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A Checklist of Host-Parasite Interactions of the Order Crocodylia

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A Checklist of Host-Parasite Interactions of the Order Crocodylia UC Office of the President UC Publications in Zoology Title Checklist of Host-Parasite Interactions of the Order Crocodylia Permalink https://escholarship.org/uc/item/3tr1g60k ISBN 9780520957367 Author Tellez, Marisa Publication Date 2013-09-01 Peer reviewed eScholarship.org Powered by the California Digital Library University of California A CHECKLIST OF HOST-PARASITE INTERACTIONS OF THE ORDER CROCODYLIA An American Crocodile, Crocodylus acutus. Photograph taken by Marisa Tellez on July 14, 2010 at WASA Lagoon, San Pedro, Ambergris Caye, Belize. A CHECKLIST OF HOST-PARASITE INTERACTION OF THE ORDER CROCODYLIA Marisa Tellez Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095-1606, U.S.A. UNIVERSITY OF CALIFORNIA PRESS BERKELEY LOS ANGELES LONDON ,'4#01'27-$*'$-0,'0#11Q-,#-$2&#+-12"'12',%3'1&#"3,'4#01'27.0#11#1',2&#,'2#"22#1Q#,0'!&#1*'4#10-3,"2&# 5-0*" 7"4,!',%1!&-*01&'.',2&#&3+,'2'#1Q1-!'*1!'#,!#1Q,",230*1!'#,!#1T21!2'4'2'#10#13..-02#" 72&# 0#11-3,"2'-,,".&'*,2&0-.'!!-,20' 32'-,1$0-+',"'4'"3*1,"',12'232'-,1T -0+-0#',$-0+2'-,Q4'1'2555T3!.0#11T#"3 !"#$%&'(&# ')('$& *&&(&+%Q!-*3+#SUX ""'2-0'*)-0"S04'"T1--"03$$""'2-0V',V&'#$Q0*'!#0-Q0-3%*1'T5#*2Q"'*##,'T(!#7Q#2#0)T6-7*#Q,"0-,*" T-221 ,'4#01'27-$*'$-0,'0#11 )#0)#*#7,"(-1',%#*#1Q*'$-0,' ,'4#01'27-$*'$-0,'0#11Q(2"T (-,"-,Q",%*," TRSU 7$&###%#,21-$2&#,'4#01'27-$*'$-0,' (' 007-$-,%0#11-,20-* 3+ #0STRSU[UV[UX ) [YZVRVWTRVR[ZZ[VU. )TS*)T..#0 6,3$!230#"',2&#,'2#"22#1-$'+#0'! SR[ZYXWVUTS $&#..#031#"',2&'1.3 *'!2'-,+##212&#+','+3+0#/3'0#+#,21-$ ' &*U[TVZVS[[T#S[[YPermanenceofPaperT To the Garcia and Tellez Family 4 This page intentionally left blank CONTENTS Acknowledgments, ix Abstract, x INTRODUCTION 1 MATERIAL AND METHODS 3 Background Information, 3 Sources of Documentation, 4 Taxonomic Clarification of Hosts and Parasites, 6 Use of the Database, 6 Interpreting Crocodilian-Parasite Database, 6 CROCODILIAN-PARASITE DATABASE 8 Family Alligatoridae, 8 Alligator mississippiensis, 8 Alligator sinensis, 25 Caiman crocodilus apaporiensis, 26 Caiman crocodilus chiapsius, 27 Caiman crocodilus crocodilus, 28 Caiman crocodilus fuscus, 46 Caiman latirostris, 50 Caiman yacare, 54 Melanosuchus niger, 64 Paleosuchus palpebrosus, 71 Paleosuchus trigonatus, 74 Family Crocodylidae, 77 Crocodylus acutus, 77 Crocodylus intermedius, 85 Crocodylus johnstoni, 87 Crocodylus mindorensis, 93 Crocodylus moreletii, 94 Crocodylus niloticus, 99 Crocodylus novaeguineae, 114 Crocodylus palustris, 119 Crocodylus porosus, 123 Crocodylus rhombifer, 136 Crocodylus siamensis, 139 Mecistops cataphractus, 142 4'' Contents 4''' Osteolaemus tetraspis, 148 Osteolaemus tetraspis osborni, 153 Osteolaemus tetraspis tetraspis, 155 Tomistoma schlegelii, 156 Family Gavialidae, 157 Gavialis gangeticus, 157 Unknown Crocodilian Species, 164 PARASITE-CROCODILIAN DATABASE 180 Proteobacteria, 180 Sacromastigophora, 181 Heterokontophyta, 184 Apicomplexa, 185 Myxozoa, 193 Platyhelminthes, 194 Rotifera, 241 Acanthocephala, 242 Annelida, 244 Nematoda, 247 Arthropoda, 283 HOST SPECIFICITY 305 CONCLUSION 308 Literature Cited, 309 Appendix, 353 Addendum, 375 ACKNOWLEDGMENTS This compilation was accompanied with a network of support from advisors and colleagues. First, I would like to express the deepest gratitude to my doctoral advisor, Dr. Donald G. Buth for his guidance, patience, and insightful criticisms on this crocodilian-parasite database. His encouragement in starting this project has greatly benefited my future prospects in parasitology and crocodilian research. I am also grateful for Dr. Malcolm Gordon and Dr. Michael Alfaro for their guidance assisting me to establish a strong scientific research background that is intellectually worthy. I would also like to acknowledge Dr. Armand Kuris’ continuous encouragement, enthusiasm, and mentorship throughout my academic career, and for introducing me to the wonderful world of parasites! Finally, I would like to extend my appreciation to Dr. Ruth Elsey and the Steering Committee of the Crocodile Specialist Group for help in obtaining information and their continual support and enthusiasm for crocodile-parasite endeavors. This crocodilian-parasite checklist and synthesis is dedicated to my Tio Fernie and Tia Rosie whose support, inspiration and love throughout their years on earth gave me the motivation to accomplish this project. The inner strength and faith they instilled in me will continue to assist me in overcoming any hurdle or challenge the future may bring. '6 This page intentionally left blank ABSTRACT Records of parasitism in crocodilians date back to the early 1800s, distributed among published and unpublished manuscripts, and international parasite catalogs. It is possible that parasites of crocodilians are highly host specific, resulting in a relationship that began over 200 million years ago. Analyzing parasite-host specificity, geographic distribution, and taxonomy can provide otherwise cryptic details about crocodilian ecology and evolution, as well as their local food web dynamics. This information may also be useful to implement improved conservation tactics for both crocodilians and their habitat. As climate change, anthropogenic conflict, and environmental pollution endanger crocodilian ecosystems, there is a need for organized information on crocodile, alligator, caiman, and gharial infectious diseases. This is the first checklist of crocodilians and their parasites. I trust this compilation will encourage further studies that incorporate ecology, parasitology, phylogeography, coevolution, and immunology to bring insight to crocodilian life-history, evolution, and conservation. Additionally, this information may encourage veterinarians, biologists, and ecologists to expand studies of other reptilian-parasite systems, and perhaps improve our understanding of human impacts on ecosystems. 6' This page intentionally left blank INTRODUCTION The order Crocodylia comprises of an archaic lineage of reptiles descended from an archosaurian ancestor that lived about 254 million years ago (Janke and Arnason, 1997). Behavioral, morphological and physiological adaptations such as parental care, a four-chambered heart, and osmoregulation capabilities are crocodilian characteristics that distinguish them from other reptilians (Shine, 1988; Mazzotti and Dunson, 1989; Franklin and Axelsson, 1994). The immediate and non-hesitant immune system of crocodilians, in comparison to other vertebrates, is an exceptional evolutionary adaptation in response to wounds from intra- and interspecific conflict in bacteria-laden environments (Merchant et al., 2003, 2004, 2005). This suite of adaptations may have contributed to their long term persistence in changing environments since the Triassic. Extant crocodilians inhabit sub-tropical and tropical locations around the world. As keystone predators, crocodilians are a significant contributor to community structure in generally high biomass, and low turnover ecosystems. However, their greatly reduced abundance under human hunting pressure has extirpated them from many locations, restricted their geographic ranges, and diminished their ecosystem role (Platt and Thorbjarnarson, 2000; Huchzermeyer, 2003; Richards et al., 2004; van der Ploeg and van Weerd, 2008; Shirley et al., 2009). Ultimately this can impact the interaction between crocodilians and their parasites, resulting in two negative outcomes. First, anthropogenic interactions can decrease parasitic prevalence and abundance in a host population by external factors hindering parasitic transmission or killing free-living stages of the parasite (Bush et al., 2001). Although this may seem beneficial, parasites that are host-specific for crocodilians may have developed relationships with their hosts, that may have contributed over evolutionary time the ability to repel a broad spectrum of invasive pathogens. The alteration of the host-parasite dynamics may contribute S T UniversityofCaliforniaPublicationsinZoology to a reduced ability to adjust to anthropogenic disturbances, enhancing crocodilian susceptibility to common and foreign parasites (Combes, 2001; Schoeb et al., 2002). In contrast, ecosystem perturbations may enhance the prevalence and intensity of certain parasites within a host population (Lafferty, 1997; Lafferty and Kuris, 1999). Increased parasite burdens in concurrence with immunosuppression caused by chronic stress in rapidly changing environments may enable viral, bacterial and parasitic infections to proliferate and overwhelm normal defense mechanisms, ultimately increasing morbidity or mortality of the host (Lafferty, 1997; Lafferty and Kuris, 1999; Koprivnikar and Walker, 2011). This is of considerable concern as the decline or elimination of keystone predators, including their parasites, can alter trophic dynamics, potentially triggering the collapse of an ecosystem (Fortin et al., 2005; Hudson et al., 2006; Myers et al., 2007; Ripple and Beschta, 2007). The purpose of this database is to provide information that can further knowledge on the crocodilian- parasite dynamic that may be useful for scientific research and conservation management. As an example of the utility of this database, knowledge of shared parasite species or genera may assist investigations on the phylogenetic relationships among the New World crocodilian clade (Densmore and White, 1991; Brochu, 2000; Ray and Densmore, 2003; White and Densmore, 2000). Molecular and fossil evidence indicate that Crocodylus originated in Africa,
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