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THE UNIVERSITY OF KANSAS MUSEUM OF NATURAL HISTORY SPECIAL PUBLICATION No. 25 Planetary Biodiversity Inventory /onno nm rA. Vertebrate Bowels of the Earth The University of Kansas Natural History Museum Special Publication No. 25 20 July 2017 Planetary Biodiversity Inventory (2008-2017): Tapeworms from Vertebrate Bowels of the Earth Edited by Janine N. Caira Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut, 06269-3043, USA and Kirsten Jensen Department of Ecology and Evolutionary Biology, Biodiversity Institute, University of Kansas, Lawrence, Kansas, 66045, USA Natural History Museum The University of Kansas Lawrence, Kansas SPECIAL PUBLICATION NATURAL HISTORY MUSEUM, THE UNIVERSITY OF KANSAS Series Editor: Kirsten Jensen Type setting and Layout: Kirsten Jensen Original Cover Art: Kendel Craig Cover Design: Kirsten Jensen & Janine N. Caira Special Publication No. 25 pp. i-ix, 1-463 Published 20 July 2017 ISBN-10: 0-89338-002-4 ISBN-13: 978-0-89338-002-1 ©The University of Kansas, Natural History Museum Chapters in this volume were peer-reviewed. This Special Publication is electroniclly available at http://hdl.handle.net/1808/24421 and http://tapeworms.uconn.edu/finalpub.html Printed by Yurchak Printing, Inc., Landisville, Pennsylvania CONTENTS Acknowledgments.viii 1 An overview of tapeworms from vertebrate bowels of the earth Janine N. Caira, K. Jensen, Boyko B. Georgiev, Roman Kuchta, D. Timothy J. Littlewood, Jean Mariaux, Tomas Scholz, Vasyl V. Tkach, and Andrea Waeschenbach.1 2 Amphilinidea Tomas Scholz and Roman Kuchta.21 3 Bothriocephalidea Roman Kuchta and Tomas Scholz.29 4 Caryophyllidea Tomas Scholz and Mikulas Oros.47 5 Cathetocephalidea Janine N. Caira, Veronica M. Bueno, and Kirsten Jensen.65 6 Cyclophyllidea Jean Mariaux, Vasyl V. Tkach, Gergana P. Vasileva, Andrea Waeschenbach, Ian Beveridge, Yana Dimitrova, Voitto Haukisalmi, Stephen E. Greiman, D. Timothy J. Littlewood, Arseny A. Makarikov, Anna J. Phillips, Tantely Razafiarisolo, Vincent Widmer, and Boyko B. Georgiev.77 7 Diphyllidea Janine N. Caira, Veronica A. Ivanov, Kirsten Jensen, and Fernando P. L. Marques.149 8 Diphyllobothriidea Roman Kuchta and Tomas Scholz.167 9 Gyrocotylidea Roman Kuchta, Tomas Scholz, and Haakon Hansen.191 10 Haplobothriidea Roman Kuchta and Tomas Scholz.201 11 Lecanicephalidea Kirsten Jensen, Joanna J. Cielocha, Kaylee S. Herzog, and Janine N. Caira.207 12 Litobothriidea Janine N. Caira, Kaitlin Gallagher, and Kirsten Jensen.231 13 Nippotaeniidea Tomas Scholz, Jan Brabec, and Roman Kuchta.243 14 Onchoproteocephalidea I Alain de Chambrier, Tomas Scholz, Jean Mariaux, and Roman Kuchta.251 15 Onchoproteocephalidea II Janine N. Caira, Kirsten Jensen, and Veronica A. Ivanov.279 16 Phyllobothriidea Timothy R. Ruhnke, Janine N. Caira, and Maria Pickering.305 17 Rhinebothriidea Timothy R. Ruhnke, Florian B. Reyda, and Fernando P. L. Marques.327 18 Spathebothriidea Roman Kuchta and Tomas Scholz. ....349 19 Tetrabothriidea Jean Mariaux, Roman Kuchta, and Eric P. Hoberg. ....357 20 "TETRAPHYLLIDEa" VAN BENEDEN, 1850 RELICS Janine N. Caira, Kirsten Jensen, and Timothy R. Ruhnke. ....371 21 Trypanorhyncha Ian Beveridge; Mohammed Haseli, Veronica Ivanov, Adriana Menoret, and Bjoern C. Schaeffner. ....401 22 A MOLECULAR FRAMEWORK FOR THE CESTODA Andrea Waeschenbach and D. Timothy J. Littlewood. ....431 Appendix. Publications citing the National Science Foundation Planetary Biodiversity Inventory program grants DEB 0818696 and 0818823. ....453 IV CONTRIBUTORS Beveridge, Ian Department of Veterinary Science, University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia. E-mail: [email protected] Brabec, Jan Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic. E-mail: [email protected] Bueno, Veronica M. Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd., Storrs, CT 06269-3043, USA. E-mail: [email protected] Caira, Janine N. Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd., Storrs, CT 06269-3043, USA. E-mail: [email protected] de Chambrier, Alain Museum d'Histoire Naturelle de Geneve, PO. Box 6434, CH-1211 Geneva 6, Switzerland. E-mail: [email protected] Cielocha, Joanna J. Biology Department, Science Center 220J, Rockhurst University, 1100 Rockhurst Road, Kansas City, MO 64110, USA. E-mail: [email protected] Dimitrova, Yana D. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria. E-mail: [email protected] Gallagher, Kahlin Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd., Storrs, CT 06269-3043, USA. E-mail: [email protected] Georgiev, Boyko B. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria. E-mail: [email protected] Greiman, Stephen E. Department of Biology, Georgia Southern University, PO. Box 8042-1, Statesboro, GA 30460, USA. E-mail: [email protected] Hansen, Haakon Norwegian Veterinary Institute, Section for Parasitology, Ullevalsveien 68, 0454 Oslo, Norway. E-mail: [email protected] Haseli, Mohammad Department of Biology, Faculty of Sciences, University of Guilan, Rasht, Iran. E-mail: [email protected] Haukisalmi, Voitto Piettasenkatu 38 A 23, 33580 Tampere, Finland. E-mail: [email protected] Herzog, Kaylee S. Department of Ecology and Evolutionary Biology and the Biodiversity Institute, University of Kansas, 1200 Sunnyside Ave., Lawrence, KS 66045, USA. E-mail: [email protected] v Hoberg, Eric P. Animal Parasitic Diseases Laboratory, Agricultural Research Service, US Department of Agriculture, Beltsville, MD, 20705-2350, USA and Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., 20560-0163, USA. E-mail: [email protected] Ivanov, Veronica A. Instituto de Biodiversidad y Biologfa Experimental y Aplicada - IBBEA (CONICET-UBA), and Departamento de Biodiversidad y Biologfa Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellon II, piso 4, Lab. 52, C1428EHA, Buenos Aires, Argentina. E-mail: [email protected] Jensen, Kirsten Department of Ecology and Evolutionary Biology and the Biodiversity Institute, University of Kansas, 1200 Sunnyside Ave., Lawrence, KS 66045, USA. E-mail: [email protected] Kuchta, Roman Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic. E-mail: [email protected] Littlewood, D. Timothy J. Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK. E-mail: [email protected] Makarikov, Arseny A. Institute of Systematics and Ecology of Animals, Siberian Branch of Russian Academy of Sciences, 11 Frunze Str., 630091, Novosibirsk, Russia. E-mail: [email protected] Mariaux, Jean Museum d'Histoire Naturelle de Geneve, P.O. Box 6434, CH-1211 Geneva 6, Switzerland and Department of Genetics and Evolution, University of Geneva, CH-1205 Geneva, Switzerland. E-mail: [email protected] Marques, Fernando P. L. Departamento de Zoologia, Instituto de Biociencias, Universidade de Sao Paulo, Rua do Matao, tv. 14, no. 101, 05508-090 Cidade Universitaria, Sao Paulo, Brasil. E-mail: [email protected] Menoret, Adriana Instituto de Biodiversidad y Biologfa Experimental y Aplicada - IBBEA (CONICET-UBA), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellon II, piso 4, Lab. 52, C1428EHA, Buenos Aires, Argentina. E-mail: [email protected] Oros, MtkulaS Institute of Parasitology of the Slovak Academy of Sciences, Hlinkova 3, 040 01 Kosice, Slovakia. E-mail: [email protected] Phillips, Anna J. Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., 20560-0163, USA. E-mail: [email protected] Pickering, Maria Department of Biological Sciences, Meredith College, 3800 Hillsborough Street, Raleigh, NC 27607-5298, USA. E-mail: [email protected] vi Razafiarisolo, Tantely Departement de Biologie Animale, Universite d'Antananarivo, B.R 906 - 101 Antananarivo, Madagascar. E-mail: [email protected] Reyda, Florian B. Biology Department, State University of New York, College at Oneonta, 120 Science I, Oneonta, NY 13820-4015, USA. E-mail: [email protected] Ruhnke, Timothy R. Department of Biology, West Virginia State University, H101, Institute, WV 25112-1000, USA. E-mail: [email protected] SCHOLZ, TomA§ Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branisovska 31, 370 05 Geske Budejovice, Czech Republic. E-mail: [email protected] SCHAEFFNER, BjOERN C. Helmintologia Departamento de Zoologia, Instituto de Biociencias, Universidade de Sao Paulo, Rua do Matao, tv. 14, no. 101, 05508-090 Cidade Universitaria, Sao Paulo, Brasil. E-mail: [email protected] Tkach, Vasyl V. Department of Biology, University of North Dakota, 10 Cornell Street Stop 9019, Grand Forks, ND 58202-9019, USA. E-mail: [email protected] Vasileva, Gergana P. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria. E-mail: [email protected] Waeschenbach, Andrea Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK. E-mail: [email protected] Widmer, Vincent Museum d'Histoire Naturelle de Geneve, PO. Box 6434, CH-1211 Geneva 6, Switzerland. E-mail: [email protected] vii ACKNOWLEDGMENTS We thank the Biodiversity Institute at the University of Kansas for providing funds for printing this document. We are especially grateful to Kathleen R. Smith for her copy editing skills; this document was much improved by her expertise and careful attention to detail. Elizabeth Barbeau and Kendra R. Mojica assisted with the generation of taxon lists that helped inform multiple chapters in the early stages of production. This endeavor was made possible with funding from the National Science Foundation's (NSF) Planetary Biodiversity Inventory program (Nos. DEB 0818696 and 0818823). One of the motivations for this document was to provide the public with an insight into the sizeable return on the investment made in this project by NSF. The title was specifically crafted to help make the research more accessible to the non-scientific community, alluding to the site of infection of the parasites under study and recognizing the global effort undertaken. This funding made a worldwide survey of tapeworms that live in the intestines of birds, mammals, bony fishes, snakes, frogs, sharks, and stingrays possible. It facilitated over 250 scientists from around the world to work together to discover hundreds of new species and tens of new genera, as well as to establish numerous new country and host records for tapeworms. As a consequence, the classification of tapeworms was largely revised to reflect our understanding of the evolutionary relationships of what are now 19 major tapeworm groups. More than 220 publications resulted directly from the investment and others are in various stages of completion. Beyond the details of the science, this funding also supported generation of the children's book. Meet the Suckers, which was designed to introduce younger readers to the fascinating world of the tapeworms that live, hidden from view, inside the animals of a typical Aquarium. It also supported establishment of the project website (www.tapeworms.uconn. edu), which, beyond serving as a public portal to the science, provides resources such as an Illustrated Glossary for teaching about tapeworms. A number of US states received direct, long-term benefits from this project because most of our now highly trained postdoctoral fellows, and graduate and undergraduate students currently hold positions as high school teachers, university professors, museum curators, lawyers, physicians, and veterinarians in Connecticut, Georgia, Kansas, Massachusetts, New York, North Carolina, North Dakota, Washington DC, and West Virginia. The solid foundation we have built will expedite future advances in this field. Although only a relatively small proportion of the more than 4,800 species of tapeworms now recognized globally are of medical or veterinary importance, insights gained from this project helped inform our understanding of their origins, evolution, and intimate association with their hosts and environment. Above all else, we have learned that tapeworms are essentially everywhere and there is much more to learn. But from what we have learned, we can affirm that knowledge is power! viii PREFACE This document is organized into 22 peer-reviewed chapters. Each of the chapters focuses on an individual cestode group, begins with the status of knowledge of the group prior to the inception of the PBI project, and ends with an assessment of the current understanding of the group. In each case, diversity, classification, morphology, phylogenetic relationships, host associations, and geographic distribution are addressed. In all but one case, each chapter includes a list of valid taxa. Synonyms have not generally been listed; this was determined to be beyond the scope of the project given the immensity of such lists for some groups. With over 3,000 valid species, the generation of a list of species for the Cyclophyllidea was also determined to be beyond the scope of this project. However, a list of valid higher taxa is provided. Each of the 19 cestode orders is addressed alphabetically in separate chapters with two exceptions. The Mesocestoididae are treated as a family in the Cyclophyllidea. Although evidence supporting recognition of the former as an independent order is mounting, the case remains to be formally made based on more detailed investigations of this enigmatic group of mammal parasites. The Onchoproteocephalidea are the second exception. So as to emphasize the dual nature of the host associations and scolex morphology of its members, the freshwater fish-parasitizing taxa (formerly assigned to the order Proteocephalidea) are treated in a chapter as the Onchoproteocephalidea I separately from the taxa that parasitize elasmobranchs, which are treated as the Onchoproteocephalidea II. Use of quotation marks around taxon names (e.g., the order "Tetraphyllidea") is to remind readers of the definitively non-monophyletic nature of these groups. The first and last chapters are more synthetic in nature. The first chapter provides an overview of the results of the project both in terms of its Intellectual Merit and Broader Impact elements (to use NSF terminology). The final chapter provides a molecular framework for the phylogenetic relationships among the cestodes as they are understood at the end of the PBI project. The final chapter also describes the molecular methods and taxon sampling employed to achieve that framework. This Special Issue concludes with an Appendix listing the more than 220 publications directly resulting from project efforts, all of which cite the PBI award (NSF DEB Nos. 0818696 and 0818823). IX