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Conservation Issues
C HA P T E R
27 Conservation Issues Charles J. Innis
VETERINARY CONTRIBUTIONS TO REPTILE CONSERVATION Veterinarians play an important role in biodiversity conservation.1 Veterinarians with expertise in the medical management of reptiles have participated in a variety of reptile conservation programs for several decades, and involvement in such programs has increased substantially in the first decade of the twenty-first century. Well-known conservation and recovery programs for species such as Galapagos Tortoises (Chelonoidis [Geochelone] nigra), Chinese Alligators (Alligator sinensis), and Kemp’s Ridley Sea Turtle (Lepidochelys kempii) have utilized veterinarians in developing quarantine programs, disease management, pathology investigations, nutritional planning, and more (Figures 27-1 and 27-2).2-7 The number of endangered reptile species is increasing, largely because of habitat loss and unsustainable harvesting or incidental mortality associated with human activities.8-10 In addition, it is likely that for some taxa, climate change, pollution, competition with invasive species, and disease, may also be detrimental.8 In 2011, the International Union for the Conservation of Nature (IUCN) Red List of Threatened Species categorized 32 turtle species, 6 crocodilian species, and 83 squamate species as critically endangered and 44 turtle species, 1 crocodilian species, and 189 squamate species as endangered.11 These categories respectively indicate an “extremely high” or “very high” risk of extinction in the wild. Of great concern is the continued decline of many populations despite significant conservation efforts over the past decade.12 Regardless of numerous conservation activities, threats to many reptile populations remain extremely serious.
in the field, and assessment of the safety of techniques used by field biologists. Surgical implantation or attachment of radio or satellite transmitters has become a routine part of many reptile ecology studies (Figure 27-3).13,14 Such transmitters can be used to track the location of the animal over time, and more advanced transmitters can also record temperature or dive depth data. While PIT tags have been used by reptile biologists for some time, recent veterinary observations have led to modification of tag implantation techniques and have highlighted complications seen with PIT tag insertion in certain species and in certain anatomic locations.15,16 See Chapter 29 for more details. Laparoscopy and, recently, cystoscopy have been used to determine the sex of immature reptiles so that sex ratios produced under natural or artificial conditions could be assessed (see Chapter 13, Diagnostic Endoscopy. 17-19 This information is especially important for programs that artificially incubate eggs of species that exhibit temperature-dependent sex determination or artificially enhance the survival likelihood of juveniles (“head starting”). Nonlethal early identification of sex may be
BASIC ECOLOGY STUDIES Implementing effective conservation strategies for any species requires a thorough understanding of its natural history. Data such as population size, home range, fecundity, recruitment, sex ratios, longevity, migratory patterns, and genetic diversity are required. While historically the realm of herpetologists, ecologists, and general biologists, field studies increasingly involve or require veterinary expertise or oversight. Veterinarians have particularly become involved with the surgical implantation or attachment of telemetry devices, passive integrated transponder (PIT or microchip) tagging, laparoscopic reproductive evaluation, oversight of capture events, administration of anesthesia
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FIGURE 27-1 Drs. Stephen Divers and Sam Rivera per-
forming endoscope-assisted oophroectomy in a Galapagos Tortoise (Chelonoidis [Geochelone] nigra) in the Galapagos Islands. This project sterilized genetically hybridized tortoises so that they could be released onto the islands to function as ecologically important large herbivores until genetically pure tortoises can be reestablished. (Photo courtesy Dr. Joe Flanagan, Houston Zoo, Houston, Tex.)
CHAPTER 27 • Conservation issues important for monitoring the potential effects of global climate change on species for which sex determination is temperature dependent. Laparoscopy has also been used, particularly in sea turtles, for assessment of the reproductive status of subadults and adults as part of population-based reproductive health studies.20 Veterinary involvement in field procedures has resulted in the development of safe short-acting anesthetic protocols and has highlighted possible adverse effects of some types of manual restraint.4,5,21-23 For example, potentially adverse positional effects on intraocular pressures were documented by veterinarians during a Loggerhead Sea Turtle (Caretta caretta) laparoscopy study.23 Blood collection is often required for basic ecology studies, and veterinarians have recently developed position statements on acceptable and unacceptable methods for blood collection from tortoises in the field.24 Federal authorities may require a veterinarian to be involved with certain procedures for protected species. For example, in the United States, studies that involve capture and handling of the endangered Leatherback Sea Turtle (Dermochelys coriacea) require the presence of a veterinarian for physiological monitoring and emergency resuscitation if adverse events occur (Figure 27-4).14,25
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HEALTH EVALUATION OF REPTILE POPULATIONS The number of “health assessment” or “health evaluation” studies of “normal” populations of free-ranging reptiles is increasing. It can be debated how to define normal, and many reptile populations have already been infiltrated by disease, toxins, and other stressors. Clinical pathologists debate whether these studies are producing baseline data, normal values, reference intervals, or other values. In many cases, the number of animals involved in the study is less than desired for determination of true reference intervals. Nonetheless, these studies seek to characterize various aspects of the health of native reptiles in their natural habitats, often focusing on hematology, plasma biochemistry, fecal parasitology, and serologic evidence of disease exposure. In many cases, these studies provide the only available data for a given species; thus they can be valuable for comparison to clinical data obtained from captive reptiles and for comparison to future data from the same population.26-31 Health evaluations have highlighted the significant effects of seasonality, sex, age, and stressors on clinical pathology data of reptiles.14,25,31-33 If free-ranging reptiles are broadly screened, specific abnormalities may be found, which may lead the way to more specific studies.
INFECTIOUS DISEASE RESEARCH
FIGURE 27-2 This Chinese Alligator (Alligator sinensis) was hatched as part of a captive breeding program for this rare species. (Photo courtesy Michael Ralbovsky, Rainforest Reptile Shows, Mass.)
FIGURE 27-3 Radio transmitter implantation into the coelom
of an Indigo Snake (Drymarchon couperi) in Georgia, United States. (Photo courtesy Dr. Terry M. Norton, Georgia Sea Turtle Center, Jekyll Island, Ga.)
The population decline of North American tortoises of the genus Gopherus has been well-documented and is likely due in part to an upper respiratory tract disease caused by Mycoplasma agassizii.34 The identification and characterization of this disease was largely due to the efforts of veterinary professionals and their colleagues.34 Similarly, much of the characterization of the fibropapilloma syndrome of sea turtles was completed by veterinarians.33,35 The threat of disease for many reptile populations is unclear, but it is likely that catastrophic population declines could occur due to the introduction of infectious diseases. As such, characterization of infectious diseases of reptiles is critical for reptile conservation, even if only characterized in captive reptiles. Familiarity with etiologic
FIGURE 27-4 A live Leatherback Turtle (Dermochelys coriacea) evaluated during fisheries gear disentanglement in Massachusetts. (Photo courtesy Dr. Charles Innis, New England Aquarium, Boston, Mass.)
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FIGURE 27-5 Typical skin lesions (black dots) seen with West Nile Virus infection of American Alligators (Alligator mississippiensis). (Photo courtesy Dr. Javier G. Nevarez, Louisiana State University, Baton Rouge, La.)
agents, clinical signs, pathologic lesions, pathogenesis, and diagnostic modalities may expedite the future identification of known pathogens in free-ranging populations and may allow for more rapid characterization of novel pathogens. In recent years, characterization of iridovirus, adenovirus, herpesvirus, and novel protozoal infections in captive and freeranging chelonians has provided a great deal of basic data that will be useful for future disease investigations.36-45 Documentation of West Nile Virus infection in alligators in the United States demonstrated infection of a novel host with an exotic virus (Figure 27-5).46-48 Such outbreaks should convince those involved with reptile conservation programs that the risk of infectious disease is real, especially for programs involving translocation and repatriation. Animals involved in such programs should be carefully screened for disease by following recommended veterinary protocols.28,49,50
ASIAN TURTLE CRISIS The magnitude of the live turtle trade in Southeast Asia has been widely reported over the past decade.9 Beginning in the late 1990s, a number of conservation organizations and private individuals began to document the unsustainable consumption of Asian turtles for food and medicinal use. Networks of turtle collectors began to harvest species broadly across Southeast Asia and channel them into large markets in cities such as Hong Kong (Figure 27-6). Among the literally tons of turtles in the trade were a variety of critically endangered species and species previously unknown to science. In some cases, novel species were described from specimens found in food markets, having never been observed in the wild.51 As species that rely on the longevity of reproductively mature individuals to ensure population survival, turtles are particularly prone to extirpation due to mortality of adults.52 It became clear that many Asian species were in imminent risk of extinction. In response to this crisis, a number of workshops were held throughout the world, and several alliances and consortiums were created. Since that time, veterinarians have continued to participate in Asian turtle conservation
FIGURE 27-6 Live turtle market in Southeast Asia. (Photo courtesy of Cris Hagen.)
efforts focused on range country programs, ex situ captive breeding, rehabilitation of confiscated specimens, disease description, and education. Initially, much effort was focused on medical management and rehabilitation of confiscated Asian turtles, for purposes of establishing ex situ “assurance colonies”. Many species’ husbandry needs were poorly known, and most individuals were seriously ill at the time of confiscation. Attempts to maintain these specimens in captivity often failed because the turtles refused food and succumbed to parasitic and bacterial diseases.53-56 Soon, however, medical management protocols began to improve the survival rate of these specimens.53-56 Combined with natural history field studies, this work led to successful treatment, establishment of founder captive populations, and eventual successful breeding of species with historically high mortality rates, such as the Impressed Tortoise (Manouria impressa) and the Sulawesi Forest Turtle (Leucocephalon yuwonoi) (Figure 27-7).57-59 Veterinary work with these species also led to descriptions of a number of novel parasites (e.g., Myxidium hardella), viral diseases (e.g., Sulawesi tortoise adenovirus-1), and common pathologic findings.55,56,60,61 Veterinarians have also helped to establish and implement range country conservation and veterinary education programs in Southeast Asia. These efforts have included provision of clinical care, implementation of quarantine programs, and education of local veterinarians at centers such as Cuc Phuong in Vietnam and Madras Crocodile Bank in India.62,63 Recently, veterinarians played a critical role in the transport of one of the last living Yangtze Giant Softshell Turtles (Rafetus swinhoei) into a captive breeding program in China, and veterinarians continue to be involved in the nutritional, medical, and reproductive management of the last individuals of this species (Figure 27-8).64,65 Despite these efforts, the outlook for the majority of Asian turtle species is grim. Recent reassessments of these species by the IUCN demonstrate a 90% increase in the number of species listed as Critically Endangered over the past decade.12
REPTILES AFFECTED BY OIL SPILLS In the last 10 years, veterinarians have been involved in medical management of reptiles affected by several major oil
CHAPTER 27 • Conservation issues
FIGURE 27-7 The first known captive-bred hatchling of the
Sulawesi Forest Turtle (Leucocephalon yuwonoi). This hatchling is the offspring of adults salvaged from the Southeast Asian live turtle trade. (Photo courtesy Dr. Charles Innis, New England Aquarium, Boston, Mass.)
FIGURE 27-8 One of the last living Yangtze Giant Softshell
Turtles (Rafetus swinhoei). (Photo courtesy Dr. Paul P. Calle, Wildlife Conservation Society, Bronx, NY.)
spills. In 2001, a large oil spill in the Galapagos Islands led to the death of 62% of Marine Iguanas (Amblyrhynchus cristatus) on one affected island, and veterinarians subsequently became involved with the health assessment of this species (Figure 27-9).66,67 In 2010, approximately 800,000 gallons of oil were spilled into the Kalamazoo River in Michigan, and approximately 2000 reptiles and amphibians were admitted into rehabilitation.68 Also in 2010, the massive Deepwater Horizon oil spill in the Gulf of Mexico resulted in contamination of hundreds of endangered sea turtles, including Kemp’s Ridley, Loggerhead, Green (Chelonia mydas), and Hawksbill (Eretmochelys imbricata) Sea Turtles (Figure 27-10).69 Although the majority of turtles that were admitted to rehabilitation survived, the number of turtles that died entrapped in oil at sea remains unknown. The most current publicly available data from the Deepwater Horizon oil spill indicate that approximately 90% of turtles that were admitted to rehabilitation were later released.69 Clinical data obtained by veterinarians during treatment of these oiled turtles are being withheld until legal aspects of the case have been resolved.
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FIGURE 27-9 Galapagos Marine Iguana (Amblyrhynchus cristatus) during general anesthesia in the Galapagos Islands. Liver biopsies were performed as part of a post–oil spill health assessment. (Photo courtesy Dr. Mark Mitchell, University of Illinois, Urbana, Ill.)
FIGURE 27-10 A Kemp’s Ridley Sea Turtle (Lepidochelys
kempii) undergoing medical evaluation after being recovered at sea during the Deepwater Horizon oil spill in the Gulf of Mexico, 2010. (Photo courtesy Dr. Charles Innis, New England Aquarium, Boston, Mass.)
COLD-STUNNED SEA TURTLES Stranding of sea turtles during periods of cold weather (coldstunning) has been reported from several countries.70-72 In January, 2010, approximately 4500 sea turtles were stranded during a cold-stun event in Florida.73 While such events inevitably occurred throughout history and may not have represented a threat to large, healthy populations of sea turtles, these events may represent a threat to the depleted sea turtle populations of the twenty-first century. In addition to widespread sea turtle mortality from fishery interactions, nesting beach destruction, harvesting, toxin exposure, and disease, the death of hundreds of sea turtles from cold-stunning likely has a negative impact on the population. In some geographic areas, cold-stunning events involving the rarest sea turtle species, Kemp’s Ridley Sea Turtle, occur annually, often affecting hundreds of turtles and resulting in a more than 50% mortality rate.70 Over the past 20 years, veterinary protocols for the management of cold-stunned turtles
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FIGURE 27-11 A Spotted Turtle (Clemmys guttata) killed by a
vehicle on a Massachusetts road. This once common species has been recently upgraded to Endangered by the International Union for the Conservation of Nature (IUCN). (Photo courtesy Dr. Charles Innis, New England Aquarium, Boston, Mass.)
have emerged, and a relatively high survival rate has been achieved.74 Data from these events have helped to document the adverse physiologic and common pathologic findings in cold-stunned sea turtles and have provided prognostic information for the assessment of individual animals.75-81
WILDLIFE REHABILITATION Wildlife rehabilitation centers throughout the world provide care for injured reptiles. Although snakes, crocodilians, and lizards are occasionally seen, the majority of reptiles presented to wildlife rehabilitators are turtles. The number of turtles that are injured by vehicles each year globally is beyond estimation. Locally, thousands of turtles and other reptiles can be killed adjacent to a single wetland in a single year (Figure 27-11).82 Marine turtles are often injured by boats, caught in fishing gear, or affected by neurologic syndromes of unknown etiology.14,83-86 In some cases, injured and ill reptiles can be successfully treated and released to the wild. A “turtle team” has been established at one U.S. veterinary school to provide students with early exposure to clinical case management of injured native reptiles.87 In addition to providing clinical care, wildlife rehabilitation centers can play an important role in reptile conservation through documenting locality data of rare native species, investigating local disease outbreaks, hatching eggs recovered from road-killed females, and educating the public about risks to local native species. Veterinarians with expertise in wildlife rehabilitation have assisted in the development of triage guidelines and injury assessment protocols for several reptile species.88,89
FIGURE 27-12 Phallectomy for sterilization of a feral Green
Iguana (Iguana iguana) in south Florida. (Photo courtesy Dr. Douglas R. Mader, Marathon Veterinary Hospital, Marathon, Fla.)
Such introductions have been especially damaging for island environments, where native species are often unable to compete with aggressive introduced species. The introduction of the Brown Tree Snake (Boiga irregularis) to Guam and other Pacific islands has been devastating for many bird species, as well as native reptiles.90 In south Florida, Monitor Lizards, Green Iguanas, pythons, and many other reptiles have been introduced.91,92 The North American Red-eared Slider (Trachemys scripta elegans) has been introduced to many other continents.93 The impact of these species is not yet well-defined but is subject to heated debate. Veterinarians have become involved in these situations to develop sterilization strategies, provide testimony in legal and political venues, assess disease risk, and determine likelihood of range expansions (Figure 27-12).94,95 Some studies have demonstrated transmission of parasites between native and invasive reptile species.93,96 See Chapter 28, Invasive and Introduced Reptiles and Amphibians for more details.
ENVIRONMENTAL TOXICOLOGY In collaboration with toxicologists, endocrinologists, and other colleagues, veterinarians have demonstrated exposures of freeranging reptiles to heavy metals, pesticides, and other toxic chemicals. High levels of such contaminants have been found in many species, and recent data demonstrate significant correlations between contaminant concentrations, immune function, and hematologic and biochemical variables.97-99 Further research is needed to document the mechanisms for these correlations, sources of contaminants, and as yet undescribed effects.
INVASIVE SPECIES
GENERAL VETERINARY MANAGEMENT OF CAPTIVE REPTILES
Global commerce has led to the purposeful and accidental movement of reptiles to localities far from their native ranges. In some cases, these new localities provide a favorable environment for establishment of breeding populations.
Although not immediately apparent, general veterinary care for captive reptiles contributes to reptile conservation. In thousands of zoos, aquaria, and nature centers around the world, healthy captive reptiles act as ambassadors for their species.
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reptile conservation. For example, the laparoscopic-assisted oophorectomy technique that was recently used to sterilize hybrid Galapagos Tortoises for an in situ ecologic recovery project was originally developed in private practice for management of pet turtle reproductive disorders.4,102 It is clear that many of the advances in clinical management of reptiles over the past 40 years were made by private practitioners that took the time to thoroughly document their work, teach veterinary students and other veterinarians, and publish their findings.103
REFERENCES
FIGURE 27-13 An endangered Fiji Iguana (Brachylophus
fasciatus) in a captive breeding facility in the United States. (Photo courtesy San Diego Zoo Global, San Diego, Calif.)
In an increasingly urbanized world, these animals may provide the only exposure of humans to live reptiles. Such experiences can be quite profound, and their importance in fostering environmental stewardship, particularly for children, should not be discounted. On a larger scale, veterinary management of captive individuals in zoos and aquaria has been important for the establishment and maintenance of captive breeding programs for endangered species such as the Fiji Banded Iguana (Brachylophus fasciatus) (Figure 27-13).100,101
ADVERSE EFFECTS OF GOOD INTENTIONS Well-intentioned programs and well-intentioned individuals can have potential adverse effects. Veterinarians are in a strong position to prevent such problems. By providing leadership in the realms of quarantine and disease risk, veterinarians can reduce the likelihood of adverse effects. Well-intentioned individuals may not, at first, recognize that untreated waste water from an exotic turtle breeding facility could present an infectious disease risk to local native turtles. They may not realize that native snakes for a head start program should not be raised in the same facility as nonnative snakes. It is critical for veterinarians to provide information and advice in such cases.
THE ROLE OF PRIVATE VETERINARY PRACTITIONERS While often considered the realm of zoo, aquarium, or university veterinarians, reptile conservation can be greatly enhanced by private practitioners. Much of the work cited herein was conducted in part or entirely by private practitioners. It is realistic that a reptile with a previously unknown disease will be seen at any private practice on any given day. It is possible that a turtle presented to a private practice after being found on a local road is, in fact, an endangered species from a previously unknown population. It is possible that veterinary care provided by a private practitioner will allow a local reptile education program to inspire the next generation of reptile conservationists. It is possible that a new technique developed in private practice may have wider application in the realm of
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19. Selleri P, DiGirolamo N, Melidone R. Cystoscopic sex identification of posthatchling chelonians. J Am Vet Med Assoc 2013;242:1744-1750. 20. Blanvillain G, Pease AP, Segars AL, et al. Comparing methods for the assessment of reproductive activity in adult male loggerhead sea turtles Caretta caretta at Cape Canaveral, Florida. Endang Spec Res 2008;6:75-85. 21. MacLean RA, Harms CA, Braun-McNeill J. Propofol anesthesia in loggerhead (Caretta caretta) sea turtles. J Wildl Dis 2008;44:143-150. 22. Harms CA, Eckert SA, Kubis SA, et al. Field anaesthesia of leatherback sea turtles (Dermochelys coriacea). Vet Rec 2007;161:15-21 23. Chittick B, Harms C. Intraocular pressure of juvenile loggerhead sea turtles (Caretta caretta) held in different positions. Vet Rec 2001;149:587-589. 24. Johnson J. Nail trimming for blood collection from desert tortoises, Gopherus agassizii: panel summary. J Herpetol Med Surg 2006;16: 61-62. 25. Harris HS, Benson SR, Gilardi KV, et al. Comparative health assessment of western Pacific leatherback turtles (Dermochelys coriacea) foraging off the coast of California: 2005-2007. J Wildl Dis 2011;47:321-337. 26. Espinosa-Aviles D, Salomon-Soto VM, Morales-Martinez S. Hematology, blood chemistry, and bacteriology of the free-ranging Mexican beaded lizard (Heloderma horridum). J Zoo Wildl Med 2008;39:21-27. 27. James SB, Iverson J, Greco V, et al. Health assessment of Allen Cays rock iguana, Cyclura cyclura inornata. J Herpetol Med Surg 2006;16:93-98. 28. Gartrell BD, Jillings E, Adlington BA, et al. Health screening for a translocation of captive-reared tuatara (Sphenodon punctatus) to an island refuge. N Z Vet J 2006;54:344-349. 29. Deem SL, Dierenfeld ES, Sounguet GS, et al. Blood values in free ranging nesting leatherback sea turtles (Dermochelys coriacea) on the coast of the Republic of Gabon. J Zoo Wildl Med 2006;37:464-471. 30. Fisse A, Draud M, Raphael B, et al. Differential leukocyte counts of critically endangered Grand Cayman blue iguanas, Cyclura nubila lewisi. J Herpetol Med Surg 2004;14:19-21. 31. Brenner D, Lewbart G, Stebbins M, et al. Health survey of wild and captive bog turtles (Clemmys muhlenbergii) in North Carolina and Virginia. J Zoo Wildl Med 2002;33:311-316. 32. Gottdenker NL, Jacobson ER. Effect of venipuncture sites on hematologic and clinical biochemical values in desert tortoises (Gopherus agassizii). Am J Vet Res 1995;56:19-21. 33. Aguirre AA, Balazs GH, Spraker TR, et al. Adrenal and hematological responses to stress in juvenile green turtles (Chelonia mydas) with and without fibropapillomas. Physiol Zool 1995;68:831-854. 34. Brown MB, Schumacher IM, Klein PA, et al. Mycoplasma agassizii causes upper respiratory tract disease in the desert tortoise. Infect Immun 1994;62:4580-4586. 35. Herbst LH, Jacobson ER, Klein PA, et al. Comparative pathology and pathogenesis of spontaneous and experimentally induced fibropapillomas of green turtles (Chelonia mydas). Vet Pathol 1999;36:551-564. 36. Johnson AJ, Pessier AP, Wellehan JFX, et al. Ranavirus infection of free-ranging and captive box turtles and tortoises in the United States. J Wildl Dis 2008;44:851-863. 37. Johnson AJ, Wendland L, Norton TM, et al. Development and use of an indirect enzyme-linked immunosorbent assay for detection of iridovirus exposure in gopher tortoises (Gopherus polyphemus) and eastern box turtles (Terrapene carolina carolina). Vet Microbiol 2010;142:160-167. 38. Johnson AJ, Pessier AP, Jacobson ER. Experimental transmission and induction of ranaviral disease in western ornate box turtles (Terrapene ornata ornata) and red-eared sliders (Trachemys scripta elegans). Vet Pathol 2007;44:285-297. 39. Rivera S, Wellehan JFX, McManamon R, et al. Systemic adenovirus infection in Sulawesi tortoises (Indotestudo forstenii) caused by a novel siadenovirus. J Vet Diagn Invest 2009;21:415-426. 40. Marschang RE, Gravendyck M, Kaleta EF. Herpesviruses in tortoises: investigations into virus isolation and the treatment of viral stomatitis in Testudo hermanni and T. graeca. Zentralbl Veterinarmed B 1997;44:385-394.
41. Origgi FC, Romero CH, Bloom DC, et al. Experimental transmission of a herpesvirus in Greek tortoises (Testudo graeca). Vet Pathol 2004;41:50-61. 42. Stacy BA, Wellehan JFX, Foley AM, et al. Two herpesviruses associated with disease in wild Atlantic loggerhead sea turtles (Caretta caretta). Vet Microbiol 2008;126:63-73. 43. Garner MM, Gardiner CH, Wellehan JF, et al. Intranuclear coccidiosis in tortoises: nine cases. Vet Pathol 2006;43:311-320. 44. Innis CJ, Garner MM, Johnson AJ, et al. Antemortem diagnosis and characterization of nasal intranuclear coccidiosis in tortoises. J Vet Diagn Invest 2007;19:660-667. 45. Schmidt V, Dyachenko V, Aupperle H, et al. Case report of systemic coccidiosis in a radiated tortoise (Geochelone radiata). Parasitol Res 2008;102:431-436. 46. Miller DL, Mauel MJ, Baldwin C, et al. West Nile virus in farmed alligators. Emerg Infect Dis 2003;9:794-799. 47. Jacobson ER, Ginn PE, Troutman JM, et al. West Nile Virus infection in farmed American alligators (Alligator mississippiensis) in Florida. J Wildl Dis 2004;41:96-106. 48. Nevarez JG, Mitchell MA, Morgan T, et al. Association of West Nile virus with lymphohistiocytic proliferative cutaneous lesions in American alligators (Alligator mississippiensis) detected by RT-PCR. J Zoo Wildl Med 2008;39:562-566. 49. Jacobson ER, Behler JL, Jarchow J. Health assessment of chelonians and release into the wild. In: Fowler ME, ed. Zoo and wild animal medicine: current therapy. 4th ed. Philadelphia: WB Saunders Co, 1999;232-242. 50. Pasmans F, Blahak S, Martel A, et al. Introducing reptiles into a captive collection: the role of the veterinarian. Vet J 2008;175:53-68. 51. Lehr E, Fritz U, Obst FJ. Cuora galbinifrons picturata subsp. nov., eine Unterart der Hinterindischen Scharnierschildkröte. Herpetofauna 1998;20(113):5-11. 52. Congdon JP, Dunham AE, van Loben Sels RC. Delayed sexual maturity and demographics of Blanding’s turtles (Emydoidea blandingii): implications for conservation and management of long-lived organisms. Conserv Biol 1993;7:826-833. 53. Bonner BB. Chelonian therapeutics. Vet Clin N Am Exot Anim Pract. 2000;3(1):257-332. 54. Innis C. Medical issues affecting the rehabilitation of Asian chelonians. Turtle Tortoise Newslett 2000;4:14-16. 55. Innis CJ, Garner M, Raymond J. Observations on captive husbandry and pathology of the critically endangered Sulawesi forest turtle, Leucocephalon yuwonoi, in Proceedings. 9th Annu Conf Assoc Rept Amphib Vet 2002;21-26. 56. Innis C, Garner M, Tabaka C, et al. Gross necropsy and histopathological findings in imported impressed tortoises (Manouria impressa): seventeen cases. J Herpetol Med Surg 2006;16:49-52. 57. Rivera S, Crane M, MacManamon R. Medical and surgical treatment of gastric foreign bodies in newly imported impressed tortoises, in Proceedings. 13th Annu Conf Assoc Rept Amphib Vet 2006: 78-82. 58. Lawson D. Captive reproduction of the impressed tortoise—sustained success. Turtle Survival Alliance Newslett 2008:17. 59. Hagen C, Platt SG, Innis CJ. Leucocephalon yuwonoi (McCord, Iverson, and Boeadi 1995)— Sulawesi forest turtle, Kura-Kura Sulawesi. In: Rhodin AGJ, Pritchard PCH, van Dijk PP, et al, eds. Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian research monographs 5. 2009;039.1-039.7. Available at: http://www.iucn-tftsg.org/cbftt/. 60. Garner MM, Bartholomew JL, Whipps CM, et al. Renal myxozoanosis in crowned river turtles Hardella thurjii: description of the putative agent Myxidium hardella n. sp. by histopathology, electron microscopy, and DNA sequencing. Vet Pathol 2005;42:589-595. 61. Bursey CR, Goldberg SR, Miller CL. Two new species of Falcaustra and comments on helminths of Norops tropidolepis (Sauria: Polychrotidae) from Costa Rica. J Parasitol 2004;90:598-603.
CHAPTER 27 • Conservation issues 62. Naorem L, Sirsi S, Singh S. Chelonian health management and rehabilitation training workshop for Indian veterinarians. Turtle Survival 2011;96. 63. Hendrie D. The Turtle Conservation Center celebrates a banner year. Turtle Survival Alliance Newslett 2006;10. 64. Kuchling G. Historic efforts to save the world’s rarest turtle. Turtle Survival Alliance Newslett 2008:4-7. 65. Kuchling G, Shunqing L, King EH. The fourth year of Rafetus swinhoei breeding attempts. Turtle Survival 2011:78-79. 66. Wikelski M, Wong V, Chevalier B, et al. Marine iguanas die from trace oil pollution. Nature 2002;417:607-608. 67. Mitchell M, Nevarez J, Kim DY, et al. Evaluating the long term health effects of an unnatural oil spill on marine iguanas (Amblyrhynchus cristatus), in Proceedings. 10th Annu Conf Assoc Rept Amphib Vet 2003;81-82. 68. Binder Park Zoo Web site. Kalamazoo River animal information. Available at: http://www.binderparkzoo.org/kalamazooriver/index. php. Accessed September 27, 2011. 69. National Marine Fisheries Service Web site. Sea turtles and the Gulf of Mexico oil spill. Available at: http://www.nmfs.noaa.gov/pr/health /oilspill/turtles.htm. Accessed September 30, 2011. 70. Morreale SJ, Meylan A, Sadove SS, et al. Annual occurrence and winter mortality of marine turtles in New York waters. J Herpetol 1992;26:301-308. 71. Still BM, Griffin CR, Prescott R. Climatic and oceanographic factors affecting daily patterns of juvenile sea turtle cold-stunning in Cape Cod Bay, Massachusetts. Chelon Conserv Biol 2005;4:883-890. 72. Bentivegnal F, Breber P, Hochscheid S. Cold stunned loggerhead turtles in the south Adriatic Sea. Marine Turtle News 2000;97:1-3. 73. Metee N. Florida’s 2010 cold stunned sea turtles, in Proceedings. 17th Annu Conf Assoc Rept Amphib Vet 2010;43. 74. Wyneken J, Mader DR, Weber ES, et al. Medical care of seaturtles. In: Mader D, ed. Reptile medicine and surgery. 2nd ed. St. Louis: Elsevier, 2006;972-1007. 75. Carminati C, Gerle E, Kiehn LL, et al. Blood chemistry comparison of healthy vs. hypothermic juvenile Kemp’s ridley sea turtles (Lepidochelys kempii) in the New York Bight, in Proceedings. 14th Ann Symp Sea Turtle Biol and Cons. NOAA Tech Mem NMFS-SEFSC-351, 1994;203-207. 76. Turnbull BS, Smith CR, Stamper MA. Medical implications of hypothermia in threatened loggerhead (Caretta caretta) and endangered Kemp’s ridley (Lepidochelys kempii) and Green (Chelonia mydas) sea turtles, in Proceedings. Joint Conf Am Assoc Zoo Vet Int Assoc Aquat Anim Med 2000;31-35. 77. Innis C, Tlusty M, Merigo C, et al. Metabolic and respiratory status of cold-stunned Kemp’s ridley sea turtles (Lepidochelys kempii). J Comp Physiol B 2007;177:623-630. 78. Innis CJ, Ravich JB, Tlusty MF, et al. Hematologic and plasma biochemical findings in cold-stunned Kemp’s ridley sea turtles (Lepidochelys kempii): 176 cases (2001-2005). J Am Vet Med Assoc 2009;235:426-432. 79. Innis CJ, Nyaoke AC, Williams CR, et al. Pathologic and parasitologic findings of cold-stunned Kemp’s ridley sea turtles (Lepidochelys kempii) stranded on Cape Cod, Massachusetts, 2001-2006. J Wildl Dis 2009;45:594-610. 80. Anderson ET, Harms CA, Stringer EM, et al. Evaluation of hematology and serum biochemistry of cold-stunned green sea turtles (Chelonia mydas) in North Carolina, USA. J Zoo Wildl Med 2011;42:247-255. 81. Keller KA, Innis CJ, Tlusty MF, et al. Metabolic and respiratory derangements associated with mortality in cold-stunned Kemp’s ridley turtles (Lepidochelys kempii): 32 cases (2005-2009). J Am Vet Med Assoc 2012;240:317-323. 82. Aresco MJ. Mitigation measures to reduce highway mortality of turtles and other herpetofauna at a North Florida lake. J Wildl Manage 2005;69:549-560. 83. Orós J, Torrent A, Calabuig P, et al. Diseases and causes of mortality among sea turtles stranded in the Canary Islands, Spain (1998-2001). Dis Aquat Organ 2005;63:13-24.
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84. Jacobson ER, Homer BL, Stacy BA, et al. Neurological disease in wild loggerhead sea turtles Caretta caretta. Dis Aquat Organ 2006;70: 139-154. 85. Valente A, Parga M, Velarde R, et al. Fishhook lesions in loggerhead sea turtles. J Wildl Dis 2007;43:737-741. 86. Deem SL, Norton TM, Mitchell M, et al. Comparison of blood values in foraging, nesting, and stranded loggerhead turtles (Caretta caretta) along the coast of Georgia, USA. J Wildl Dis 2009;45:41-56. 87. Lewbart GA, Kishimori J, Christian LS. The North Carolina State University College of Veterinary Medicine Turtle Rescue Team: a model for a successful wild-reptile clinic. J Vet Med Ed 2005;32: 377-381. 88. Phelan SM, Eckert KL. Marine turtle trauma response procedures: a field guide. Beaufort, North Carolina: Wider Caribbean Sea Turtle Conservation Network (WIDECAST), 2006. 89. Upite C. Evaluating sea turtle injuries in northeast fishing gear. US Dept Commerce, Northeast Fish Sci Cent Ref Doc 11-10; 2011. Available at http://www.nefsc.noaa.gov/nefsc/publications. Accessed September 30, 2011. 90. Perry G, Rodda GH, Fritts TH, et al. The lizard fauna of Guam’s fringing islets: island biogeography, phylogenetic history, and conservation implications. Glob Ecol Biogeogr Lett 1998;7:353-365. 91. Krysko KL, Burgess JP, Rochford MR, et al. Verified non-indigenous amphibians and reptiles in Florida from 1863 through 2010: outlining the invasion process and identifying invasion pathways and stages. Zootaxa 2011;3028:1-64. 92. Reed RN, Rodda GH. Giant constrictors: biological and management profiles and an establishment risk assessment for nine species of pythons, anacondas, and the boa constrictor. USGS Open File Report 2009;1202. 93. Hidalgo-Vila J, Díaz-Paniagua C, Ribas A, et al. Helminth communities of the exotic introduced turtle Trachemys scripta elegans in southwestern Spain: transmission from native turtles. Res Vet Sci 2009;86:463-465. 94. Mader D. Methods for altering reproductive status in green iguanas (Iguana iguana), in Proceedings. 16th Annu Conf Assoc Rept Amphib Vet 2009;61-62. 95. Jacobson ER. The ability of large constrictors to invade areas of the United Sates beyond southern Florida: fact vs fiction, in Proceedings. 17th Annu Conf Assoc Rept Amphib Vet 2010;58-59. 96. Criscione CD, Font WF. The guest playing host: colonization of the introduced Mediterranean gecko, Hemidactylus turcicus, by helminth parasites in southeastern Louisiana. J Parasit 2001;87:1273-1278. 97. Keller JM, Kucklick JR, Stamper MA, et al. Associations between organochlorine contaminant concentrations and clinical health parameters in loggerhead sea turtles from North Carolina, USA. Environ Health Perspect 2004;112:1074-1079. 98. Day RD, Segars AL, Arendt AD, et al. Relationship of blood mercury levels to health parameters in the loggerhead sea turtle (Caretta caretta). Environ Health Perspect 2007;115:1421-1428. 99. Innis C, Tlusty M, Perkins C, et al. Trace metal and organochlorine pesticide concentrations in cold-stunned, juvenile Kemp’s Ridley sea turtles (Lepidochelys kempii) from Cape Cod, Massachusetts, USA. Chelon Conserv Biol 2008;7:230-239. 100. Stacy BA, Howard L, Kinkaid J, et al. Yolk coelomitis in Fiji Island banded iguanas (Brachylophus fasciatus). J Zoo Wildl Med 2008;39:161-169. 101. Association of Zoos and Aquariums. Aruba Island rattlesnake (Crotalus unicolor) SSP master plan. Available at: http://snaketag.org/SSP-PMPs/ Unicolor%20files/Uni_Start.html, Accessed June 8, 2013. 102. Innis C, Hernandez-Divers SJ, Martinez-Jimenez D. Coelioscopicassisted pre-femoral oophorectomy in chelonians. J Am Vet Med Assoc 2007;230:1049-1052. 103. Jacobson E, Heard D, Isaza R. Future directions in zoological medical education: expectations, potential, opportunities, and mandates: future directions in reptile medical education. J Vet Med Ed 2006;33:373-381.
27 Conservation Issues Charles J. Innis
VETERINARY CONTRIBUTIONS TO REPTILE CONSERVATION Veterinarians play an important role in biodiversity conservation.1 Veterinarians with expertise in the medical management of reptiles have participated in a variety of reptile conservation programs for several decades, and involvement in such programs has increased substantially in the first decade of the twenty-first century. Well-known conservation and recovery programs for species such as Galapagos Tortoises (Chelonoidis [Geochelone] nigra), Chinese Alligators (Alligator sinensis), and Kemp’s Ridley Sea Turtle (Lepidochelys kempii) have utilized veterinarians in developing quarantine programs, disease management, pathology investigations, nutritional planning, and more (Figures 27-1 and 27-2).2-7 The number of endangered reptile species is increasing, largely because of habitat loss and unsustainable harvesting or incidental mortality associated with human activities.8-10 In addition, it is likely that for some taxa, climate change, pollution, competition with invasive species, and disease, may also be detrimental.8 In 2011, the International Union for the Conservation of Nature (IUCN) Red List of Threatened Species categorized 32 turtle species, 6 crocodilian species, and 83 squamate species as critically endangered and 44 turtle species, 1 crocodilian species, and 189 squamate species as endangered.11 These categories respectively indicate an “extremely high” or “very high” risk of extinction in the wild. Of great concern is the continued decline of many populations despite significant conservation efforts over the past decade.12 Regardless of numerous conservation activities, threats to many reptile populations remain extremely serious.
in the field, and assessment of the safety of techniques used by field biologists. Surgical implantation or attachment of radio or satellite transmitters has become a routine part of many reptile ecology studies (Figure 27-3).13,14 Such transmitters can be used to track the location of the animal over time, and more advanced transmitters can also record temperature or dive depth data. While PIT tags have been used by reptile biologists for some time, recent veterinary observations have led to modification of tag implantation techniques and have highlighted complications seen with PIT tag insertion in certain species and in certain anatomic locations.15,16 See Chapter 29 for more details. Laparoscopy and, recently, cystoscopy have been used to determine the sex of immature reptiles so that sex ratios produced under natural or artificial conditions could be assessed (see Chapter 13, Diagnostic Endoscopy. 17-19 This information is especially important for programs that artificially incubate eggs of species that exhibit temperature-dependent sex determination or artificially enhance the survival likelihood of juveniles (“head starting”). Nonlethal early identification of sex may be
BASIC ECOLOGY STUDIES Implementing effective conservation strategies for any species requires a thorough understanding of its natural history. Data such as population size, home range, fecundity, recruitment, sex ratios, longevity, migratory patterns, and genetic diversity are required. While historically the realm of herpetologists, ecologists, and general biologists, field studies increasingly involve or require veterinary expertise or oversight. Veterinarians have particularly become involved with the surgical implantation or attachment of telemetry devices, passive integrated transponder (PIT or microchip) tagging, laparoscopic reproductive evaluation, oversight of capture events, administration of anesthesia
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FIGURE 27-1 Drs. Stephen Divers and Sam Rivera per-
forming endoscope-assisted oophroectomy in a Galapagos Tortoise (Chelonoidis [Geochelone] nigra) in the Galapagos Islands. This project sterilized genetically hybridized tortoises so that they could be released onto the islands to function as ecologically important large herbivores until genetically pure tortoises can be reestablished. (Photo courtesy Dr. Joe Flanagan, Houston Zoo, Houston, Tex.)
CHAPTER 27 • Conservation issues important for monitoring the potential effects of global climate change on species for which sex determination is temperature dependent. Laparoscopy has also been used, particularly in sea turtles, for assessment of the reproductive status of subadults and adults as part of population-based reproductive health studies.20 Veterinary involvement in field procedures has resulted in the development of safe short-acting anesthetic protocols and has highlighted possible adverse effects of some types of manual restraint.4,5,21-23 For example, potentially adverse positional effects on intraocular pressures were documented by veterinarians during a Loggerhead Sea Turtle (Caretta caretta) laparoscopy study.23 Blood collection is often required for basic ecology studies, and veterinarians have recently developed position statements on acceptable and unacceptable methods for blood collection from tortoises in the field.24 Federal authorities may require a veterinarian to be involved with certain procedures for protected species. For example, in the United States, studies that involve capture and handling of the endangered Leatherback Sea Turtle (Dermochelys coriacea) require the presence of a veterinarian for physiological monitoring and emergency resuscitation if adverse events occur (Figure 27-4).14,25
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HEALTH EVALUATION OF REPTILE POPULATIONS The number of “health assessment” or “health evaluation” studies of “normal” populations of free-ranging reptiles is increasing. It can be debated how to define normal, and many reptile populations have already been infiltrated by disease, toxins, and other stressors. Clinical pathologists debate whether these studies are producing baseline data, normal values, reference intervals, or other values. In many cases, the number of animals involved in the study is less than desired for determination of true reference intervals. Nonetheless, these studies seek to characterize various aspects of the health of native reptiles in their natural habitats, often focusing on hematology, plasma biochemistry, fecal parasitology, and serologic evidence of disease exposure. In many cases, these studies provide the only available data for a given species; thus they can be valuable for comparison to clinical data obtained from captive reptiles and for comparison to future data from the same population.26-31 Health evaluations have highlighted the significant effects of seasonality, sex, age, and stressors on clinical pathology data of reptiles.14,25,31-33 If free-ranging reptiles are broadly screened, specific abnormalities may be found, which may lead the way to more specific studies.
INFECTIOUS DISEASE RESEARCH
FIGURE 27-2 This Chinese Alligator (Alligator sinensis) was hatched as part of a captive breeding program for this rare species. (Photo courtesy Michael Ralbovsky, Rainforest Reptile Shows, Mass.)
FIGURE 27-3 Radio transmitter implantation into the coelom
of an Indigo Snake (Drymarchon couperi) in Georgia, United States. (Photo courtesy Dr. Terry M. Norton, Georgia Sea Turtle Center, Jekyll Island, Ga.)
The population decline of North American tortoises of the genus Gopherus has been well-documented and is likely due in part to an upper respiratory tract disease caused by Mycoplasma agassizii.34 The identification and characterization of this disease was largely due to the efforts of veterinary professionals and their colleagues.34 Similarly, much of the characterization of the fibropapilloma syndrome of sea turtles was completed by veterinarians.33,35 The threat of disease for many reptile populations is unclear, but it is likely that catastrophic population declines could occur due to the introduction of infectious diseases. As such, characterization of infectious diseases of reptiles is critical for reptile conservation, even if only characterized in captive reptiles. Familiarity with etiologic
FIGURE 27-4 A live Leatherback Turtle (Dermochelys coriacea) evaluated during fisheries gear disentanglement in Massachusetts. (Photo courtesy Dr. Charles Innis, New England Aquarium, Boston, Mass.)
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SECTION IV • ADVANCES IN BIOLOGY, CONSERVATION, LAW, AND RESEARCH
FIGURE 27-5 Typical skin lesions (black dots) seen with West Nile Virus infection of American Alligators (Alligator mississippiensis). (Photo courtesy Dr. Javier G. Nevarez, Louisiana State University, Baton Rouge, La.)
agents, clinical signs, pathologic lesions, pathogenesis, and diagnostic modalities may expedite the future identification of known pathogens in free-ranging populations and may allow for more rapid characterization of novel pathogens. In recent years, characterization of iridovirus, adenovirus, herpesvirus, and novel protozoal infections in captive and freeranging chelonians has provided a great deal of basic data that will be useful for future disease investigations.36-45 Documentation of West Nile Virus infection in alligators in the United States demonstrated infection of a novel host with an exotic virus (Figure 27-5).46-48 Such outbreaks should convince those involved with reptile conservation programs that the risk of infectious disease is real, especially for programs involving translocation and repatriation. Animals involved in such programs should be carefully screened for disease by following recommended veterinary protocols.28,49,50
ASIAN TURTLE CRISIS The magnitude of the live turtle trade in Southeast Asia has been widely reported over the past decade.9 Beginning in the late 1990s, a number of conservation organizations and private individuals began to document the unsustainable consumption of Asian turtles for food and medicinal use. Networks of turtle collectors began to harvest species broadly across Southeast Asia and channel them into large markets in cities such as Hong Kong (Figure 27-6). Among the literally tons of turtles in the trade were a variety of critically endangered species and species previously unknown to science. In some cases, novel species were described from specimens found in food markets, having never been observed in the wild.51 As species that rely on the longevity of reproductively mature individuals to ensure population survival, turtles are particularly prone to extirpation due to mortality of adults.52 It became clear that many Asian species were in imminent risk of extinction. In response to this crisis, a number of workshops were held throughout the world, and several alliances and consortiums were created. Since that time, veterinarians have continued to participate in Asian turtle conservation
FIGURE 27-6 Live turtle market in Southeast Asia. (Photo courtesy of Cris Hagen.)
efforts focused on range country programs, ex situ captive breeding, rehabilitation of confiscated specimens, disease description, and education. Initially, much effort was focused on medical management and rehabilitation of confiscated Asian turtles, for purposes of establishing ex situ “assurance colonies”. Many species’ husbandry needs were poorly known, and most individuals were seriously ill at the time of confiscation. Attempts to maintain these specimens in captivity often failed because the turtles refused food and succumbed to parasitic and bacterial diseases.53-56 Soon, however, medical management protocols began to improve the survival rate of these specimens.53-56 Combined with natural history field studies, this work led to successful treatment, establishment of founder captive populations, and eventual successful breeding of species with historically high mortality rates, such as the Impressed Tortoise (Manouria impressa) and the Sulawesi Forest Turtle (Leucocephalon yuwonoi) (Figure 27-7).57-59 Veterinary work with these species also led to descriptions of a number of novel parasites (e.g., Myxidium hardella), viral diseases (e.g., Sulawesi tortoise adenovirus-1), and common pathologic findings.55,56,60,61 Veterinarians have also helped to establish and implement range country conservation and veterinary education programs in Southeast Asia. These efforts have included provision of clinical care, implementation of quarantine programs, and education of local veterinarians at centers such as Cuc Phuong in Vietnam and Madras Crocodile Bank in India.62,63 Recently, veterinarians played a critical role in the transport of one of the last living Yangtze Giant Softshell Turtles (Rafetus swinhoei) into a captive breeding program in China, and veterinarians continue to be involved in the nutritional, medical, and reproductive management of the last individuals of this species (Figure 27-8).64,65 Despite these efforts, the outlook for the majority of Asian turtle species is grim. Recent reassessments of these species by the IUCN demonstrate a 90% increase in the number of species listed as Critically Endangered over the past decade.12
REPTILES AFFECTED BY OIL SPILLS In the last 10 years, veterinarians have been involved in medical management of reptiles affected by several major oil
CHAPTER 27 • Conservation issues
FIGURE 27-7 The first known captive-bred hatchling of the
Sulawesi Forest Turtle (Leucocephalon yuwonoi). This hatchling is the offspring of adults salvaged from the Southeast Asian live turtle trade. (Photo courtesy Dr. Charles Innis, New England Aquarium, Boston, Mass.)
FIGURE 27-8 One of the last living Yangtze Giant Softshell
Turtles (Rafetus swinhoei). (Photo courtesy Dr. Paul P. Calle, Wildlife Conservation Society, Bronx, NY.)
spills. In 2001, a large oil spill in the Galapagos Islands led to the death of 62% of Marine Iguanas (Amblyrhynchus cristatus) on one affected island, and veterinarians subsequently became involved with the health assessment of this species (Figure 27-9).66,67 In 2010, approximately 800,000 gallons of oil were spilled into the Kalamazoo River in Michigan, and approximately 2000 reptiles and amphibians were admitted into rehabilitation.68 Also in 2010, the massive Deepwater Horizon oil spill in the Gulf of Mexico resulted in contamination of hundreds of endangered sea turtles, including Kemp’s Ridley, Loggerhead, Green (Chelonia mydas), and Hawksbill (Eretmochelys imbricata) Sea Turtles (Figure 27-10).69 Although the majority of turtles that were admitted to rehabilitation survived, the number of turtles that died entrapped in oil at sea remains unknown. The most current publicly available data from the Deepwater Horizon oil spill indicate that approximately 90% of turtles that were admitted to rehabilitation were later released.69 Clinical data obtained by veterinarians during treatment of these oiled turtles are being withheld until legal aspects of the case have been resolved.
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FIGURE 27-9 Galapagos Marine Iguana (Amblyrhynchus cristatus) during general anesthesia in the Galapagos Islands. Liver biopsies were performed as part of a post–oil spill health assessment. (Photo courtesy Dr. Mark Mitchell, University of Illinois, Urbana, Ill.)
FIGURE 27-10 A Kemp’s Ridley Sea Turtle (Lepidochelys
kempii) undergoing medical evaluation after being recovered at sea during the Deepwater Horizon oil spill in the Gulf of Mexico, 2010. (Photo courtesy Dr. Charles Innis, New England Aquarium, Boston, Mass.)
COLD-STUNNED SEA TURTLES Stranding of sea turtles during periods of cold weather (coldstunning) has been reported from several countries.70-72 In January, 2010, approximately 4500 sea turtles were stranded during a cold-stun event in Florida.73 While such events inevitably occurred throughout history and may not have represented a threat to large, healthy populations of sea turtles, these events may represent a threat to the depleted sea turtle populations of the twenty-first century. In addition to widespread sea turtle mortality from fishery interactions, nesting beach destruction, harvesting, toxin exposure, and disease, the death of hundreds of sea turtles from cold-stunning likely has a negative impact on the population. In some geographic areas, cold-stunning events involving the rarest sea turtle species, Kemp’s Ridley Sea Turtle, occur annually, often affecting hundreds of turtles and resulting in a more than 50% mortality rate.70 Over the past 20 years, veterinary protocols for the management of cold-stunned turtles
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FIGURE 27-11 A Spotted Turtle (Clemmys guttata) killed by a
vehicle on a Massachusetts road. This once common species has been recently upgraded to Endangered by the International Union for the Conservation of Nature (IUCN). (Photo courtesy Dr. Charles Innis, New England Aquarium, Boston, Mass.)
have emerged, and a relatively high survival rate has been achieved.74 Data from these events have helped to document the adverse physiologic and common pathologic findings in cold-stunned sea turtles and have provided prognostic information for the assessment of individual animals.75-81
WILDLIFE REHABILITATION Wildlife rehabilitation centers throughout the world provide care for injured reptiles. Although snakes, crocodilians, and lizards are occasionally seen, the majority of reptiles presented to wildlife rehabilitators are turtles. The number of turtles that are injured by vehicles each year globally is beyond estimation. Locally, thousands of turtles and other reptiles can be killed adjacent to a single wetland in a single year (Figure 27-11).82 Marine turtles are often injured by boats, caught in fishing gear, or affected by neurologic syndromes of unknown etiology.14,83-86 In some cases, injured and ill reptiles can be successfully treated and released to the wild. A “turtle team” has been established at one U.S. veterinary school to provide students with early exposure to clinical case management of injured native reptiles.87 In addition to providing clinical care, wildlife rehabilitation centers can play an important role in reptile conservation through documenting locality data of rare native species, investigating local disease outbreaks, hatching eggs recovered from road-killed females, and educating the public about risks to local native species. Veterinarians with expertise in wildlife rehabilitation have assisted in the development of triage guidelines and injury assessment protocols for several reptile species.88,89
FIGURE 27-12 Phallectomy for sterilization of a feral Green
Iguana (Iguana iguana) in south Florida. (Photo courtesy Dr. Douglas R. Mader, Marathon Veterinary Hospital, Marathon, Fla.)
Such introductions have been especially damaging for island environments, where native species are often unable to compete with aggressive introduced species. The introduction of the Brown Tree Snake (Boiga irregularis) to Guam and other Pacific islands has been devastating for many bird species, as well as native reptiles.90 In south Florida, Monitor Lizards, Green Iguanas, pythons, and many other reptiles have been introduced.91,92 The North American Red-eared Slider (Trachemys scripta elegans) has been introduced to many other continents.93 The impact of these species is not yet well-defined but is subject to heated debate. Veterinarians have become involved in these situations to develop sterilization strategies, provide testimony in legal and political venues, assess disease risk, and determine likelihood of range expansions (Figure 27-12).94,95 Some studies have demonstrated transmission of parasites between native and invasive reptile species.93,96 See Chapter 28, Invasive and Introduced Reptiles and Amphibians for more details.
ENVIRONMENTAL TOXICOLOGY In collaboration with toxicologists, endocrinologists, and other colleagues, veterinarians have demonstrated exposures of freeranging reptiles to heavy metals, pesticides, and other toxic chemicals. High levels of such contaminants have been found in many species, and recent data demonstrate significant correlations between contaminant concentrations, immune function, and hematologic and biochemical variables.97-99 Further research is needed to document the mechanisms for these correlations, sources of contaminants, and as yet undescribed effects.
INVASIVE SPECIES
GENERAL VETERINARY MANAGEMENT OF CAPTIVE REPTILES
Global commerce has led to the purposeful and accidental movement of reptiles to localities far from their native ranges. In some cases, these new localities provide a favorable environment for establishment of breeding populations.
Although not immediately apparent, general veterinary care for captive reptiles contributes to reptile conservation. In thousands of zoos, aquaria, and nature centers around the world, healthy captive reptiles act as ambassadors for their species.
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reptile conservation. For example, the laparoscopic-assisted oophorectomy technique that was recently used to sterilize hybrid Galapagos Tortoises for an in situ ecologic recovery project was originally developed in private practice for management of pet turtle reproductive disorders.4,102 It is clear that many of the advances in clinical management of reptiles over the past 40 years were made by private practitioners that took the time to thoroughly document their work, teach veterinary students and other veterinarians, and publish their findings.103
REFERENCES
FIGURE 27-13 An endangered Fiji Iguana (Brachylophus
fasciatus) in a captive breeding facility in the United States. (Photo courtesy San Diego Zoo Global, San Diego, Calif.)
In an increasingly urbanized world, these animals may provide the only exposure of humans to live reptiles. Such experiences can be quite profound, and their importance in fostering environmental stewardship, particularly for children, should not be discounted. On a larger scale, veterinary management of captive individuals in zoos and aquaria has been important for the establishment and maintenance of captive breeding programs for endangered species such as the Fiji Banded Iguana (Brachylophus fasciatus) (Figure 27-13).100,101
ADVERSE EFFECTS OF GOOD INTENTIONS Well-intentioned programs and well-intentioned individuals can have potential adverse effects. Veterinarians are in a strong position to prevent such problems. By providing leadership in the realms of quarantine and disease risk, veterinarians can reduce the likelihood of adverse effects. Well-intentioned individuals may not, at first, recognize that untreated waste water from an exotic turtle breeding facility could present an infectious disease risk to local native turtles. They may not realize that native snakes for a head start program should not be raised in the same facility as nonnative snakes. It is critical for veterinarians to provide information and advice in such cases.
THE ROLE OF PRIVATE VETERINARY PRACTITIONERS While often considered the realm of zoo, aquarium, or university veterinarians, reptile conservation can be greatly enhanced by private practitioners. Much of the work cited herein was conducted in part or entirely by private practitioners. It is realistic that a reptile with a previously unknown disease will be seen at any private practice on any given day. It is possible that a turtle presented to a private practice after being found on a local road is, in fact, an endangered species from a previously unknown population. It is possible that veterinary care provided by a private practitioner will allow a local reptile education program to inspire the next generation of reptile conservationists. It is possible that a new technique developed in private practice may have wider application in the realm of
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