens, which lies to the left and forms loops. The diameter of the colon descendens is 7–10 mm and it has a length of about 1.55 m. In the two species belonging to the rodent family Dasyproctidae (Fig. 4.129), Azara’s agouti, Dasyprocta azarae, and Myoprocta acouchy (red acouchi), the colonic configuration is similar and comparable with Cavia sp. First, the ascending colon follows the convexity of the caecum and forms a paracaecolic loop, which is connected with the caecum (Bonfert, 1928; Gorgas, 1967). Afterwards, it passes into a spiral, which can be imagined as being developed out of the parallel loop, bent on itself. The following colon transversum is characterised by loose loops. Dorsally, on the left abdominal side, follows the descending colon, which passes into the rectum. Both colon transversum and descendens are relatively short. Fig. 4.130 presents two species, both illustrated by two drawings from different authors. From the head of the caecum, the colon ascendens of the lowland paca, Cuniculus paca, the colon ascendens starts, its configuration is similar to Dasyprocta, but typical differentiations can also be found: the ampulla coli is prominent, a paracaecal loop can be seen. About a third of the caecal length is not connected with the paracaecal loop, which passes into a spiral and lies in a plane and is no three-dimensional structure. This situation can be derived from the U-shaped parallel loop. From the centrifugal branch of the spiral, the

Fig. 4.130: 9. Illustration of the large intestine of Hystricomorpha (caecum black). Adapted from Tullberg (1899), Gorgas (1967) and Bonfert (1928).

transverse colon starts, which proceeds into the winding descending colon (Bonfert, 1928). Both colon transversum and descendens are extraordinarily long, the latter has a broad mesocolon (Gorgas, 1967). Tullberg (1899) presents information on the differentiation of the colon in the “Coruro” from Chile (Spalacopus cyanus), a species of the hystricomorph family Octodontidae (Fig. 4.130). According to Gorgas (1967), the colonic configuration is only little differentiated. The colon ascendens is short and not connected with the caecum. The colon ascendens has a well-developed parallel loop. Tullberg (1899) writes that the colon transversum has a small parallel loop. From the distal branch of the right parallel loop, a short colon descendens starts. Taeniae could not be found. It should be mentioned that another species of the Octotontidae, the Degu, Octodon degus, González and Feder (1997) mention that “the ascending colon…is arranged in two superimposed, often spiral folds….” Such a spiral structure was neither depicted nor described by Tullberg (1899) for the other octodontid Spalacopus cyanus. The Nutria or Coypu (Myocastor coypus) is an intensively investigated and depicted species (Fig. 4.131). As early as 1845, Lereboullet published an illustration, although many anatomical differentiations cannot be seen on it. Wagner (1963) differentiates between large and

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held together by mesenterial duplicatures. This loop begins 17 ± 2 cm distal from the caecocolical junction (Snipes et al., 1988). The initial 39 ± 4 cm of the colon displays on the external surface a haustrated appearance. This portion is termed the proximal colon. It ends at the flexure of the parallel loop. Distal to the flexure, begins the distal colon, and this includes the distal limb of the loop and the remainder of the colon from the loop approximately 33 + 8 cm to the rectum. The haustrated portion, i.e. the macroscopically visible, external outpouchings of the proximal colon from the caecocolical junction to the flexure of the loop, was seen to consist of a double ridge running along the longitudinal axis of the intestines on the internal surface. The distal branch of the parallel loop passes into the transverse colon, which shows only few curves (Bonfert, 1928) and passes to the left where the colon descendens with a few bends runs caudad and passes in the pelvis into the rectum. According to Gorgas (1967), the colon transversum follows, which also forms a small loop. The descending colon is short (Gorgas, 1967) and has a wide mesentery (Tullberg, 1899).

Fig. 4.131: 10. Illustration of the large intestine of Hystricomorpha (caecum black – with the exception of the stretched organ). All five illustrations are of Myocastor coypus. Adapted from Lereboullet (1845), Tullberg (1899), Bonfert (1928), Gorgas (1967) and Snipes (1988).

small colon. The first 28 to 30 cm are haustrated due to two longitudinal bands or taenia coli and form the “large colon”. It has a variable diameter from 2.5 to 3 cm. The greater portion of the large colon is supported by a mesentery which originates from the outer curvature of the duodenum. The small colon commences as the distal arm of a loop of the large colon and is continued at the pelvic inlet by the rectum. Its length is about 30 cm, and it is about 1.5 cm in diameter. There are no longitudinal bands or sacculations in the small colon. The terminal end of the small colon is the rectum. It is a straight tube approximately 80 mm in length and about 10 mm in diameter. Snipes et al. (1988) give a detailed description of the colonic configuration parallel to a strongly schematised illustration (Fig. 4.131, upper panel). It begins as a funnelshaped extension from the caecum. It is approximately 93 (75–113) cm in length. The taeniae of the caecum disappear at the beginning of the colon and the longitudinal muscle layer has a uniform thickness for two-thirds to threefourths of the gut circumference. The colon ascendens forms a small paracaecal loop (Tullberg, 1899; Gorgas, 1967). On the right side of the abdomen lies the right parallel loop, which is very large and the most conspicuous differentiation macroscopically. The limbs of the loop are

19.4.1 Compilation of colonic differentiations After having obtained information on the differentiation of parallel loops, colonic spirals and paracaecal loops in the Hystricomorpha, the question arises whether there is a connection between taxonomy, on the one hand, and these anatomical differentiations, on the other. To obtain material to answer this question the colonic differentiations were compiled schematically on top of a tree published by Macdonald (2004) (Fig. 4.132). A differentiation was made between those species where just one parallel loop could be found and those where two such parallel loops could be discerned. With the exception of the Ctenodactylidae, those hystricomorph rodent families which have a colonic spiral (Dasyproctidae, Cuniculidae, Caviidae and Hydrochaeridae) are closely related with each other. It is interesting that the closely related Erethizontidae have two parallel loops. The differentiation of two colonic parallel loops, which can also be found in five additional families (Echimyidae, Myocastoridae, Abrocomidae, Bathyergidae and Hystricidae) is widely distributed in Hystricomorpha and does neither show a clear connection with the systematic relationship, nor with the average concentration of fibre (g crude protein/kg dry matter) in the food (Langer, 2008), which is indicated by the columns in Fig. 4.132. Paracaecal loops are also considered in the illustration. The close connection between the proximal part of the colon ascendens with the caecum under formation of a paracaecal loop can be found in closely related families; only the Myocastoridae, where a short section of the colon

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 IV Euarchontoglires – 19 Hystricomorpha spiral can be understood as a hairpin-shape parallel loop that is bent on itself, thus forming a U in a U. When the apex of this spiral is “lifted” out of the plane of the outer coils, a cone-shaped can be formed, as, for example, in Cuniculus paca (Fig. 4.130). A very prominent example of the formation of a spiral cone has already been shown by Sperber et al. (1983) for Lemmus lemmus (Myomorpha, Muroidea), illustrated in Fig. 4.93.

19.4.2 Mesenteries of the rodent colon

Fig. 4.132: Colonic differentiations in Hystricomorpha. For Hydrochaeridae only a descriptive text is available. Tree after Macdonald (2004).

lies immediately adjacent to the caecum, do not belong to the group of related families. A special remark has to be made in connection with the colonic spiral, which is also called the “coiled portion” of the colon ascendens by Snipes (1982a). The illustration, which was adapted from the drawing published by that author (Fig. 4.133), shows clearly that the coils of that

Fig. 4.133: Spiral (also called “coiled portion”) of the colon ascendens in Cavia sp.. Modified after Snipes (1982a).

The morphology and position of mesenteries and peritoneal ligaments that are connected with the colon is often complex in rodents. In his detailed study on the guinea pig Snipes (1982a) makes a remark, which can be generalised for Rodentia: “The graphic representation of the mesenterial situation in the abdomen presents certain inherent problems, especially the fact that in situ the mesenteries and different portions of the intestines lie one upon the other. For a clear definition of the individual mesenterial components the necessity of displacing the intestines and connecting mesenteries from their normal positions is unavoidable. The resultant schematic presentations are thus approximations of the actual situation” (page 101). It is characteristic for all mammals that the mesenteries of the whole gut caudal to the opening of the ductus choledochus and the ligamentum hepatoduodenale, i.e. caudal of the liver and the umbilicus, is derived from a dorsal mesentery, which – as a peritoneal duplicature – is fixed on the dorsal body wall (Broman, 1905). Right and left peritoneal cavities merge in this abdominal region ventral of the digestive tract, which means that in mammals an anlage of the ventral mesentery is not present in mammals (Starck, 1982). “Rotation” of the gut and secondary fixation of smaller or larger sections of it are responsible for the formation of recesses or pockets, which are lined by the peritoneum (Davis et al., 2008). This allows either mobility or fixation of the abdominal organs. In his studies on five rodent species, Snipes (1979a, b, 1981, 1982a, b) gives detailed information on the morphology of mesenteries and “ligamentous connections”, which are fastened to the colon. There are special differentiations in the rodent colon, such as parallel loops and colonic spirals, which are responsible for making the architecture of peritoneal duplications rather complex. It is certain that the situation in humans with two secondarily retroperitoneal colonic sections, the colon ascendens and colon descendens without mesentery, and two intraperitoneal parts, the colon transversum and colon sigmoideum with mesocolon transversum and mesocolon sigmoideum, is different from the conditions in rodents.

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In the following, reference will be made to the studies on the comparative anatomy of the rodent digestive tract published by Snipes (1979a, b, 1981, 1982a, b). This author presented descriptions and illustrations of the following species: Myomorpha: Cricetinae: Microtus agrestis (Field vole) and Phodopus sungorus (Striped desert hamster) (Fig. 4.134), Myomorpha: Murinae: Meriones unguiculatus (Mongolian jird or gerbil) and Mus musculus (House mouse) (Fig. 4.135), as well as Hystricomorpha: Caviinae: Cavia porcellus (guinea pig) (Fig. 4.136). According to Snipes (1979a), the ascending colon in Microtus agrestis lies dorsal to the distal ileum and is connected to it and to the left portion of the corpus caeci by mesenterial-like, ligamentous structures (A) (Fig. 4.134). From the radix mesenterii, a mesentery (B) extends to the more distal part of the colon ascendens and towards the colon transversum. Other thin mesenterial ligaments, which are not directly connected to the main mesenteries of the radix mesenterii span between the flexura coli sinistra and the ascending duodenum (C). In the striped desert hamster, Phodopus sungorus, the entire intestinal tract appears to hang on a continuous mesentery (Fig. 4.134). It is anchored on the dorsal body

wall at the midline in the upper quadrant of the abdomen. From this point of fixation, the radix mesenterii (star), mesenterial sheets fan out. A discrepancy between descriptions and illustration given by Snipes (1979b) have to be stated: According to this author, a mesenterial duplicature (gastro-colonic ligament) connects stomach (and spleen) of Phodopus sungorus with the cranial border of the transverse colon, extending from the flexura coli sinistra to the body midline. The colonic loop is not involved in this mesenterial connection. The present author did not indicate this ligament described by Snipes (1979b) because this illustration shows that the pars descendens duodeni runs under the mesenterial root (“From the right, the duodenum runs under [dorsal to] the fix-point of the mesenterium”, Snipes, 1979b, page 332). The mesentery runs to the caecum and proximal colon (A); a second part runs into the colonic loop on the right body side (B); and a third consisting of a thin connection (C) on the left body side to the mesentery of the descending colon (D), which is fixed independently on the dorsal body wall along the length of the midline. The radix mesenterii of the intestinal mesentery of the gerbil (Meriones unguiculatus) is located mid-abdominally

Fig. 4.134: The large intestine and its mesenteria in myomorph Cricetinae: Microtus agrestis and Phodopus sungorus. Colon marked black. Modified after Snipes (1979a, 1979b).

Fig. 4.135: The large intestine and its mesenteria in myomorph Muridae: Meriones unguiculatus and Mus musculus. Colon marked black. Modified after Snipes (1981, 1982b).

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on the dorsal body wall (Snipes, 1982b) (Fig. 4.135). The distal portion of the duodenum forms a loop around this site of fixation. From this site, two main mesenteric sheets emerge: one for the jejuno-ileal loops, the caecum and initial portion of the proximal colon (A) and the other sheet for the ascending and transverse colon (C). The ascending colon and descending portion of the duodenum are connected by a duplicature of this mesentery. The two main sheets blend together at the proximal colon approximately 2 mm from the caecocolical junction. The descending colon possesses its own mesentery (D). A small duplicature or ligament occurs between the proximal portion of the descending colon and distal portion of the duodenum (C). The caecum itself is supplied by a continuation of the mesentery to the small intestine (A). The colonic mesenteries of the house mouse, Mus musculus, are also described in detail by Snipes (1981) (Fig. 4.135). A thin mesenterial duplicature runs along the end of the ileum, on one side, onto the caecum and down to the apex (A). On the other side of the ileum, the mesentery stretches out over the ampulla ceci onto the proximal colon (B). These extensions of the mesenteries are derivatives of the radix mesenterii (star). This mesenterial root itself is bound to the dorsal abdominal wall under the stomach. The greater portion of the small intestine and proximal and transverse portions of the colon are attached to the radix mesenterii (B). The descending colon is attached to the dorsal wall by a separate mesenterium (D). The duodenum, via a ligament or duplicature (C), is secondarily attached to the transverse colon and, along its distal portion, to the descending colon. The entire gut structure is very movable in the abdominal cavity and hangs together via the radix mesenterii. The entire intestine of Cavia porcellus (Fig. 4.136) from duodenum to descending colon as a unit is very mobile within the abdominal cavity, being affixed to the dorsal body wall along the midline over a short distance, the radix mesenterii (Snipes, 1982a). The exception is the descending colon (D) which possesses its own mesentery, its site of fixation stretching over a greater craniocaudal length of the dorsal body wall. The main mesenterial sheets extend from the radix to the proximal and ascending colon and to the transverse colon (B). The ligamentous connections between different portions of the intestines include a duplicature between the proximal portion of the duodenum and transverse colon (arrows), and a connection between the proximal colon and the major portion of the corpus ceci (A). The mesentery of the descending colon merges cranially into that of the transverse colon (B). A few remarks on the colonic mesenterial situation in the hystricomorph nutria or coypu, Myocastor coypus,

Fig. 4.136: The large intestine and its mesenteria in hystricomorph Caviidae: Cavia porcellus. Colon marked black. Modified after Snipes (1982a).

have been made by Wagner (1963). According to him, the large colon proper commences near the ileocaecal junction and is largely confined to the right of the abdominal cavity. The greater portion of the large colon is supported by a mesentery which originates from the outer curvature of the duodenum. This is similar to the situation just described above for another species belonging to the Hystricomorpha, the guinea pig (note arrows in Fig. 4.136). Wagner (1963) calls the following section the small colon, which is a straight tube with a simple mesentery that arises from along the mid-dorsal line. 19.4.3 Arterial supply of the rodent colon Reference to the conditions in humans can be helpful (Lippert and Pabst, 1985; Moore, 1992; Fanghänel et al., 2003): The A. ileocolica is defined as the vessel that supplies the most distal part of the ileum, the caecum and the most oral part of the colon ascendens. The A. colica dextra supplies the following more aboral section of the colon ascendens. The colonic section supplied by the A.  colica media is the colon transversum; the A.  colica sinistra runs towards the colon descendens; in humans it is a branch of the A. mesenterica inferior (or A. mesenterica caudalis in domestic mammals) (Koch and Berg, 1985). The combination of the sequence of arterial

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Fig. 4.137: Arterial supply of the gut in a sciuromorph and hystricomorph rodent species. In both illustrations the colon transversum lies between the two arrows. 1: Aorta abdominalis; 2: A. mesenterica superior; 3: Aa. jejunales et ilei; 4: A. ileocolica; 5: A. colica dextra; 6: A. colica media; 7: A. colica sinistra; 8: A. mesenterica inferior. Modified after Gorgas (1967).

branches and the sequence of colonic regions gives information on the identification of colonic sections as applied in the anatomical nomenclature. According to Gorgas (1967), the first and the last vessel that supply the colon are clearly defined: The A. ileocolica (Fig. 4.137, No. 4) runs towards and supplies the border region between the ileum and the colon, including the caecum. On the other hand, the last colonic vessel is the A.  mesenterica inferior (caudalis) (8). Between the two vessels lie Aa.  colicae (5, 6, 7). The A.  ileocolica (4) presents the trivial information on the beginning of the colon ascendens, but the colon descendens is not identified unambiguously because the A. colica sinistra (7) in rodents is not generally a branch of the A.  mesenterica

inferior (caudalis). In addition, the information supplied by the illustrations published by Gorgas (1967) does not allow to differentiate the colon sigmoideum from the colon descendens. However, the anastomosis between A. colica dextra (5) and A. colica media (6) identifies the border between the colon ascendens and the colon transversum and the anastomosis between A. colica media and A. colica sinistra. In the following, reference will be made to a couple of illustrations originally published by Gorgas (1967). In one of his illustrations (Abb. 6, page 262), he identifies the arterial vessels of the gut, but creates problems by depicting the A. colica sinistra as an anastomosis of the A. colica media with the A.  mesenterica inferior. However, an

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anastomosis is the terminal region of arterial blood supply in the area of a natural connection between two arteries. As has already been written above, the anastomosis between Aa. colica media and sinistra can be found in the area of the border between the transverse and descending colon. In the semi-schematic illustration published by Behmann (1973) (Fig. 4.138) for myomorph rodents there are separate branches from the A. mesenterica superior (1) to the different sections of the colon. One branch forms the A. ileocolica (3) to ileum, caecum and to the proximal part of the colon ascendens (4). Separate branches of the A.  mesenterica superior are formed as A.  colica dextra (5) and media (6) as well as the A. colica sinistra (7). The latter two anastomose with each other in the area of a parallel loop (right upper arrow). The anastomosis between the A.  colica dextra (5) and media (6) clearly marks the demarcation between the colon ascendens and transversum and is marked by the left arrow. On the other hand, the right upper arrow marks the border between the colon transversum and descendens. The caudalmost part of the

Fig. 4.138: Arterial supply of the large intestine in myomorph rodents. 1: Aorta mesenterica superior; 2: Aa. ilei; 3: A. ileocolica; 4: Ramus colicus; 5: A. colica dextra; 6: A. colica media; 7: A. colica sinistra; 8: A. mesenterica inferior. Modified after Behmann (1973).

colon descendens, as well as the rectum are supplied by the A.  mesenterica inferior (caudalis) (8), which anastomoses with the A. colica sinistra. In myomorph rodents, the A. colica sinistra (7) and A. mesenterica inferior (caudalis) (8) are independent from each other. The colon ascendens of Spermophilus suslicus (speckled ground squirrel) follows the caecum and its end is represented by the site where an anastomose is formed between the A.  colica dextra (5 in Fig. 4.137) and the A. colica media (6). This site is marked with the left arrow in the illustration. Of course, an anastomosis cannot represent a clear demarcation line. The colon transversum starts in the area just identified and ends in the area of an anastomosis between the A. colica media (6) and A.  colica sinistra (7) (right arrow). Again, the colon transversum and colon descendens are not clearly delineated from each other. In contrast to Gorgas (1967), the present author is of the opinion that the A.  colica sinistra (7) is a branch of the A. mesenterica inferior (caudalis) (8), which are both marked in Fig. 4.137 as “7/8”. The colon descendens and colon sigmoideum cannot be clearly separated from each other, nor can the colon sigmoideum be separated from the rectum with the help of their arterial vessels. To which of the sections of the colon do special differentiations like the parallel loop (which is forked in Spermophilus suslicus [Sciuromopha] and forms so-called Gabelschlingen [Gorgas, 1967]) belong? Positioned between the two arrows, it can clearly be attributed to the colon transversum. The parallel loop is supplied by a vessel that originates from the A.  colica media (6). In Cavia porcellus (domesticated guinea pig, Hystricomorpha), an anastomosis between the A.  colica dextra (5) and the A.  colica media (6) is formed at the apex of its colonic spiral, i.e. at the point where incoming windings end and outgoing ones begin. The branched parallel loop in Spermophilus suslicus is part of the colon transversum and the colonic spiral in Cavia porcellus belongs partly to the colon ascendens and partly to the colon transversum. The A. colica media (6) in Cavia p. proceeds aborad to the colon descendens, where it forms an anastomosis with the A. colica sinistra (7). In the two species just described, the situation of the arterial supply of the colon shows similarities with arterial conditions in humans (Lippert and Pabst, 1985), horse, cow, sheep goat, pig and dog (Koch and Berg, 1985): The A. colica sinistra (7) is a branch of the A. mesenterica inferior or caudalis (8). In another Sciuromorph, Cynomys ludovicianus (black-tailed prairie dog), the most proximal part of the colon ascendens is supplied by the A.  ileocolica (4) and the A.  colica dextra (5) (Fig. 4.139, Gorgas, 1967). As in

19 Hystricomorpha 

Fig. 4.139: Arterial supply of the gut in a sciuromorph and a myomorph rodent species. 1: Aorta abdominalis; 2: A. mesenterica superior; 3: Aa. jejunales et ilei; 4: A. ileocolica; 5: A. colica dextra; 6: A. colica media; 7: A. colica sinistra; 8: A. mesenterica inferior. Modified after Gorgas (1967).

Spermophilus suslicus, the A.  colica media in Cynomys ludovicianus supplies the branched parallel loop. At the colon descendens, an A.  colica sinistra (7) that is independent of the A.  mesenterica inferior (caudalis) (8) is the supplying vessel; a situation different from that in humans and domestic mammals that has just been mentioned in the previous paragraph. In a representative of the Myomorpha, Spalax leucodon (lesser blind mole rat) (Fig. 4.139), the situation in the two parallel loops is more complex than in Cynomys ludovicianus, but shows similarities with the illustration given by Behmann (1973) from Fig. 4.138: The first parallel loop is supplied both from the A. colica dextra (5) and the A. caecocolica (4). The second parallel loop obtains arterial blood completely via the A. colica media (6), which in this species is a branch of the A. colica dextra (5), a situation different from that depicted by Behmann (1973) for “myomorph rodents” in general. At first glance, the situation in the arterial supply of Hystrix cristata (crested porcupine, Hystricomorpha) is superficially similar (Fig. 4.140) to that in the myomorph

 253

Fig. 4.140: Arterial supply of the gut in two hystricomorph rodent species. 1: Aorta abdominalis; 2: A. mesenterica superior; 3: Aa. jejunales et ilei; 4: A. ileocolica; 5: A. colica dextra; 6: A. colica media; 7: A. colica sinistra; 8: A. mesenterica inferior. Modified after Gorgas (1967).

Spalax leucodon (Fig. 4.139). However, the A. colica dextra (5) supplies the long parallel loop, which thus has to be homologised with the colon ascendens. The short parallel loop is supplied by the A. colica media (6) and the demarcation between colon transversum and descendens lies in the region of the anastomosis between this latter artery (6) and the A. colica sinista (7), a branch of the A. mesenterica inferior (caudalis) (8). In Erethizon dorsatum, the North American porcupine, on the other hand, both parallel loops are supplied by one branch, the A. colica dextra (5), from which the A. colica media (6) branches off. In another hystricomorph, Chinchilla lanigera (longtailed chinchilla), the right (5) and middle (6) colonic arteries are as related as in Erethizon dorsatum, but only the A. colica media (6) supplies the single parallel loop, whereas the A. colica dextra (5) brings blood to the paracaecal loop (Fig. 4.141). Although there is no paracaecal loop in Heliophobius argenteocinereus (silvery mole rat, Hystricomorpha), many short branches, which represent the A. mesenterica superior (5), supply the colon ascendens. The arterial supply of the parallel loop comes from the A. colica media (6).

254 

 IV Euarchontoglires – 19 Hystricomorpha

Fig. 4.141: Arterial supply of the gut in two hystricomorph rodent species. 1: Aorta abdominalis; 2: A. mesenterica superior; 3: Aa. jejunales et ilei; 4: A. ileocolica; 5: A. colica dextra; 6: A. colica media; 7: A. colica sinistra; 8: A. mesenterica inferior. Modified after Gorgas (1967).

From these findings for Myomorpha, Sciuromorpha and Hystricomorpha, it is in some cases difficult to identify clear demarcation lines between sections of the colon. The problem of the clear discrimination between the midgut and the hindgut in human anatomy (Starck, 1975) cannot be resolved in rodents, but in some species within this order, the A. colica sinistra (7) is not a branch of the A. mesenterica inferior (caudalis) (No. 8), as in man (Lippert and Pabst, 1985) or in domestic mammals (Koch and Berg, 1985). In the species depicted, the A. colica sinistra (7) is separate branch from the A.  mesenterica superior (1) in: Cynomys ludovicianus (Sciuromorpha), Spalax leucodon (Myomorpha), Erethizon dorsatum (Hystricomorpha) and Heliophobius argenteocinereus (Hystricomorpha).

19.4.4 Macroscopic configuration of the rodent colon Now, after the colonic configuration of all rodent suborders has been considered, the situation in the whole order should be taken into account. A tree that represents

a wide range of rodents was modified after a publication by Veniaminova et al. (2007) and colonic spirals, parallel loops and paracaecal loops were projected on that tree (Fig. 4.142 [compare with Fig. 4.132]). Because of the variability of the above-mentioned anatomical differentiations, the general characteristics of the colon cannot be given. Also projections on other recent phylogenetic trees of the order Rodentia, such as those published by Huchon et al. (2002) and Blanga-Kanfi et al. (2009), do not create improved clearness. For example, the spiral can be a threedimensional cone, as, for example, in the Murinae, or a flat disc, as in many hystricomorphs. In closely related families, either one or two parallel loops can be differentiated. In hystricognath rodents, the paracaecal loop can follow the convexity of the caecum. The association between this loop and the caecum can be of different intensity. In two publications, Vorontsov (1960, 1967) presents data on the length of the colon, expressed as percentage of the total gut. These data were combined with information on the differentiation of the colon (Fig. 4.143). The mean percentage of the relative colonic length in rodents is 30%, but variability can be observed. However, it was not possible to make out any relationship between mean relative colonic length and the differentiation of paracaecal or parallel loops or of colonic spirals. There is no proof of a relationship between anatomical differentiations of the colonic configuration with functional characteristics, such as food quality. In his detailed study, Gorgas (1967) states that food is not the relevant factor that determines the length of the gut. For example, a causal relationship between a long absolute gut length and herbivorous nutrition does not exist. Also the relative gut length (expressed either as percentage of body length or as percentage of total length of the gut from pylorus to anus) is not related with the type of food. It has to be assumed that paracaecal or parallel loops, as well as colonic flat spiral discs or conic spirals are the result of optimal use of the available space in the abdominal cavity during ontogenetic growth. What are the mechanisms that regulate position, and shape of the intestines within the cavity? The first is represented by the internal abdominal volume. During ontogeny the available volume is not sufficient because if the rapid growth of the gut. An umbilical hernia is formed to accommodate the increasing length of the gut (Hinrichsen, 1990). The continuing elongation of the midgut, combined with increasing intra-abdominal pressure due to dramatic growth of abdominal organs, particularly the liver, forces the intestinal loop to herniate into the umbilicus (Larsen, 1993). However, it is not only the limited volume of the abdominal cavity that induces the digestive tract to form loops, discs or cones, but different

19 Hystricomorpha 

 255

Fig. 4.142: Colonic differentiations in Rodentia. The tree is modified after Veniaminova et al. (2007).

growth intensities of gut sections. In a brilliant study, Davis et al. (2008) argue that the asymmetric rotation of the primitive midgut maintains a symmetric crosssectional profile during the looping process. The biomechanical forces driving this process must originate from outside the gut tube. Under these conditions, the alternative possibility that changes in the position of the dorsal mesentery are passive responses to changes in the gut itself. In contrast, Davis et al. (2008) believe that changes in the shape of the dorsal mesentery tilt the developing midgut and induce subsequent gut rotation. The asymmetrical development of the abdominal organs is regulated by underlying molecular mechanisms (Christ and Wachtler, 1998), which are encoded by homeobox genes (Liu et al., 2001). Asymmetry at the molecular level is “converted” into asymmetries at the cellular and multicellular level (Brown and Wolpert, 1990), i.e. at the anatomical state. Forces from outside the gut, as assumed by Davis et al. (2008) may be sufficient to explain characteristic positions of different sections of the digestive tract, but certainly not the highly variable shapes of

gut parts. The craniocaudal gradient of growth, which is mentioned by Hinrichsen (1990), can contribute to characteristic shapes of gut sections. For example, the two branches of the hairpin-shaped umbilical loop behave differently during ontogeny. According to the craniocaudal growth gradient (Hinrichsen, 1990), the branch proximal to the vitelline duct elongates rapidly and intensively and rotates around a hypothetical axis that is formed by the A.  mesenterica superior and the vitelline duct, but the distal branch of the umbilical loop starts its rotational movement around the “axis” much later (Larsen, 1993). The width of the mesentery plays an important role in establishing shape and position of gut sections. For example, the position of the human colon is influenced by the fact that ascending and descending colon are fixed to the dorsal abdominal wall because the mesenteria are so reduced in width that only connective tissue, but no mesothel, can be found between gut tube and dorsal abdominal wall. However, the U-shaped form of the human colon can only be understood when we assume a lengthening of the colonic tube, a process which affords growth activity

256 

 IV Euarchontoglires – 19 Hystricomorpha

Fig. 4.143: Colonic differentiations in Rodentia under consideration of colonic length relative to total gut length (boxplots). Modified after Vorontsov (1960/1976).

in the gut wall. Not only the histogenesis is regulated by molecular stimuli (Christ and Wachter, 1998), but also the increase in length and changes in diameter. The combination of external changes influences the position of gut sections, whereas their shape is influenced by differentiated internal growth of the gut wall.

19.4.5 Differentiations of the colon wall in rodents Information of the differentiation of the wall of the large intestine of all five rodent suborders was compiled in Tab. 4.8 from the detailed studies of Gorgas (1967) and Behmann (1973) under consideration of the classical paper published by Tullberg (1899). When no differentiations are listed, insufficient information is available to be compiled in the table. In relation with the differentiation of taeniae – longitudinal muscular bands, which are formed by the stratum longitudinale of the tunica muscularis – not only the colon, but also the caecum will be considered here. In none of the Sciuromorpha (23 listed

species), Castorimorpha (one species) and Anomaluromorpha (three species) taeniae can be found in the caecum, whereas all listed species of the Hystricomorpha (30 species) differentiate two lateral caecal taeniae. The Myomorpha demonstrate considerable diversity: In the Dipodidae and Nesomyidae neither caecum nor colon differentiate taeniae, the situation in the Cricetidae is more complex: Longitudinal non-muscular bands can be found in the caecum and colon ascendens, which are responsible for the formation of semilunar folds and “sacculations” in between on the mesenterial side. The longitudinal bands are not well characterised by Behmann (1973), but in most cases, he states clearly that these bands are free of muscles. In the proximal colon (colon ascendens and colon transversum), longitudinal bands, which are identical with internal longitudinal folds, can be seen in most species of the Hystricomorpha. Snipes et al. (1988) show in cross sections through the initial segment of the proximal colon that thickening of the longitudinal muscle layer in the colon of the nutria (Myocastor coypus) is responsible for the formation of internal ridges or folds.

19 Hystricomorpha 

 257

Tab. 4.8: Differentiation of taeniae and types of food in rodents. Suborder

Family

Caecum

Colon ascendens

Colon transversum

Food

Aplodontia rufa Ratufa bicolor Sciurus vulgaris

Sciuromorpha Sciuromorpha Sciuromorpha

Aplodontidae Sciuridae Sciuridae

No No No

No No No

No No No

Juicy plants

Glaucomys volans Petaurista petaurista Pteromys volans Callosciurus pygerythrus Funambulus palmarus Menets berdmoriei Atlantoxerus getulus Spermophilopsis leptodactylus Xerus erythropus Funisciurus bayoni Heliosciurus gambianus Myosciurus pumilio Paraxerus ochraceus Spermophilus citellus Cynomys ludovicianus Marmota marmota

Sciuromorpha Sciuromorpha

Sciuridae Sciuridae

No No

No No

No No

Omnivore, seeds, nuts, small animals, eggs Tree seeds  

Sciuromorpha Sciuromorpha

Sciuridae Sciuridae

No No

No No

No No

Tree seeds  

Sciuromorpha

Sciuridae

No

No

No

 

Sciuromorpha Sciuromorpha

Sciuridae Sciuridae

No No

No No

No No

  Roots, seeds, insects

Sciuromorpha

Sciuridae

No

No

No

Plants, insects

Sciuromorpha Sciuromorpha Sciuromorpha

Sciuridae Sciuridae Sciuridae

No No No

No No No

No No No

Roots, seeds, insects    

Sciuromorpha

Sciuridae

No

No

No

 

Sciuromorpha

Sciuridae

No

No

No

 

Sciuromorpha

Sciuridae

No

No

No

Sciuromorpha

Sciuridae

No

No

No

Seeds, frains, roots, leaves Herbivore

Sciuromorpha

Sciuridae

No

No

No

Tamias striatus

Sciuromorpha

Sciuridae

No

No

No

Eutamias sibiricus

Sciuromorpha

Sciuridae

No

No

No

Geomys pinetis Thomomys bottae

Sciuromorpha Sciuromorpha

Geomyidae Geomyidae

No No

No No

No No

Castor canadensis Castorimorpha

Castoridae

No

+

+

Allactaga major Pygerethmus shitkovi Salpingotus crassicauda Dipus sagitta

Myomorpha Myomorpha

Dipodidae Dipodidae

No No

No No

No No

Herbivore, stomach contents 50% insects Nuts, seeds, fruit, corn, insects Tree seeds, berries, fruit, insects, eggs   Roots, “extremely herbivorous” Herbivore, fresh bark, green plants Plants, bulbs, bark Herbivore

Myomorpha

Dipodidae

No

No

No

Invertebrates

Myomorpha

Dipodidae

No

No

No

Jaculus jaculus Sicista betulina

Myomorpha Myomorpha

Dipodidae Dipodidae

No No

No No

No No

Napaeozapus insignis

Myomorpha

Dipodidae

No

No

No

Euphorbians, sprouts, insect larvae Grass, bulbs, roots, insects Grass seeds, berries, insects Seeds, fruits, mushrooms, invertebrates

Information is from Gorgas (1967) and Behmann (1973) under consideration of Tullberg (1899) Numbers of taeniae are given in brackets.

258 

 IV Euarchontoglires – 19 Hystricomorpha

Tab. 4.8 (continued) Suborder

Family

Caecum

Colon ascendens

Colon transversum

Food

Myomorpha

Dipodidae

No

No

No

Myomorpha

Nesomyidae

No

No

No

Seeds, fruits, mushrooms, larvae, beetles Seeds, fruits

Myomorpha

Cricetidae

Longitudinal bands

No

Microtus subterrraneus Arvicola amphibius

Myomorpha

Cricetidae

No

Myomorpha

Cricetidae

Longitudinal bands Longitudinal bands

Caryomys eva

Myomorpha

Cricetidae

Longitudinal bands

No

Dicrostonyx groenlandicus Ellobius talpinus

Myomorpha

Cricetidae

No

No

Myomorpha

Cricetidae

Longitudinal bands

No

Lemmus lemmus

Myomorpha

Cricetidae

Longitudinal bands

No

Myopus schisticolor Ondatra zibethicus

Myomorpha

Cricetidae

No

Myomorpha

Cricetidae

Longitudinal bands Longitudinal bands

Grass, herbs, agricultural produce, roots, bark Grass, herbs, roots Water plants, agricultural produce Herbivore, nuts, seeds, lichens, mushrooms, insects No Plants, grass, lichens, roots Beets, bulbs, rhizomes, blossoms, herbs Grasses, bark, leaves, roots, lichens Masses, bark

Reithrodontomys megalotis Peromyscus sp.

Myomorpha

Cricetidae

No

No

Water plants, agricultural produce, mussels No Seeds, sprouts, insects

Myomorpha

Cricetidae

No

No

No

Oryzomys subflavus Oxymycterus sp. Cricetulus migratorius Cricetus cricetus

Myomorpha

Cricetidae

No

No

No

Myomorpha Myomorpha

Cricetidae Cricetidae

No No

No No

No No

Myomorpha

Cricetidae

No

No

No

Acomys mullah Deomys ferrugineus Deomys ferrugineus Lophuromys sikapusi Tatera sp.

Myomorpha Myomorpha

Muridae Muridae

No No

No No

No No

Myomorpha

Muridae

No

No

No

Myomorpha

Muridae

No

No

No

Myomorpha

Muridae

+ (1)

No

No

Gerbillus nanus

Myomorpha

Muridae

+ (1)

No

No

Zapus hudsonicus Cricetomys gambianus Microtus oeconomus

No

No

Information is from Gorgas (1967) and Behmann (1973) under consideration of Tullberg (1899) Numbers of taeniae are given in brackets.

Seeds, fruits, berries, insects, invertebrates Grasses, fruits, fish, invertebrates Insects Sprouts, seeds Omnivores, grains, legumes, grass, herbs, insects, small mammals Omnivore Snails, insects, small animals Snails, aquatic insects Herbivore, worms, caterpillar, larvae Bulbs, roots, seeds, plant parts Seeds, roots, grass, insects

19 Hystricomorpha 

 259

Tab. 4.8 (continued) Suborder

Family

Caecum

Colon ascendens

Colon transversum

Food

Meriones crassus

Myomorpha

Muridae

+ (2)

No

No

Nesokia indica Apodemus flavicollis Hydromys chrysogaster

Myomorpha Myomorpha

Muridae Muridae

No + (1)

No No

No No

Myomorpha

Muridae

No

No

No

Myomorpha

Muridae

+ (1)

No

No

Myomorpha Myomorpha Myomorpha

Muridae Muridae Muridae

No No + (1)

No No No

No No No

Seeds, leaves, tubers, roots Grass, roots, grains Seeds, shoots, roots, insects Mussels, crustaceans, snails, fish, frogs, plant parts Soft seeds, bananas, potatoes, manioc Seeds, insects Omnivore Herbivore, insects

Myomorpha Myomorpha

Muridae Muridae

No + (1)

No No

No No

Spalax sp. Spalax leucodon Tachoryctes sp. Anomalurus derbianus Idiurus zenkeri

Myomorpha Myomorpha Myomorpha Anomaluromorpha

Spalacidae Spalacidae Spalacidae Anomaluridae

Spiral Spiral Spiral No

No No No No

No No No No

Anomaluromorpha Anomaluridae

No

No

No

Pedetes capensis

Anomaluromorpha Pedtidae

No

No

No

Ctenodactylus Hystricomorpha gundi Cryptomys bocagei Hystricomorpha Georychus Hystricomorpha capensis

Ctenodactylidae No

No

No

Bathyergidae Bathyergidae

+ (2) + (2)

Heliophobius argenteocinereus Atherurus africanus Hystrix cristata Ctenomys mendocinus Makalata didelphoides Thrichomys aperoidea Trichomys albispinus Kannabateomys amblyonyx Thryonomys swinderianus Coendou prehensilis Erethizon dorsatum

Hystricomorpha

Bathyergidae

+ (2)

Hystricomorpha

Hystricidae

+ (2)

Longitudinal bands Roots, bulbs Longitudinal bands Bulbs, roots, seeds, plant parts Longitudinal bands Roots, bulbs, insects Longitudinal bands Herbivore

Hystricomorpha Hystricomorpha

Hystricidae Ctenomyidae

+ (2) + (2)

Longitudinal bands Herbivore No No

 

Hystricomorpha

Echimyidae

+ (2)

No

 

Hystricomorpha

Echimyidae

+ (2)

Longitudinal bands Fruits

Hystricomorpha

Echimyidae

+ (2)

No

Hystricomorpha

Echimyidae

+ (2)

Longitudinal bands  

Hystricomorpha

Thryonomyidae

+ (2)

Longitudinal bands Herbivore

Hystricomorpha

Erethizontidae

+ (2)

Longitudinal bands Herbivore

Hystricomorpha

Erethizontidae

+ (2)

Longitudinal bands Tree shoots, bark

Lemniscomys striatus Micromys minutus Mus musculus Pogonomys macrourus Rattus norvegicus Otomys sp.

Information is from Gorgas (1967) and Behmann (1973) under consideration of Tullberg (1899) Numbers of taeniae are given in brackets.

No

No

Omnivore Seeds, berries, grass, roots, sprouts, bark Roots, bulbs   Grass, bulbs, roots Leaves, blossoms, unripe fruits, soft wood Mainly insects, some plant parts Roots, leaves, fruits, insects Herbivore

 

260 

 IV Euarchontoglires – 19 Hystricomorpha

Tab. 4.8 (continued) Suborder

Family

Caecum

Colon ascendens

Colon transversum

Chinchilla lanigera Lagidium peruanum Lagostomus maximus Cavia sp. Microcavia australis Dolichotis patagonum Hydrochoerus hydrochaeris

Hystricomorpha Hystricomorpha

Chinchillidae Chinchillidae

+ (2) + (2)

Longitudinal bands Herbivore Longitudinal bands Herbivore

Hystricomorpha

Chinchillidae

+ (2)

Longitudinal bands Herbivore

Hystricomorpha Hystricomorpha

Caviidae Caviidae

+ (2) + (2)

Longitudinal bands Herbivore Longitudinal bands Plants, insects

Hystricomorpha

Caviidae

+ (2)

Longitudinal bands Herbivore

Hystricomorpha

Caviidae

+ (2)

Kerodon rupestris Dasyprocta agouti Myoprocta acouchy Cuniculus paca Octodon degus Spalacopus cyanus Abrocoma bennettii Myocastor coypus

Hystricomorpha

Caviidae

+ (2)

Longitudinal bands Grass, aquatic plants, bark, agricultural produce Longitudinal bands Herbivore

Hystricomorpha Hystricomorpha

Dasyproctidae Dasyproctidae

+ (2) + (2)

Longitudinal bands Fruits Longitudinal bands Fruits

Hystricomorpha Hystricomorpha Hystricomorpha

Cuniculidae Octodontidae Octodontidae

+ (2) + (2) + (2)

Longitudinal bands Fruits Longitudinal bands Purely vetarian Longitudinal bands  

Hystricomorpha

Abrocomidae

+ (2)

Longitudinal bands  

Hystricomorpha

Myocastoridae

+ (2)

Mysateles prehensilis Plagiodontia aedium

Hystricomorpha

Capromyidae

+ (2)

Hystricomorpha

Capromyidae

+ (2)

Longitudinal bands Roots aquatic grasses, snails, mussels Longitudinal bands Leaves, bark, fruits No No

Food

Leaves, blossoms, unripe fruits, soft wood

Information is from Gorgas (1967) and Behmann (1973) under consideration of Tullberg (1899) Numbers of taeniae are given in brackets.

In the Muridae, the situation in the wall of the colon is quite uniform, i.e. no taeniae are differentiated in the colonic wall, but in the caecal wall, in 7 of the 16 listed species of the Muridae, either one or two taeniae are differentiated and documented. In another family of Myomorpha, in the Spalacidae, an internal valva spiralis can be found in the caecum, whereas the muscular colonic wall in this family does not show differentiations. In beavers, Castoridae, we find a non-hystricomorph rodent with taeniae in the colon. However, the information given by the literature is quite controversial. Gorgas (1967) states that there are no lateral taeniae in the beaver colon, although the musculature between the sacculations looks similar to taeniae (“Die Längsmuskelschicht […] zwischen den Sacculi erscheint taenienartig”, page 303). On the other hand, Tullberg (1899) mentions that the colon of Castor canadensis – with the exception of the colon

descendens – is intensively haustrated (sacculated). In an illustration (Fig. 4.78), Tullberg (1899) clearly depicts a lateral taenia in the proximal colonic wall. Summing up, it can be stated that muscular differentiations of the rodent colon can only be found in beavers (Castoridae), whereas the caecum shows taeniae in some species of the Muridae and in Hystricomorpha. 19.4.6 Macroscopically visible internal differentiations of the colon Concerning availability of information on the internal lining and differentiation of the colon, the situation is quantitatively very unbalanced when different rodent suborders are compared. Only little information is available for Sciuromorpha, Castorimorpha and Anomaluromorpha. On the other hand, very detailed and

19 Hystricomorpha 

diverse information is given for Myomorpha, especially for rat (Rattus norvegicus) and mouse (Mus musculus), as well as for Hystricomorpha, of which the guinea pig (Cavia porcellus) has been intensively studied by many investigators. The macroscopic differentiation of the internal mucosal lining of the colon in Myomorpha has been carefully studied and described for more than 40 species by Behmann (1973). Gorgas (1967) dealt with Sciuromorphy, Castorimorpha, Anomaluromorpha and Hystricomorpha. A few other researchers studied and described the internal lining of a few rodent species (Tab. 4.8). In this table, only those differentiations are listed that are clearly mentioned in the texts of different authors. This means that empty spaces in the table do not represent a structure that is not differentiated, but is simply not mentioned by the authors. It can generally be said for all species that it is the ascending colon, and especially the proximal part of this section, that shows the most intensive differentiation. In this part of the colon, Behmann (1973) speaks of a Kerckring network (“Kerckring-Winkelfalten-Relief”). This terminology can lead to confusion because the literature on human and domestic animal anatomy presents the misleading impression that Kerckring’s folds or “valves of Kerckring” are strictly circular folds (“Plicae circulares”), as described for the human small intestine by Gray and Goss (1973) or Moore (1992), or for the small intestine of domestic mammals by Grau (1960), or for mammals in general (Grassé, 1973). It has to be emphasised that a mucosal fold in general is an epithelial “projection with an indented basal surface, into which the underlying mesenchyme protrudes” (Johnson, 1913, page 191). It was Cremer (1921), who clearly stated that Kerckring’s folds are not necessarily strictly circular. In his study on the foetal human gut, he found that circular folds can be connected with short longitudinal folds, thus forming a net-like or reticular system of folds. In addition, he also made clear that Kerckring’s folds are not necessarily differentiations of the small intestine. During ontogeny they are also formed in the large intestine, but in man a reduction and final complete dissolution of this fold system takes place during the perinatal period. Foetal folds in the colon are not related to the plicae semilunares of the adult colon, they are only ontogenetically transient structures (Johnson, 1913); these semilunar folds are differentiated later than folds of the Kerckring system and are strictly related with taeniae in the gut wall (Jacobshagen, 1937). An overview about the differentiation of the macroscopically visible internal differentiations of the colon has been compiled in Tab. 4.9 The following internal structures have been considered: Circular folds (CF) with epithelial elevations on a “skeleton” of connective tissue, which belongs to the lamina propria mucosae, secondly folds

 261

belonging to the Kerckring network system (KN), which is also formed under participation of the lamina epithelialis mucosae and the lamina propria mucosae, and, third, the longitudinal folds (LC), which are the effect constriction of the stratum circulare of the tunica muscularis. The fourth type of differentiation are longitudinal folds (LF), which are formed by the lamina propria mucosae, which protrudes towards the lumen, but is separated from it by the lamina epithelialis mucosae. Oblique folds (OF) have the same architecture as the just mentioned longitudinal folds, but do neither run longitudinally along the lumen, nor do they encircle the lumen like plicae circulares. The oblique folds run, as seen from the antimesenterial side, caudad and towards the mesenterial side of the colonic tube. Finally, semilunar folds (SF), which have already been characterised above, can be differentiated in the colon, for example in the Canadian beaver (Castor canadensis), where it can be found in the colon ascendens, transversum and descendens. As there is only information for one species of the Castorimorpha available, it cannot be said whether semilunar folds are characteristic for the colon of all representatives of the suborder Castorimorpha. Especially at the very beginning of the colon ascendens, right after the caecocolic aperture, the Kerckringnetwork has been found by Behmann (1973) in many myomorph species, especially in Dipodidae, a few Cricetidae, Gerbillinae and Murinae within the Muridae. On the other hand, longitudinal folds can be found in Arvicolinae, a subfamily of the Cricetidae, as well as in Spalacidae, in the suborder Anomaluromorpha, as well as in the hystricomorph families Chinchillidae, Caviidae, Myocastoridae and Capromyidae. In these hystricomorph taxa, longitudinal folds cannot only be found in the direct proximity of the caecocolic aperture, but in the total colon ascendens. In the Myomorpha, on the other hand, the second section of the ascending colon has an internal lining with oblique folds, the “Kerckring-Winkelfalten-Relief” of Behmann (1973). The side of the rodent colon ascendens that is orientated towards the line of fixation of the mesocolon is called the “dorsal” side (Behmann, 1973), which is ontogenetically defined. Along this side a groove can be found in Myomorpha, Anomaluromorpha and Hystricomorpha. In many species, one or two longitudinal folds that start at the opening of the ileum into the large intestine, line the “dorsal” groove and form “abutments”, on which plicae semilunares can be formed with haustra between them. It is interesting that Behmann (1973) stated explicitly in certain cases, such as some Dipodidae and in some Muridae (e.g. Acomys mullah, Gerbillus pyramidum, Micromys minutus) that a groove is not differentiated. The oblique folds that extend on both sides of the groove in sail-like processes have been described for myomorph species.

262 

 IV Euarchontoglires – 19 Hystricomorpha

Tab. 4.9: Differentiations of the colon in rodent species.

Suborder

Family

Taxon Sub-family

Genus and species

Reference

proximal

Sciuromorpha Castorimporpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha

Sciuridae Heteromyidae Dipodidae Dipodidae Dipodidae Dipodidae Dipodidae Dipodidae Dipodidae Dipodidae Nesomyidae

Citellus citellus Castor canadensis Allactaga major Pygeretmus shitkovi Salpingotus crassicauda Dipus sagitta Jaculus jaculus Sicista subtilis Napaeozapus insignis Zapus hudsonicus Cricetomys gambianus

Gorgas (1967) Gorgas (1967) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973), Knight and Knight-Eloff (1987) Behmann (1973, Amasaki et al. (1988) Behmann (1973) Behmann (1973) Behmann (1973)

CF SF KN, LF KN, LF KN, LF-OF KN, 8 LF, OF KN KN KN KN

Myomorpha

Cricetidae

Arvicolinae

Microtus arvalis

Myomorpha Myomorpha Myomorpha

Cricetidae Cricetidae Cricetidae

Arvicolinae Arvicolinae Arvicolinae

Myomorpha Myomorpha

Cricetidae Cricetidae

Arvicolinae Arvicolinae

Microtus subterraneus Arvicola amphibius Dicrostonyx groenlandicus Ellobius talpinus Lemmus lemmus

Myomorpha Myomorpha Myomorpha Myomorpha

Cricetidae Cricetidae Cricetidae Cricetidae

Arvicolinae Arvicolinae Arvicolinae Neotominae

Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha Myomorpha

Cricetidae Cricetidae Cricetidae Cricetidae Cricetidae Muridae Muridae Muridae Muridae Muridae Muridae Muridae Muridae Muridae Muridae Muridae Muridae Muridae Muridae

Neotominae Sigmodontinae Sigmodontinae Cricetinae Cricetinae Deomyinae Deomyinae Deomyinae Gerbillinae Gerbillinae Gerbillinae Murinae Murinae Murinae Murinae Murinae Murinae Murinae Murinae

Myomorpha Myomorpha Myomorpha Anomaluromorpha Hystricomorpha Hystricomorpha

Muridae Spalacidae Spalacidae Pedetidae Bathyergidae Bathyergidae

Otomyinae

Myodes glareolus Myopus schisticolor Ondatra zibethicus Reithrodontomys megalotis Peromyscus spec. Oryzomys subflavus Oxymycterus sp. Cricetulus migratorius Cricetus cricetus Acomys mullah Deomys ferrugineus Lophuromys sikapusi Tatera sp. Gerbillus pyramidum Meriones crassus Nesokia indica Apodemus flavicollis Hydromys chrysogaste Lemniscomys striatus Micromys minutus Mus musculus Pogonomys macrourus Rattus norvegicus Otomys irroratus Spalax sp. Tachyoryctes sp. Pedets sp. Cryptomys hottentotus Georychus capensis

Behmann (1973) Behmann (1973), Sperber et al. (1983), Björnhag and Snipes (1999) Behmann (1973) Behmann (1973) Luppa (1961), Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Behmann (1973) Hebel (1969b), Behmann (1973), Sperber et al. (1983) Behmann (1973) Behmann (1973) Behmann (1973) Gorgas (1967) Perrin and Curtis (1980) Gorgas (1967)

LF LF LF

one LF LF LF KN LF, KN LF, KN KN LF

7 LF 7 LF KN KN KN KN LF KN KN KN, OF KN KN, LF KN 2 LF 2 LF 1 LF many LF OF

F: circular fold; KN: “Kerckring” network; LC: longitudinal constriction folds; LF: longitudinal folds; OF: oblique folds; SF: semilunar folds

19 Hystricomorpha 

Colon ascendens

distal SF OF OF OF OF

Longitudinal folds

Colon On mesenterial side “Sail-like” process

Colon transversum

Colon descendens

SF

SF

LC

LC

diff

(OF)

LC

Groove

LC diff diff

diff not diff not diff not diff

OF OF

2 LF

OF OF

2 LF 2 LF 2 LF

not diff diff

diff diff diff

LC

LC

4–5 LC

4–5 LC

OF OF

2 LF 2 LF

diff

diff

LC

LC

OF KN OF

2 LF

diff

(OF) LC LC LC

LC LC LC LC

LC

LC

LC 7 LF

LC 7 LF

LC KN

LC KN

LC

LC

OF

OF

OF OF, KN OF, KN OF, KN KN 7LF OF

KN

2 LF

2 LF 2 LF

(diff)

diff diff

7 LF

not diff diff diff not diff

KN

No folds in colon

yes

diff

OF

diff not diff

OF (2 rows)

diff diff

KN KN KN CF OF

Colonic Separation Mechanism

LF

diff

LF

diff

LF

diff

yes

 263

264 

 IV Euarchontoglires – 19 Hystricomorpha

Tab. 4.9 (continued)

Suborder

Family

Hystricomorpha Hystricomorpha

Bathyergidae Thryonomyidae

Hystricomorpha

Taxon Sub-family

Genus and species

Reference

proximal

Kotzé et al. (2009) Gorgas (1967)

Chinchillidae

Heterocephalus sp. Thryonomys swinderianus Chinchilla lanigera

Hystricomorpha

Caviidae

Cavia porcellus

Hystricomorpha Hystricomorpha

Caviidae Myocastoridae

Dolichotis patagonum Myocastor coypus

Hystricomorpha

Capromyidae

Capromys prehensilis

Gorgas (1967), Holtenius and Björnhag (1985), Björnhag and Snipes (1999) Gorgas (1967), Holtenius and Björnhag (1985), Björnhag and Snipes (1999) Weissengruber (2000) Kämmerer and Wetzig (1966), Gorgas (1967), Snipes et al. (1988), Björnhag and Snipes (1999) Gorgas (1967)

2 LF

2 LF

2 LF 2 LF

LF

F: circular fold; KN: “Kerckring” network; LC: longitudinal constriction folds; LF: longitudinal folds; OF: oblique folds; SF: semilunar folds

Sperber et al. (1983) give an excellent illustration of the situation (Fig. 4.144): The two depicted oblique folds (OF) have free sail-like edges, which “cover” the groove (Gr) and separate it from the main lumen (Lu). This illustration gives an idea of two lumina that are set off from each other, but not totally separated from each other. The illustration does not depict any trace of cross-sectioned longitudinal folds lining the groove. It is plausible that oral-aboral transport can move digesta through the main lumen and synchronously allow retrograde transport in the groove. The colonic separation mechanism (CSM) has been described in detail by Sperber et al. (1983) and Björnhag and Snipes (1999). Fine particles, including microbes, are transported in retrograde direction through the groove on the mesenterial side, the main bulk of digesta is transported aborally. 19.4.7 Histological differentiations of the colonic internal lining Before this paragraph will give some information on the internal lining of the rodent colon, a few remarks on function and ontogeny of the colon will be made. The herbivore gut is capable of considerable modification to respond to varying diet quality or metabolic demands. According to Breton et al. (1989), Microtus ochrogaster (Prairie vole) and Peromyscus maniculatus (North American deermouse), which are both myomorph species, increase their gut length and wet mass in response to a decrease in digestible energy content of their diet. An increase in their energy requirements can also be

Lu

OF

OF Gr Ms

Fig. 4.144: Cross-section of a turn of the outer colonic spiral of Lemmus lemmus. Abbreviations: OF: “sail-like” processes on the end of two oblique folds; Ms: Tunica muscularis; Gr: groove on the mesenterial side of the tube; Lu: main lumen of the colon. From Sperber et al. (1983).

responsible for an increase in gut length. The presumed function of these gut modifications is to increase the net uptake of energy. It should already be mentioned here that separate presentation and discussion of caecal and colonic characters does not mean that these two sections of the large intestine are totally separated from each

19 Hystricomorpha 

Colon ascendens

distal

Longitudinal folds

Colon On mesenterial side “Sail-like” process papillae

Colon transversum

Groove

Colon descendens

 265

Colonic Separation Mechanism

diff diff, SF

2 LF

2 LF

diff

2 LF

2 LF

diff

2 LF 2 LF

2 LF 2 LF

diff, SF diff

LF

2 LF

other. Sakaguchi et al. (1985) observed that the caecum and upper section of the proximal colon in Cavia porcellus (Hystricomorpha) have mixed contents in normal animals and formed a common fermentation chamber. At the end of the first week after birth facultative anaerobes colonise the total bowel – not only the colon – of the mouse (Mus musculus) to high population levels (Savage, 1978). Many microbial types establishing themselves in the murine tract do so by colonising layers of mucin on the various epithelial surfaces. When the animal begins to sample solid food, oxygen-intolerant anaerobic bacteria colonise the large bowel of rodents after the tract has been colonised by facultative or oxygen-tolerant bacteria. The function of the luminal mucin of the large intestine has been suggested to be protection, lubrication and barrier for the transport of solutes (Sakata and Engelhardt, 1981b). However, according to these authors, mucin does not form a continuous layer and therefore may not be an effective mechanical protection. Second, mucin in the caecum lacks acid mucin which is considered to be important for the protection. Fibre-induced increase in gastrointestinal mucin production may be responsible for more rapid transit times (Satchithanandam et al., 1990). Although the digesta in the proximal colon are more fibrous in guinea pigs than in mice or rats, the mucin layer in guinea pigs is thinner and less compact than in the other species. No penetration of digesta into the mucin layer or into the mucosa was seen. Finally, sulpho-mucin, which is believed to be responsible for lubrication, is not present in the proximal colon luminal mucin layer. Sakata and Engelhardt (1981b) assume that the major function of the

luminal mucin in the caecum and in the proximal colon is to provide a favourable condition for certain microorganisms and to form a special micro-environment with these microorganisms at the epithelial surface. In the distal colon, a compact mucin layer protects the mucosa. According to Takahashi and Sakaguchi (2006), who studied the large intestine of Cavia porcellus, the guinea pig, this part of the intestine in mammals may have several different micro-environments and there may be a complex system of fermentation within the lumen. A stable pH microclimate at the surface of the epithelium of the gastrointestinal tract has been demonstrated by Rechkemmer et al. (1986). The physiological function of a pH microclimate may be different in the various gastrointestinal segments of Cavia porcellus and Rattus norvegicus. For the large intestine, Rechkemmer et al. (1986) produced evidence that the microclimate provides the basis for a constant absorption of short-chain fatty acids independent of changes in luminal pH. The microclimate thus functions as a barrier against rapid diffusion of luminally produced short-chain fatty acids at low luminal pH, which potentially could acidify the intracellular pH and damage the epithelial cells. A neutral pH is present in all intestinal segments of the guinea pig as well as in the rat. In the proximal colon, the mucus layer contains mainly neutral mucins, whereas in the distal colon acid mucins dominate. The vascular system in the colonic mucosa in the rat, apart from catering to the needs of a secretory epithelium, removes water absorbed across the epithelium, thereby returning this water to the general circulation (Browning and Gannon, 1986). The human colon removes 80–90%

266 

 IV Euarchontoglires – 19 Hystricomorpha

of the water that has entered into it (Kerlin and Phillips, 1983) and it is capable of absorbing far greater quantities of water when the amount passing to it is higher than normal. The proximal colon (and the caecum) of Cavia porcellus are regions responsible for absorbing the excess of fluid. The distal colon, on the other hand, contributes little to total water and sodium absorption (Rechkemmer and Engelhardt, 1981). According to Luciano et al. (1984), the crypts in the colon of the guinea pig seem to have mainly a secretory function for chloride or macromolecules; very likely, crypts do not play a major role in absorption. Short-chain fatty acids are absorbed across the surface cells of the colonic epithelium between the crypts and not in them. Morphologically, the colon of the rat (Rattus norvegicus) develops about 1 day after the small intestine (Potter et al., 1983) and shows internal differentiations that are characteristic for other gut sections in adults. For example, the foetal colon, not only of the rat, but in mammals in general, has villi rather than a flat epithelium. Both the small and large intestinal mucosae of Rattus norvegicus develop three types of epithelial cells, which are practically identical in the two organs (Helander, 1973). The most important differences relate to the chronology of the development – events of similar nature generally take place a few days earlier in the small intestine than in the colon. Also, after copying many features from the small intestine, the colon goes into its own, special development, abandoning such features as villi. At birth, the development of the rat colon is usually well advanced, but by no means finished at birth (Helander, 1975). For example, some of the enzymes of the colonic mucosa reach peaks of activity during the neonatal period, suggesting that the colonic mucosa may have a different function in the infant than in the adult. In addition, Urban et al. (1978) demonstrated a proximal to distal absorption gradient in the large bowel of Rattus norvegicus. After a fasting period, there is a huge burst in colonic proliferative activity in response to refeeding (Hagemann and Stragand, 1977). Following this, the response in the colon in Mus musculus coincides with entry of the G1-phase of the cell cycle. During this phase, the biosynthetic activities of the cell increase considerably. Studies in the rat colon by Shamsuddin and Trump (1981) show clearly that three types of cells can be formed from undifferentiated ones: mucous cells, columnar cells, intestinal endocrine cells. The dividing cells in the colon of the rat are concentrated in the lower portions of the crypts. From this location the new cells migrate towards the surface of the mucosa (Helander, 1973). In studies of Gutschmidt et al. (1983) in the colon of Rattus norvegicus, there was a gradual significant decrease in the number of crypts and

in the surface of these crypts per unit area from caecum to rectum. There was an increase in the surface of the epithelium between the crypts. The proximal-to-distal decrease in the overall surface, especially between the caecum and ascending colon on the one hand and the descending colon and rectum on the other, substantiates the impression of a decrease in the mucosal folds apparent to the naked eye.

19.4.8 The colonic separation mechanism and colonic anatomy Sperber et al. (1983) gave a detailed account of the relationship between the anatomy and the colonic separation mechanism in two species of the Myomorpha, the Scandinavian lemming (Lemmus lemmus) and the Norway rat (Rattus norvegicus). According to this author, the proximal colon in the lemming may be divided into the following sections: The ampulla coli is the short wide part from the entry of the ileum to the base of the colonic spiral. The first part of the spiral is made up of about four windings which are held together by the axial mesenterial structure (Fig. 4.93). At the apex, the inner spiral is continued by the outer spiral which runs down towards the base where it leaves the colonic spiral and passes into the distal colon. The windings of the outer spiral are attached to the axial structure by fairly wide mesenteries. At least three features appear peculiar to the lemming colon: A longitudinal fold which divides the two first windings of the colonic spiral into two parallel channels; second, the distribution of the intestinal contents between the two channels; third, the heavy thickening of the mucosa at the end of the longitudinal fold (Sperber et al., 1983). The longitudinal fold almost completely divides the lumen of the two basal windings of the inner spiral into two channels, the narrow and the main channel. At its distal end the narrow channel is continued by a longitudinal groove with connected oblique furrows in the colonic wall (Fig. 4.144). From the middle of the inner spiral to the end of the proximal colon these oblique mucosal folds form two longitudinal rows, each fold running from the antimesenterial midline in an obliquely transverse proximal direction, ending before it reaches the mesenterial midline. As the base of the folds does not extend into the midline on the mesenterial side, the above-mentioned groove is formed. This groove is (incompletely) separated from the lumen of the colon by the “sail-like” processes of the folds, which form a sort of roof to the groove. The caecal contents in the lemming appear as a mixture of food residues and bacteria (Sperber et al., 1983). The mucosa of the proximal colon has a relatively complicated pattern of permanent folds which project

19 Hystricomorpha 

into the lumen. The largest of these folds, the longitudinal fold, runs along the colon for about two windings, starting at the end of the ampulla coli. Sperber et al. (1983) give a detailed account of a mechanism, which separates most of the bacteria in the colonic contents from the food residues and returns them to the caecum. This process is made possible by the structure of the proximal colon, which mainly consists of a double spiral similar to that which is depicted for the lemming in Fig. 4.93. It has already been mentioned that the mucosa of this colonic spiral is provided with a longitudinal fold running along the first two windings of the spiral, separating a narrow channel almost completely from the main lumen. The narrow channel regularly contains bacteria mixed with mucus, but hardly any food residues, which are abundant in the main lumen (Sakaguchi, 2003). The mucus is produced by tubular glands in a considerable mucosal thickening distal to the longitudinal fold. This heavy thickening of the mucosa at the end of the longitudinal fold has already been mentioned above. The bacteria mixed with mucus are separated from the food residues in the longitudinal groove of the more distal parts of the colonic spiral (Fig. 4.144). The bacteria accumulate in this groove and are brought back to the caecum via the narrow channel. Haustral dilation and contraction can transport fine particles in retrograde direction. In the lemming, the colonic separation mechanism appears essential for the capacity of the animal to digest the food of low digestibility which is normally eaten in large quantities. The effect of this process is that at the end of the digestive tract very few microbes are seen among the food residues in the faeces. Only at the beginning of the spiral colon the furrow or groove the contents of microbes is high. “Lemmings have only one type of faeces and practise coprophagy” – this means that “the presence of the separation mechanism is not always linked to caecotrophy” (Hörnicke and Björnhag, 1980, page 715). Rattus norvegicus forms two types of faecal pellets, one of which has higher protein content and is eaten by the rat (Sperber et al., 1983). The other type is formed by a separation process similar to that of the lemming. In the proximal colon, which contains two rows of oblique folds, a part of the bacteria in the colonic contents are concentrated in a layer of mucus, mainly between the folds. The mixture of bacteria and mucus is most probably brought back into the caecum by retrograde transport. Sakaguchi (2003) illustrates the separation via haustra. In the rat, the separation mechanism leads to a considerable saving of protein and energy and contributes to the process of coprophagy. The mechanisms found in the lemming and the rat appears to be of a fundamentally different type. In the lemming, bacteria are separated from the normal

 267

food and not lost from the caecum. The colonic separation mechanism makes it possible for the lemming to digest a food of low digestibility because the highly nutritious bacteria are accumulated in the groove on the mesenterial side and are brought back to the caecum via the narrow channel of the first colonic segment (Sperber et al., 1983). In the rat, two types of faecal pellets are produced, the “normal” type with degraded digesta and another type, which has high protein content, making the process of coprophagy valuable to the nutrition of the animal (Sperber et al., 1983). Holtenius and Björnhag (1985) studied the colonic separation mechanism in two representatives of the Hystricomorpha, the guinea pig (Cavia porcellus) and the chinchilla (Chinchilla lanigera). Under consideration of colonic anatomy they elucidated the mode of production of special faeces that is eaten in the caecotrophic hystricomorphs. In the groove or furrow on the mesenterial side of the proximal colon, they found that the concentration of nitrogen in the digesta contents is significantly higher than in the main colonic lumen. The nitrogen concentration in the main lumen decreases significantly along the first half of the proximal colon, nitrogen absorption – which is low – cannot explain the decrease. The only reliable explanation of the difference in nitrogen concentration between the contents of the groove and the main lumen is transport of nitrogen-rich matter from the main lumen into the furrow. Holtenius and Björnhag (1985) stated that most of the nitrogen transported to the groove in the form of bacteria, which can be reingested. An overview on the reingestion of faeces and on the differentiation between coprophagy and caecotrophy has been presented by Hörnicke and Björnhag (1980). In addition to Lagomorpha and a few primates, caecotrophy was documented in the following rodents: Two representatives of the Sciuromorpha, Spermophilus citellus (ground squirrel) and Aplodontia rufa (mountain beaver) as well as the Eurasian beaver (Castor fiber) (Castorimorpha) and two hystricomorph species: Heterocephalus glaber, the naked mole rat, and the chinchilla (Chinchilla lanigera). The caecotrophes found in the distal colon always showed higher nitrogen concentrations than in the caecal contents. The guinea pig differs in this respect from what is found in the rat. This species produces faecal pellets with about the same nitrogen concentration as that found in the caecal contents (Sperber et al., 1983). In the guinea pig, special pellets – caecotrophes – are produced. Their nitrogen concentrations are very similar to the concentrations found in the contents of the colonic groove. Antiperistalsis of the haustra ceases from time to time to bring the contents of the groove into the distal colon, from where it is forwarded to the rectum and then taken up by the guinea pig. The guinea pig produces two types

268 

 IV Euarchontoglires – 19 Hystricomorpha

of pellets. The two types differ considerably in bacterial content. To produce these two types of pellet, bacteria are probably trapped in mucin and moved to the furrow. The material remaining in the main lumen are given off as faecal pellets. The surplus bacteria are transferred into the special caecotroph pellets and used by the guinea pig. The mechanism of separation and retrograde transport also maintains the bacterial concentration and the fermentation capacity of the caecal contents at high levels (Holtenius and Björnhag, 1985). The guinea pig does not have distinct ingestion periods for their caecotrophes, which contain more nitrogen than the “normal” pellets (Hörnicke and Björnhag, 1980). According to these authors, the chinchilla also produces two types of faeces with different nitrogen content, which are excreted during the day and which contain twice the nitrogen content of the faecal pellets that are excreted during the night. The importance of haustra for the separation mechanism differentiating between coarse and fine particles, including microbes, has been elucidated by Snipes et al. (1988) for the hystricomorph nutria, Myocastor coypus. Externally, the proximal colon is haustrated (Fig. 4.131, upper panel). Internally, the intestinal wall is characterised on the mesenteric side by a longitudinally running groove or furrow delineated on both sides by an elevation of the intestinal wall in the form of ridges. Distal to the flexure of the parallel loop, all these structures are missing. It is in this distal segment (the distal colon) where formed faeces (scybala) are present, the content of the proximal colon is not formed, but fluid (chyme). It is uncertain whether the thickenings of the longitudinal layer beneath the two ridges can be considered as true taeniae. Biomechanically, however, the two ridges present in the proximal colon of the nutria, as well as in several other rodents (Gorgas, 1967), act like taeniae in anchoring the circular muscle in the process of haustra formation. Thus, it seems appropriate to extend the term “haustrated” to all guts where relatively rigid longitudinal structures like taeniae or ridges present two “anchors” for the circular musculature that forms “outpockets” or haustra. Outside the area of the ridge-lined furrow, the proximal colon demonstrates prominent plicae longitudinales. These are interpreted as a means of surface enlargement (Kämmerer and Wetzig, 1966). From measurements by Snipes et al. (1988), the proximal colon of the nutria has a histological surface enlargement factor (SEF) of approximately 2.5 compared to 1.4 in the distal colon where these structures are not present. Surface enlargement in the former area can be envisioned as being important for the secretory functions and water absorption of this area. The groove at the mesenterial side of the proximal colon

is distinguished by its transport properties and by its motility from the main circumference of this gut region. In Myocastor coypus, the furrow and main lumen do not represent separated compartments. Nevertheless, clear differences in composition of the digesta from the two regions with respect to water content, Na, Ca, Cl and K concentrations have been found. Differential motility of the groove and the main lumen similar to the illustration depicted by Sakaguchi (2003) are to be expected.

19.5 Caecum of Hystricomorpha A schematic overview, dealing with different orders of the Euarchotoglires, has already been given in Tab. 4.1. In the rodent suborder Hystricomorpha, the caecal wall shows taeniae as special differentiations of the external longitudinal layer of the tunica muscularis. This is illustrated in a tree (Fig. 4.145) that was adapted from Veniaminova et al. (2007), but is not in total accordance with the systematic classification presented by Wilson and Reeder (2005). Taeniae liberae (not covered by a line of fixation of a mesenterium) can be seen on all outlines of caeca in the Hystricomorpha (Fig. 4.145). This fact is certainly related with the type of food these animals eat. For reasons of comparison not only outlines of the caecal types in Hystricomorpha are presented, but also of Myomorpha and Anomaluromorpha. In the Myomorpha, there is a tendency towards the development of caecal taeniae.

19.5.1 The caecum of Bathyergidae The Bathyergidae were already dealt with in the chapter on the colon. The gut is depicted in Fig. 4.123, presenting information on Bathyergus suillus (Cape dune mole rat), originally published by Tullberg (1899), on Cryptomys bocagei (Bacage’s mole rat) and Heliophobius argenteocinereus (Silvery mole rat), both originally from Gorgas (1967). In an excellent comparative study, Kotzé et al. (2010) published illustrations of the digestive tracts of six species of mole rats (Hystricomorpha; three subspecies of Cryptomys hottentotus). From these illustrations, the present author “extracted” the caecal region, brought the caeca into comparable position, indicated the number of caecal taeniae according to Kotzé et al. (2010) and marked the influx via the ileum and the efflux via the colon ascendens (Fig. 4.146, the caeca are marked in grey). The food of species of Cryptomys hottentotus; the Southern African mole rat, consists of succulent underground organs of plants, tubers and bulb, roots and succulent underground stolons of grasses (Bennett and Jarvis, 2004;

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Fig. 4.145: Outlines of the caecum in Myomorpha, Anomaluromorpha and Hystricomorpha. When present, taeniae are marked in black. Marked scale-bars represent 1 cm, unmarked bars 5 cm. Morphological data are adapted from Gorgas (1967), Behmann (1973) and Naumova (1981), the tree adapted from Veniaminova et al. (2007).

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Skinner and Chimimba, 2005), but also worms, termites and larvae (Kingdon, 1974b). The food of the Damara mole rat (Cryptomys damarensis), as well as of the Cap dune mole rat (Bathyergus suillus), does not differ considerably from the composition presented for C. hottentotus (Skinner and Chimimba, 2005). On the other hand, the Cape mole rat (Georychus capensis), does not only ingest plant underground storage organs, but also about 6% above-ground plant material (Skinner and Chimimba, 2005; Bennett et al., 2006). It can be assumed that this material supplies more fibrous constituents than the underground storage organs. This seems also to be the case in the naked mole rat (Heterocephalus glaber), which eats roots of trees and tubers, bulbs, but also above-ground vines (Kingdon, 1974b, 1997). According to Jarvis and Sherman (2002), Heterocephalus glaber eat low-quality, high-fibre diets. It is interesting to note that neither the type of food, nor the presence or absence of caecal taeniae seems to be related with the practise of coprophagy. This has been documented in Cryptomys hottentotus by Bennett and Jarvis (2004), in Georychus capensis by Bennett et al. (2006), as well as in the naked mole rat (Heterocephalus glaber) by Hill et al. (1957), Kingdon (1974b, 1997) and Jarvis and Sherman (2002). In the Southern African mole rat, Cryptomys hottentotus, Bennett and Jarvis (2004) mention that the caecum and colon of that species contain large numbers of cellulosedigesting endosymbionts, making reingestion of faeces (coprophagy) a functionally useful process. Young pups of Heterocephalus glaber obviously depend on the establishment of a microbial population. They first beg for caecotrophes from adults and “nibble on plant materials when they are ca. 2 weeks old, first practise autocoprophagy when ca. 4–5 weeks old” (Jarvis and Sherman, 2002, page 3). The illustration “extracted” from Kotzé et al. (2010) (Fig. 4.146) shows that all bathyergid caeca – with the exception of Heterocephalus glaber – are more or less intensely coiled, though with variable width in relation to caecal length. Additionally, the same authors state that H.  glaber does not have caecal taeniae. However, this species has a tendency towards ingestion of fibrous above-ground plant material, as does Georychus capensis, which tends to eat a similar food, but has a caecum which is similar to those species that live mainly on subterranean storage organs of their plant food. In their study, Kotzé et al. (2010) determined the internal surface area of gut sections according to the following procedure: “The relative macroscopic surface area of the various intestinal parts was estimated by calculating the mean of three different circumference measurements, taken at corresponding positions in all species, multiplied by the length of each part and expressed as a percentage of the total gut surface area” (page 51). From these data a triangular

Fig. 4.146: Outlines of the caeca in eight species of the Bathyergidae. Scale-bars represent 10 cm. Adapted from Kotzé et al. (2010).

(ternary) diagram that refers to small intestine, caecum and colon was drawn (Fig. 4.147). It shows that Heterocephalus glaber has a caecum with relative internal surface of about 40% of the total gut surface (small int. + caecum + colon = 100). On the other hand, Georychus capensis, which also eats some above-ground (= fibrous?) food, has the relatively smallest internal surface of the caecum. A clear relationship between the type of food of a bathyergid species and its caecal size cannot be drawn. 19.5.2 The caecum of Hystricidae and Erethizontidae The Old World porcupines (Hystricidae) and the New World porcupines (Erethizontidae) are predominantly vegetarian, eating bulbs, tubers, roots and fallen fruits (Hystrix africaeaustralis, Skinner and Chimimba, 2005) and can even be strictly folivorous and highly selective in food choice (Chaetomys subspinosus, thin-spined porcupine, Fernandez-Giné et al., 2010). This species is possibly the most folivorous among Erethizontidae eating about 75% leaves, 10% flowers and very little fruit (de Souto Lima et al. (2010). The North American porcupine, Erethizon dorsatum, eats a wide range of plant material and is especially fond of the cambium layer of conifers (Kays and Wilson, 2002). Banfield (1981) supplies more differentiated information: In summer, this species eats green

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19.5.3 The caecum of Thryonomyidae

Fig. 4.147: Relative internal surface areas of three regions of the gastrointestinal tract in six species of the Bathyergidae, including three subspecies of Cryptomys hottentotus. Raw data are from Kotzé et al. (2010).

leaves of forbs, shrubs and trees, but also field crops like clover, alfalfa and young corn. In winter, they feed on the cambium layer and inner bark of trees, especially conifers, as well as new twigs and buds. In the chapter on the colon, illustrations on the caecum were presented for the Hystricidae (Fig. 4.121, based on a drawing by Tullberg, 1899) and the Erethizontidae (Fig. 4.122, Bonfert, 1928). In the publications of van Jaarsveld (1983) and van Jaarsveld and Knight-Eloff (1984), semi-schematic sketches of the Cape porcupine’s gastrointestinal tract can be found, showing lateral taeniae, which run along the intensively haustrated caecum. Van Jaarsveld (1983) writes that the caecum in Hystrix africaeaustralis is relatively small; it comprises only 2.7% of the body mass. It can be assumed that an extensive fermentation chamber is not necessary to digest the food consisting of bulbs, tubers, roots and fallen fruits. According to Van Jaarsveld (1983), fibre is probably only included in the diet at times of food shortage and small quantities of this fibre are digested through colon fermentation. The information on the food of Erethizon dorsatum, the North American porcupine, indicates that the type of food eaten by this species is of lower quality that that of the Cape porcupine. According to Johnson and McBee (1967), about 88% of the total volatile fatty acids produced during alloenzymatic digestion are absorbed in the caecum and only 12% in the colon. These acids contribute considerably to the metabolic needs of the animal; 16% of the required maintenance energy are supplied by volatile or short-chain fatty acids.

This family is represented in the literature by one species, the greater cane rat, Thryonomys swinderianus. According to Skinner and Chimimba (2005), greater cane rats are vegetarians; grasses are their principal food, but roots, shoots and stems of reeds are also eaten, as well as agricultural crops: maize, millet, sorgum, wheat and sugar cane. van Zyl et al. (2005) published an illustration of the digestive tract. In this species, the caecum represents 29% of all regions of the alimentary tract. The caecum consists of three distinct regions, the apex, corpus and ampulla ceci, into which the ileum opens. The caecum displays a series of approximately eight irregularly spaced sacculations and constrictions along its length; taeniae are not mentioned by van Zyl et al. (2005). The transition from the ampulla ceci to the proximal colon is not well defined, although the proximal colon has a smaller diameter than the caecum. The lumen of the ampulla ceci narrows gradually as it approaches the proximal colon. Goblet cells secrete mucus into the lumen of the caecum, which might trap bacteria. Long villi lined with dense and prominent microvilli create a micro-environment where small particles can be separated from the large particles of digesta. “Higher fibre levels in the diet reduced the digestibility of dry matter, protein and fat, while animals digested fibre components (neutral-detergent fibre, acid detergent fibre, hemicellulose and cellulose) with a comparable efficiency to those maintained on a low fibre diet” (van Zyl et al., 1999, page 129). These authors also mention that the greater cane rat practises coprophagy to make use of the products of fermentation in the caecum. According to van Zyl and Delport (2010), small digesta particles in Thryonomys swinderianus are probably retained by the “mucus trap” in the furrow of the proximal colon and moved back to the caecum by antiperistaltic movements (van Zyl et al., 2005).

19.5.4 The caecum of Chinchillidae Food of the long-tailed chinchilla, Chinchilla lanigera, was characterised from faecal remains by Cortés et al. (2002). It varied markedly between seasons and consisted of shrubs, herbs, succulents and of other, very often unrecognised, material. Between 60 and 80% of the food were represented by fibres. These fibrous items may correspond to highly lignified plant parts such as bark or woody stems of shrubs and of succulents. The seed component in the chinchilla diet is almost absent from the diet during a wet season. In Chile, chinchillas live in thickets of the succulent bromeliad Puya bertoroniana, which does not only provide shelter, cover and protection, but also food Deane (pers. comm.,

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July, 1, 2011). Cortés et al. (2002) call the long-tailed chinchilla a generalist and opportunist herbivorous rodent, which incorporates herbaceous plants into its food when they are available. Stems, leaves, roots and fruits can be found in the food of C. lanigera (Deane, pers. comm.). Valuable information on the caecum of different chinchillid species has been supplied by Gorgas (1967), but some of the drawings of the caecum in Fig. 4.125 of Chinchilla lanigera are from Tullberg (1899) and Hebel (1969a). According to Gorgas (1967), the position of the caecum, which has two lateral taeniae, in the abdominal cavity is variable and the caecal length in that species amounts from 74 to 87 mm, Hebel (1969a) measured a caecal length of up to 120 mm. This author writes that the caecum of the long-tailed chinchilla lies in the left part of the abdominal cavity, of which it occupies a large section. The caecum extends from the caudal pole of the left kidney cranio-ventrally and reaches the gastric wall with its apex. Hebel (1969a) mentions a taenia under the line of fixation of the mesentery and a second one on the antimesenterial side of the caecum, i.e. two taeniae are differentiated in the chinchilla. The taeniae end 15 mm before the apex of the caecum. Mucosal villi cannot be found. Hirakawa (2001) describes the digestive process in Chinchilla lanigera, a species which practises coprophagy. In contrast to the chinchilla, the Argentine plains viscacha (Lagostomus maximus) is a strict grazer according to Redford and Eisenberg (1992). Its caecum can be found on the right abdominal wall. It also has two lateral taeniae and its shape is bag-like (Fig. 4.125), its length 138 to 160 mm. Arterial supply via A. colica dextra from A. mesenterica cranialis (superior) (Gorgas, 1967). According to this author, the caecum of Lagidium peruanum (northern mountain viscacha) is not as wide as that of Lagostomus maximus. The caecal apex is bent to the mesenterial side and the length of the organ of the adult lies between 110 and 137 mm.

19.5.5 The caecum of Caviidae The hystricomorph family that was most intensively studied are the Caviidae. They are clearly herbivorous mammals and relatively large rodents. The capybara (Hydrochoerus hydrocaeris) has a body mass between 30 and 43 kg (Silva and Downing, 1995), but according to Mones and Ojasti (1986), this species has an average body mass of about 49 kg in the Venezuelan llanos and a female from Uruguay weighed as much as 91 kg! Dolichotis patagonum, the mara, is the second largest rodent after the capybara (Sombra and Mangione, 2005); its body mass lies in the range between 8 and 16 kg (Silva and Downing, 1995);

Campos et al. (2001a) refer to a mean weight for eight males captured in southern Argentina of 7.73 kg and for 15 females of 8.33 kg. When capybaras in captivity were fed low-protein diets, they practise coprophagy (Herrera, 1985, Hirakawa, 2002). This behaviour was not observed in animals fed nitrogen-rich diets. This facultative behaviour may be a strategy through which capybaras meet their protein requirements. “Energy content seemed to be the only variable on which capybaras based food selection” (Corriale et al., 2011, page 261). Generally, the genus Cavia consists of terrestrial species, which are herbivorous and live on temperate grasslands (O’Connell, 1982). Cavia aperea is a grazer which will also eat the grass inflorescences (Eisenberg and Redford, 1999). This type of food affords alloenzymatic digestion with the help of microbes. The caecum is an important site to house a large volume of digesta, as well as a dense microbial population. The outlines of caeca of the Caviidae are depicted in Fig. 4.126, Fig. 4.127 (Cavia sp.) and Fig. 4.128 (Microcavia, Dolichotis, Kerodon). In addition to data on mammals of different sizes, Snipes (1997) determined the caecal volume in relation to colonic volume (Fig. 4.148). In the domestic guinea pig, the caecal volume (135.2 mL) is 4.6 times the volume of the colon. It represents as much as 62.5% of the total gut (small intestine + caecum + colon) volume (not depicted). An excellent and detailed description of the guinea pig caecum has been published by the same author (Snipes, 1982a), from which the present author will quote, especially from his pages 98 to 100. The caecum lies in the left lateral side of the abdominal cavity. Upon laparotomy only the middle portion of the corpus ceci is visible, the other regions of the caecum being obscured by loops of the small intestines. The caecocolical junction lies cranial. The proximal colon runs parallel to the corpus caeci, being connected to it by a mesenterial ligament. The middle portion of the corpus caeci runs under the proximal colon, crossing the body midline, and curves cranially, dorsal to the loops of the small intestine. The apex caeci bends to the left side of the body approaching the caecocolical region. Also according to Snipes (1982a), the ileocaecal junction lies at the approximate border between the ampulla caeci and the corpus caeci. At the end of the ampulla, the caecocolical junction is found. On the corpus and the apex, the caecum has two prominent, laterally situated taeniae, as well as a third one on the concave side, which is hidden by the attachment of the mesocaecum and which is covered by large blood vessels (Gabella, 1981a). A very detailed study of the wall of the caecum of the guinea pig can be found in the publication of that author. The taeniae in the caecum run along the full length of the organ from

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Fig. 4.148: Volume of the caecum as compared with that of the colon in different mammalian species. Raw data are from Snipes (1997).

its broad base, near the opening of the ileum and colon, to the tip, where they merge with each other. Two of the taeniae, the taenia libera and the taenia mesocolica, are directly visible at the outer surface of the caecum. They follow the broad curvature of the organ along its convex side and they continue into the longitudinal muscle of the colon. Gabella (1981a) erroneously calls a taenia on the wall of the caecum a “taenia coli” (his Fig. 8A, page 145). This terminological mistake can also be found in publications by Bennett and Rogers (1967) (page 574) and Lowy and Mulvany (1973) (page 124). This mistake by these authors is surprising because the term “taeniae caeci” is available in the literature, for example, for the caecum of the horse (Schaller, 1992, page 164/5). Details on the histology of a taenia caeci have been reported by Gabella (1976b). Between the taenia and the circular muscle, there is a space of 30–60 µm occupied by connective tissue and by a tightly meshed myenteric plexus. Prominent septa of connective tissue, carrying blood vessels and nerves, originate from this space and penetrate into the taenia. Some septa span the full thickness of the taenia, although they become rather attenuated near the serosal surface. Occasionally, a bundle of muscle cells leaves the deep surface of the taenia, changes direction and becomes part of the circular layer. The circular muscle often does not run orthogonal to the taenia, but it deviates by up to about 10° from an orthogonal course (Gabella, 1981b) and is made up of flattened bundles

arranged in a position which is reminiscent of a Venetian blind with one bundle partly covered by one neighbouring “lamella” and partly covering itself the bundle or “lamella” on the other side. However, where the caecal wall is distended and forms transient haustrations, the “lamellae” of the circular muscle are turned in a different way, as in a fully closed Venetian blind with the circular muscle bundles marginally overlapping each other and forming almost a continuous sheet. Schulze-Delrieu et al. (1996) deal with motility and function of taeniae and haustra in the guinea pig caecum. From that paper the present author will cite extensively. Local contractions of the taeniae shorten and deepen haustral pockets and shift luminal contents back and forth between adjacent pockets. Circular muscular contractions accomplish the “caterpillar movements” of the haustra known as haustral rolling. The walls of fully expanded haustral pockets were thin and transparent as they bulged between their proximal and distal septa. On the other hand, the walls of collapsed haustral pockets were level with their septa, fleshy and opaque. By folding their walls, the haustral pockets collapsed. Conversely, when haustral pockets were passively filled, their walls expanded and folds popped out. During this “haustral rolling”, each haustral segment subdivided into many segments. Haustral rolling in the guinea pig caecum is never associated with any luminal pressure waves. The back-and-forth shifting of contents between haustral

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Fig. 4.149: Schematic representation of the arterial supply of caecum and colon in Cavia porcellus. Adapted from Snipes (1982a).

segments, that high-frequency contractions of intrahaustral folds are responsible for colonic absorption of water and solute by separating liquid and solid phases and by thus exposing contents to luminal surfaces and compound faecal material (Schulze-Delrieu et al., 1996). In Cavia porcellus, caecal contractions begin with the shortening of the taeniae and are associated with low-amplitude pressures and expulsion of a 5- to 10-mL volume (Lange et al., 1995), which represents only a small portion of the already mentioned total colonic volume of 135 mL as mentioned by Snipes (1997). Its large capacity and great distensibility make the caecum suitable for reservoir functions. In his detailed paper on the anatomy of the guinea pig caecum, Snipes (1982a) also deals with the arterial supply of the organ in Cavia porcellus. From his illustration and description the schematic presentation Fig. 4.149 has been compiled. Information on another of the Caviidae, the Mara (Dolichotis patagonum) has been given by Weissengruber (2000). The photos in that publication are unclear and insufficient. Despite these deficits it was tried to depict the arterial supply of the mara caecum (Fig. 4.150). In this species, Weissengruber (2000) did not show arterial anastomoses. The present author is not able to give a comment whether the differences between the results of Snipes (1982a) and Weissengruber (2000) really represent interspecific variation. Not all species of the Caviidae are predominantly grazers as the guinea pig. For example, Microcavia australis (southern mountain cavy) is called a facultative specialist on dicots with a broad trophic niche (Sassi et al., 2011). In this species, as in many other herbivores, the caecum is the organ that is most closely related to cellulose fermentation (Sassi et al., 2007). However, the caecum should not be considered in isolation. According to Sakaguchi et al. (1985), the caecum and the proximal colon of Cavia porcellus together formed a common fermentation chamber. Contents of this common compartment were 6.7% of body weight. Most of the short-chain fatty acids produced in

Fig. 4.150: Schematic representation of the branches originating from the Aorta abdominalis in Dolichotis patagonum (mara). Adapted from Weissengruber (2000).

this section of the gut are absorbed, only 15% pass into the lower large intestine. Rechkemmer and Engelhardt (1993) write that 95–99% of short-chain fatty acids produced in the large intestine of Cavia porcellus are absorbed, as well as sodium and chloride, but this absorption is combined with small net potassium secretion. Generally speaking different micro-environments exist in the large intestine, as Takahashi and Sakaguchi (2006) mention for the guinea pig. In the caecum and in the proximal colon, the bacterial activity is higher than in the distal colon and rectum. Accumulation of bacteria within the caecum occurred after the accumulation in the colonic furrow, which was mentioned in the chapter dealing with the colon; the furrow is the main route of retrograde transport of bacteria towards the caecum. As the furrow and the main lumen of the colon are not separated completely,

19 Hystricomorpha 

it is likely that flow can occur in opposite directions simultaneously within the proximal colon during the feeding period (Takahashi and Sakaguchi, 2006). According to Holtenius and Björnhag (1985), the concentration of nitrogen and viable bacteria in the guinea pig were nearly twice as high in the colonic groove compared to the open colonic lumen. Bacteria infused experimentally into the proximal colon of guinea pigs were transported back via the furrow into the caecum. To avoid a radical wash-out of symbiotic and autochthonous flora of the guinea pig caecum, spiral-shaped bacteria are firmly attached to the apical portion of the caecal epithelium of Cavia porcellus (Mora-Galindo, 1978, 1987) and Franz et al. (2010). In guinea pigs, small particles and microbes are “mucous-trapped”. A high digestibility of fibre from the feed in guinea pigs is combined with slow and potentially incomplete removal of bacteria from digesta in the colon (Franz et al., 2010). Plasticity in food assimilation, retention time and coprophagy allow herbivorous cavies (Microcavia australis) to cope with low quality food (Sassi et al., 2010). According to Hörnicke and Björnhag (1980), coprophagy is also practised by the guinea pig.

19.5.6 The caecum of Octodontidae Members of this family are adapted to different types and qualities of food. For example, the red viscacha-rat (Tympanoctomys barrerae) specialises on halophytic vegetation (salt bushes) (Redford and Eisenberg, 1992). Graminae are eaten by this species in lower proportion than is found in the plant cover (Diaz et al., 2000). On the other hand, the diet of Spalacopus cyanus is apparently composed exclusively of underground tubers and roots (Redford and Eisenberg, 1992); it also feeds underground, eats underground storage organs and stalks (Torres-Mura and Contreras, 1998). The degu, Octodon degus, is a diurnal herbivore-folivore; it is the most common mammal of central Chile (Woods and Boraker, 1975). In one study, the diet consisted of 25.6% by volume seeds and 60.0% shrub and herbaceous foliage; in another study, grass composed 41.7%, herbs 15.4%, flowers 8.4%, seeds 9.6%, fruit 7.8%, bush bark and leaves 16%, and adult insects 0.8% (Redford and Eisenberg, 1992). At older age, even meat is eaten according to Woods and Boraker (1975). The caecum of Spalacopus cyanus is depicted in Fig. 4.130, originally published by Tullberg (1899) and Gorgas (1967). It has a length of about 50 mm. Lateral taeniae are differentiated on that organ, which has a corpus, widened like an ampulla, and narrows towards the apex. A valvula ileocaecalis is found (Gorgas, 1967). In Octodon degus, the

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caecal shape is similar to that of S. cyanus; the organ has a length between 85 and 95 mm. A circular fold between the caecum and the colon can be found (Gorgas, 1967). Despite the above-mentioned different type of food that is eaten by the degu (Octodon degus), its caecum is similar to that of the coruro (Spalacopus cyanus). Gonzalez and Feder (1997) discuss the degu caecum. As is characteristic for this organ, it is subdivided into three sections: the capud, corpus and apex caeci. A greater and a lesser curvature are formed, as well as a facies dextra and sinistra. The ileum enters on the side of the lesser curvature (ostium ileale). Taenia caeci dextra and sinistra can be easily recognised, as is also illustrated in a drawing by Gorgas (1967). Opening into the colon ascendens is the ostium caecocolicum. The mesocaecum is fixed on the right side of the caecum. The position of the caecum in the abdomen is very variable (Gonzalez and Feder, 1997): In the majority of investigated cases the caecum could be found to the left of the median plane. The capud caeci can lie either in the left cranial section of the abdominal cavity, in other individuals it lies left and caudally. The corpus caeci could be found left and ventrally and the apex caeci lies in the pelvic entrance. In some cases, the caecum had a transverse position.

19.5.7 The caecum of Echimyidae The digestive tract of this South American family has already been depicted in Fig. 4.124. In this illustration, three species are represented, Makalata didelphoides, the red-nosed armoured tree rat, (Gorgas, 1967), Trinomys setosus (hairy Atlantic spiny rat) (Tullberg, 1899), Kannabateomys amblyonyx (Atlantic bamboo rat) (Gorgas, 1967). Eisenberg and Redford (1999) do not present information on the type of food eaten by Kannabateomys amblyonyx and Trinomys setosus. According to these authors, Makalata didelphoides eats immature seeds. On the other hand, Thrichomys aperoides or common punaré, living in the Campos Cerrados of Brazil, is an insectivorous rodent that also consumes fruits and other plant parts of different proportions in dry and rainy season (Lessa and Costa, 2009).

19.5.8 The caecum of Myocastoridae In the introduction to his chapter on the nutrition in the nutria (Myocasor coypus), Allgöwer (2005c) writes that their large caecum already demonstrates digestion of a food rich in cellulose. According to Lereboullet (1845), the caecum of Myocastor coypus is long and narrow (Fig. 4.151), a fact that is also demonstrated by the

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Fig. 4.152: Large intestine of Myocastor coypus (Hystricomorpha, Myocastoridae). Modified after Lereboullet (1845), Tullberg (1899), Bonfert (1928) and Gorgas (1967).

Fig. 4.151: Two illustrations of the large intestine of the Myocastor coypus (nutria). Adapted from Lereboullet (1845) (A) and from Snipes et al. (1988) (B).

photos published by Warner (1963) and Stahl (1987) and by the semi-schematic illustration (Fig. 4.151 and 4.131, top panel), from the paper by Snipes et al. (1988), as well as in the drawings by Lereboullet (1845), Tullberg (1899), Bonfert (1928) and Gorgas (1967), which are compiled in Fig. 4.152. According to Allgöwer (2005c), nutrias need a daily intake that is equivalent in weight to a quarter of their body weight (between 4 and 8 kg, but sometimes up to 12 kg, Stubbe, 1982; for Switzerland Kohli, 1995, gives 7 to 9 kg. For Denmark Baagøe, 2007, mentions 5 to 10 kg) to supply themselves with sufficient energy. Rhizomes, shoots, leaves and bark characterise the food of Myocastor coypus (Stubbe, 1982). Because of this relatively large quantity of plant material that has to be ingested, Warner (1963) characterised the caecum of the nutria as a large sacculated sac. It extends transversally across the abdominal cavity ventral to the distal portion of the abdominal aorta. The caecum has an average length of approximately 43 cm and is spiralled. Two longitudinal bands of muscles form lateral taeniae. The blind end or apex of the caecum does not form a discrete appendix. As has already been indicated, the function of the nutria caecum can only be understood when the proximal portion of the colon with

its ridge-lined furrow is also considered (Snipes et al., 1988). Retrograde transport of bacteria and small particle transport caecalwards is evidently carried out in the colonic groove or furrow.

20 Lagomorpha Lagomorphs range from small Ochotonidae (