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Dutton Thesis -Compressed.Pdf Biodiversity and Phylogenetics of Metazoan Parasites Infecting Freshwater Turtles by Haley Rebecca Dutton A thesis submitted to the Graduate Faculty of Auburn University in partial fulfillment of the requirements for the Degree of Master of Science Auburn, Alabama May 02, 2020 Keywords: Pitiutrema, Taxonomy, Systematics, Phylogeny, Marine Derived Lineage Copyright 2020 by Haley Rebecca Dutton Approved by Stephen Ashton Bullard, PhD, Chair, Professor of Fisheries, Aquaculture, and Aquatic Sciences Paul D. Johnson, PhD, Alabama Department of Conservation and Natural Resources, Alabama Aquatic Biodiversity Center Nathan V. Whelan, PhD, Director, United States Fish and Wildlife Service Southeast Conservation Genetics Lab ABSTRACT There are 356 extant turtle species (Testudines), including 60 polytypic taxa that add 122 subspecies. Among the more diverse groups of metazoan parasites that infect turtles are the turtle blood flukes (TBFs) (Digenea: Schistosomatoidea; 106 species; 24 genera). Polystomes (Monogenoidea: Polystomatidae; 61 species; 5 genera) are another underexplored group of parasites infecting turtles. They belong to a much larger group of flatworms that are, nearly without exception, fish ectoparasites and are further intriguing by infecting unusual sites (conjunctival sac, buccal cavity, urinary bladder) of turtles and frogs. Both of these taxonomic groups are understudied in North America. TBFs, especially of freshwater turtles, are largely ignored outside of North America. TBFs and polystomes infect members of both major turtle lineages, sub-order Pleurodira Cope, 1864 (side-necked turtles, withdraw neck by bending in horizontal plane; 93 species) and sub-order Cryptodira Cope, 1868 (hidden-necked turtles, withdraw head by bending neck in vertical plane; 263 species). Extant cryptodires range in the northern and southern hemispheres, whereas extant pleurodires range in southern hemisphere freshwater habitats only. Herein, I necropsied 86 turtles of 24 species (14 genera: 7 families; including cryptodires and pleurodires) from 3 continents (North America, Africa, Asia). In addition, I published a taxonomic description from TBFs collected previously by the Bullard Lab in South America (Peru). I used alpha taxonomy, light microscopy, nucleotide sequencing techniques (PCR; large subunit ribosomal DNA [28S], small subunit ribosomal DNA [18S], and Cytochrome c oxidase subunit I [CO1]), and molecular phylogenetic analyses (Baysian inferences) to (i) redescribe a species long-regarded as a species complex, (ii) emend a genus that lacked extant type material and described a new species of the genus, (iii) proposed two new genera and described two new species, and (iv) shed light on a particular taxonomically- troubling polystome; including the first record of this lineage of parasite in the alligator snapping turtle or from Mississippi. The turtle blood fluke work is published in The Journal of Parasitology, Folia Parasitologica, and Systematic Parasitology. The final chapter detailing the polystome was in review at the time of the defense of this thesis. ii ACKNOWLEDGMENTS I thank my advisor, mentor, and friend Stephen Ash Bullard (Aquatic Parasitology Laboratory, School of Fisheries, Aquaculture, and Aquatic Sciences [SFAAS], College of Agriculture [COA], Auburn University [AU], Auburn, AL) for sharing his expertise and experiences with me. I thank Ash for his patience and understanding, along with his ability to see my strengths and capabilities even when I unable to see them myself. I thank Ash for his guidance and most of all his unwavering curiosity and constant encouragement to better myself. I am thankful to my committee members Paul Johnson (Aquatic Biodiversity Center) and Nathan Whelan (United States Fish and Wildlife, SFAAS, COA, AU, Auburn, AL) for providing comments on this thesis. I thank Jackson Roberts for sharing his collection with me. I thank Tom Platt and Louis Du Preez for their knowledgeable insight on these groups and support. I thank my laboratory mates Micah “Brett” Warren and Steven “Steve-o” Kspeka for their friendship, insights, and assistance in the laboratory and field; Edna Fernandez-Figueroa, for her encouragement and friendship; James “Jim” C. Godwin (Alabama Natural Heritage Program) for sharing his knowledge about and assistance with locating turtles in Alabama. I thank Anna Phillips, William Moser, Katie Ahlfield, and Karen Reed (Smithsonian National Museum of Natural History: Department of Invertebrate Zoology, Washington D.C.) for accepting our type materials and vouchers as well as for loaning us critical type specimens. I thank my parents Tracy and Kevin Haake and Ross Dutton for talking me through the lows and celebrating with me during the highs and for their unwavering love and support. I am inspired by my Mimi (Martha Drake) for always being optimistic and joyful. Thank you to my sisters, cousins, niece, nephews, and friends for all of their kindness and support. iii TABLE OF CONTENTS Abstract ......................................................................................................................................... ii Acknowledgments ........................................................................................................................ iii List of Tables ................................................................................................................................ v List of Figures .............................................................................................................................. vi Chapter 1: New genus and species of turtle blood fluke (Platyhelminthes: Digenea: Schistosomatoidea) infecting six-tubercled Amazon River turtles, Podocnemis sextuberculata (Pleurodira: Podocnemididae) from the Amazon River Basin (Peru) ........................................ 1 Introduction ..................................................................................................................... 2 Materials and methods .................................................................................................... 3 Description ...................................................................................................................... 5 Pitiutrema Dutton and Bullard n. gen. ............................................................................ 7 Differential diagnosis .............................................................................................. 7 Taxonomic summary ............................................................................................... 7 Pitiutrema revelae Dutton and Bullard n. sp. ................................................................ 7 Description of adult ................................................................................................. 7 Taxonomic summary ............................................................................................. 11 Molecular results .......................................................................................................... 12 Remarks ........................................................................................................................ 13 Discussion ..................................................................................................................... 14 Literature cited .............................................................................................................. 23 Chapter 2: Ruavermis mikebargeri gen. et sp. nov. (Digenea: Schistosomatoidea) infecting the yellow-headed temple turtle, Heosemys annandalii (Cryptodira: Geoemydidae) in Vietnam, including an updated phylogeny for the turtle blood flukes. ...................................................... 39 Introduction ................................................................................................................... 40 iv Materials and methods .................................................................................................. 41 Results ........................................................................................................................... 43 Ruavermis Dutton and Bullard n. gen. .......................................................................... 43 Differential diagnosis ............................................................................................ 45 Taxonomic summary ............................................................................................. 45 Ruavermis mikebargeri Dutton and Bullard n. sp. ...................................................... 46 Description of adult ............................................................................................... 46 Taxonomic summary ............................................................................................. 49 Phylogenetic results ...................................................................................................... 50 Discussion ..................................................................................................................... 50 References ..................................................................................................................... 54 Chapter 3: A new species and emendation of the seldom reported Enterohaematotrema Mehra, 1940 (Digenea: Schistosomatoidea), including a revised phylogenetic hypothesis for turtle blood flukes) ......................................................................................................................................
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