Article

A SURVEY OF DISEASES IN CAPTIVE RED WOLVES ( CANIS RUFUS ), 1997–2012

Authors:
  • Point Defiance Zoo & Aquarium
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Abstract

Conservation efforts to preserve the red wolf ( Canis rufus ) have been in progress since the 1970s through the U.S. Fish and Wildlife Service Red Wolf Recovery Program and the Association of Zoos and Aquarium's Red Wolf Species Survival Plan. An ongoing part of this project has been to monitor mortality trends, particularly to look for potential genetic conditions resulting from inbreeding given the small founding population of only 14 individuals. An initial survey was conducted in the 1990s but a comprehensive assessment of the population has not been done since then. This retrospective review evaluates mortality in the population from 1997 to 2012 through analysis of gross necropsy and histology records provided by cooperating institutions that housed red wolves during the time period of interest. Of the 378 red wolves that died during this 15-yr period, 259 animals had gross necropsy records, histology records, or both that were evaluated. The major causes of neonatal death were parental trauma, stillbirth, or pneumonia. Overall, juveniles had very low mortality rates with only 12 wolves aged 30 days to 6 mo dying during the study period. The most common cause of death within the adult populations was neoplasia, with epithelial neoplasms, carcinomas, and adenocarcinomas being the most common types reported. Gastrointestinal disease was the second most common cause of death, particularly gastric dilation and volvulus, inflammatory bowel disease, and gastrointestinal perforations. These findings are in stark contrast to causes of mortality in the wild population, which are primarily due to human-related activities such as vehicular trauma, gunshot, or poisoning. Overall, the captive population has few health problems, but an increase in inflammatory bowel disease in particular warrants further investigation.

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... Among the diseases affecting wild animals, birth defects are not commonly observed, and there are only a few reports of congenital abnormalities occurring in wild canids (8,20,22,24,30). Diaphragmatic hernias are disruptions of the diaphragm that result in the misplacement of abdominal viscera within the thoracic cavity, and they may be acquired or congenital (2). ...
... Birth defects in wild canids are rare and usually associated to ocular (8), cardiac (22,24) or musculoskeletal abnormalities (20,22,30). There are only a few reports of hernias in wild carnivores and they are restricted to wild felids (12,14) and a maned wolf (10). ...
... Birth defects in wild canids are rare and usually associated to ocular (8), cardiac (22,24) or musculoskeletal abnormalities (20,22,30). There are only a few reports of hernias in wild carnivores and they are restricted to wild felids (12,14) and a maned wolf (10). ...
Article
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An approximately 3-month-old crab-eating fox (Cerdocyon thous) was found by environmental authorities in the State of Paraiba, Northeastern Brazil and referred to a wildlife care center. The fox was presenting respiratory distress and it was referred to the Veterinary Hospital of the Federal University of Paraiba (UFPB) for ancillary testing. Abdominal and thoracic ultrasound and radiographies were performed. These imaging tests indicated the fox had a possible diaphragmatic hernia and ectopic kidney. The imageology results were confirmed on necropsy, which revealed a postero-lateral focal discontinuity of the dorsal aspect of the diaphragmatic muscle with protrusion of the gastrointestinal tract into the thoracic cavity. The stomach and intestinal loops were filled with gas and obliterated the visualization of the heart and lungs. Additionally, only the right kidney was found, and no vestigial left kidney was identified. Congenital diaphragmatic hernias are not commonly observed in wildlife but should be considered as a potential differential diagnosis for acute onset of respiratory distress in young carnivores.
... 10 Prior studies have identified disease exposure and mortality in both captive and free-ranging red wolves. 2,9 A survey of mortality in captive red wolves examined postmortem between 1997 and 2012 identified neoplasia and gastrointestinal disease as the most common causes of death in adult animals. 9 Infectious disease (primarily bacterial pathogens) contributed to 9% of adult mortality. ...
... 2,9 A survey of mortality in captive red wolves examined postmortem between 1997 and 2012 identified neoplasia and gastrointestinal disease as the most common causes of death in adult animals. 9 Infectious disease (primarily bacterial pathogens) contributed to 9% of adult mortality. 9 A recent analysis of infectious diseases affecting free-ranging red wolves identified exposure to ectoparasites (ticks, biting lice, mange mites), endoparasites (hookworm, heartworm), viral disease (canine distemper, canine parvovirus, rabies), and tick-borne disease (Lyme disease, ehrlichiosis, and Rocky Mountain spotted fever). 2 Prior determination that free-ranging red wolves are exposed to vector-borne organisms (VBOs) raises the question whether these pathogens affect the ex situ population. ...
... 9 Infectious disease (primarily bacterial pathogens) contributed to 9% of adult mortality. 9 A recent analysis of infectious diseases affecting free-ranging red wolves identified exposure to ectoparasites (ticks, biting lice, mange mites), endoparasites (hookworm, heartworm), viral disease (canine distemper, canine parvovirus, rabies), and tick-borne disease (Lyme disease, ehrlichiosis, and Rocky Mountain spotted fever). 2 Prior determination that free-ranging red wolves are exposed to vector-borne organisms (VBOs) raises the question whether these pathogens affect the ex situ population. The goal of this study was to assess the prevalence of selected VBOs in captive red wolves to evaluate their potential as threats to species survival and to provide a baseline that may facilitate ongoing disease monitoring and the detection of emergent threats from such VBOs. ...
Article
The red wolf (Canis rufus) is a critically endangered North American canid, with surviving conspecifics divided between a captive breeding population and a reintroduced free-ranging population. The goal of this study was to assess the prevalence of selected vector-borne pathogens in captive red wolves. Whole blood samples were collected from 35 captive red wolves. Quantitative polymerase chain reaction (PCR) assays were performed on extracted DNA to identify infection by Trypanosoma cruzi and vector-borne organisms within the following genera: Anaplasma, Babesia, Bartonella, Ehrlichia, Mycoplasma, Neoehrlichia, Neorickettsia, and Rickettsia. All red wolves sampled were PCR-negative for all tested organisms. These pathogens are unlikely to constitute threats to red wolf conservation and breeding efforts under current captive management conditions. The results of this study establish a baseline that may facilitate ongoing disease monitoring in this species.
... Unfortunately, the captive red wolf population is threatened by health issues, especially gastrointestinal (GI) disease that are not described in the wild population (Acton et al., 2000). Gastrointestinal disease is the second most common cause of mortality in the captive red wolf population (Acton et al., 2000;Seeley et al., 2016). For instance, from 1992 through 2012, 21% (32/151) of mortalities in adult red wolves were related to GI disease, with 25% (8/32) of these individuals suffering from inflammatory bowel disease (IBD) (Acton et al., 2000;Seeley et al., 2016). ...
... Gastrointestinal disease is the second most common cause of mortality in the captive red wolf population (Acton et al., 2000;Seeley et al., 2016). For instance, from 1992 through 2012, 21% (32/151) of mortalities in adult red wolves were related to GI disease, with 25% (8/32) of these individuals suffering from inflammatory bowel disease (IBD) (Acton et al., 2000;Seeley et al., 2016). An additional 25% (37/151) of wolves that died from 1992 to 2012 had non-lethal GI lesions (Acton et al., 2000;Seeley et al., 2016). ...
... For instance, from 1992 through 2012, 21% (32/151) of mortalities in adult red wolves were related to GI disease, with 25% (8/32) of these individuals suffering from inflammatory bowel disease (IBD) (Acton et al., 2000;Seeley et al., 2016). An additional 25% (37/151) of wolves that died from 1992 to 2012 had non-lethal GI lesions (Acton et al., 2000;Seeley et al., 2016). While IBD did not kill these individuals, 68% (22/37) possessed lesions similar to IBD (Acton et al., 2000;Seeley et al., 2016). ...
Article
Full-text available
Captive management of many wildlife species can be challenging, with individuals displaying health disorders that are not generally described in the wild population. Retrospective studies have identified gastrointestinal (GI) diseases, in particular inflammatory bowel disease (IBD), as the second leading cause of captive adult red wolf (Canis rufus) mortality. Recent molecular studies show that imbalanced gut microbial composition is tightly linked to IBD in the domestic dog. The goal of the present study was to address two main questions: (1) how do red wolf gut microbiomes differ between animals with loose stool consistency, indicative of GI issues, and those with normal stool consistency and (2) how does dietary type relate to stool consistency and red wolf gut microbiomes? Fresh fecal samples were collected from 48 captive wolves housed in eight facilities in the United States and from two wild wolves living in Alligator River National Wildlife Refuge, NC, United States. For each individual, the stool consistency was categorized as loose or normal using a standardized protocol and their diet was categorized as either wild, whole meat, a mix of whole meat and kibble or kibble. We characterized gut microbiome structure using 16S rRNA gene amplicon sequencing. We found that red wolves with a loose stool consistency differed in composition than wolves with normal stool consistency, suggesting a link between GI health and microbiome composition. Diet was not related to stool consistency but did significantly impact gut microbiome composition; gut microbiome composition of wolves fed a kibble diet were significantly different than the gut microbiome composition of wolves fed a mixed, whole meat and wild diet. Findings from this study increase the understanding of the interplay between diet and GI health in the red wolf, a critical piece of information needed to maintain a healthy red wolf population ex situ.
... Association of Zoos and Aquariums and related facilities, the incidence of CEH or endometrial hyperplasia was 75% and the incidence of pyometra was 11.1%. Results of a 2009 retrospective mortality review 4 indicate that 2 of 64 (3.1%) red wolves died of pyometra over a 4-year period, whereas results of a 2016 review 5 of mortality records from 1997 to 2012 indicated that 8.8% of female red wolves died of reproductive tract disease and 11.8% of female red wolves had ancillary reproductive lesions such as suppurative endometritis or CEH. Additionally, Veterinary Advisor Reports a from 2009 to 2013 identified 8 female red wolves that were treated for, died of, or were euthanized because of pyometra. ...
... Factors that contribute to that increased risk include red wolf management, limited space available for breeding, and possibly a species predilection. 2,3,5,14 As the current population of red wolves ages, an increase in the frequency of age-associated diseases such as CEH and pyometra is expected. Results of a study 15 [3] 10.73 (7.14-18.67) ...
... Results of a study 15 [3] 10.73 (7.14-18.67) [5] 8.86 (7.14-12.85) [3] 16.31 (8.57-18.67) ...
Article
OBJECTIVE To describe ultrasonographic characteristics of the reproductive tract and serum progesterone and estradiol concentrations in captive female red wolves (Canis rufus) with and without reproductive tract disease. DESIGN Prospective study. ANIMALS 13 adult female red wolves. PROCEDURES Wolves with varying parity and history of contraceptive treatment were anesthetized to facilitate ultrasonographic examination and measurement of the reproductive tract and blood collection for determination of serum progesterone and estradiol concentrations in December 2011 and June 2012. Additionally, during the December evaluation, fine-needle aspirate samples of the uterus were obtained for cytologic evaluation. Measurements were compared between wolves with and without reproductive tract disease and between wolves that had and had not received a contraceptive. RESULTS 7 of 13 wolves had or developed reproductive tract disease during the study. Ranges for measurements of reproductive tract structures overlapped between ultrasonographically normal and abnormal tracts, but measurements for abnormal tracts were generally greater than those for normal tracts. The ultrasonographic diagnosis was consistent with the histologic diagnosis for reproductive tracts obtained from wolves that were sterilized, were euthanized, or died during the study. Cytologic results for fine-needle aspirate samples of the uterus and serum progesterone and estradiol concentrations were unable to distinguish wolves with and without reproductive tract disease. Reproductive tract disease was not associated with parity or contraceptive administration. CONCLUSIONS AND CLINICAL RELEVANCE The ultrasonographic images, reproductive tract measurements, and descriptions of reproductive tract lesions provided in this study can be used as diagnostic guidelines for the treatment and management of red wolves with reproductive tract disease.
... Association of Zoos and Aquariums and related facilities, the incidence of CEH or endometrial hyperplasia was 75% and the incidence of pyometra was 11.1%. Results of a 2009 retrospective mortality review 4 indicate that 2 of 64 (3.1%) red wolves died of pyometra over a 4-year period, whereas results of a 2016 review 5 of mortality records from 1997 to 2012 indicated that 8.8% of female red wolves died of reproductive tract disease and 11.8% of female red wolves had ancillary reproductive lesions such as suppurative endometritis or CEH. Additionally, Veterinary Advisor Reports a from 2009 to 2013 identified 8 female red wolves that were treated for, died of, or were euthanized because of pyometra. ...
... Factors that contribute to that increased risk include red wolf management, limited space available for breeding, and possibly a species predilection. 2,3,5,14 As the current population of red wolves ages, an increase in the frequency of age-associated diseases such as CEH and pyometra is expected. Results of a study 15 [3] 10.73 (7.14-18.67) ...
... Results of a study 15 [3] 10.73 (7.14-18.67) [5] 8.86 (7.14-12.85) [3] 16.31 (8.57-18.67) ...
Article
OBJECTIVE To describe ultrasonographic characteristics of the reproductive tract and serum progesterone and estradiol concentrations in captive female red wolves (Canis rufus) with and without reproductive tract disease. DESIGN Prospective study. ANIMALS 13 adult female red wolves. PROCEDURES Wolves with varying parity and history of contraceptive treatment were anesthetized to facilitate ultrasonographic examination and measurement of the reproductive tract and blood collection for determination of serum progesterone and estradiol concentrations in December 2011 and June 2012. Additionally, during the December evaluation, fine-needle aspirate samples of the uterus were obtained for cytologic evaluation. Measurements were compared between wolves with and without reproductive tract disease and between wolves that had and had not received a contraceptive. RESULTS 7 of 13 wolves had or developed reproductive tract disease during the study. Ranges for measurements of reproductive tract structures overlapped between ultrasonographically normal and abnormal tracts, but measurements for abnormal tracts were generally greater than those for normal tracts. The ultrasonographic diagnosis was consistent with the histologic diagnosis for reproductive tracts obtained from wolves that were sterilized, were euthanized, or died during the study. Cytologic results for fine-needle aspirate samples of the uterus and serum progesterone and estradiol concentrations were unable to distinguish wolves with and without reproductive tract disease. Reproductive tract disease was not associated with parity or contraceptive administration. CONCLUSIONS AND CLINICAL RELEVANCE The ultrasonographic images, reproductive tract measurements, and descriptions of reproductive tract lesions provided in this study can be used as diagnostic guidelines for the treatment and management of red wolves with reproductive tract disease. ( J Am Vet Med Assoc 2018;252:343–352)
... Cystic endometrial hyperplasia (CEH) and pyometra are commonly identified in aged red wolves and African wild dogs (Acton et al., 2000;Seeley et al., 2016). Although spontaneous disease occurs, it is thought that the use of synthetic progestagin contraceptives, such as melengestrol acetate, may increase the risk for severe CEH and mineralization (Moresco and Agnew, 2013). ...
... Gastric dilatation and volvulus (GDV) has been reported a number of times in captive red wolves, in several maned wolves, and in a red panda. As in domestic dogs, conformation may be a predispositing factor (Acton et al., 2000;Seeley et al., 2016). Additionally, wolves may develop GDV immediately after a struggle associated with capture, and dietary factors have been suggested, but not conclusively proven, to predispose to GDV. ...
... However, environmental factors are also likely to be important [91]. It has even been suggested that only individuals in captivity experience immunopathology as a result of dysbiosis associated with the artificial environment (e.g., in marmosets [92], red wolves [93], and cheetahs [94]). This idea in turn suggests that a wide variety of mammals might be prone to immunopathology in certain environments, due to their own legacies of coevolution with symbionts (as outlined above). ...
Article
The mammalian immune system packs serious punch against infection but can also cause harm: for example, coronavirus disease 2019 (COVID-19) made headline news of the simultaneous power and peril of human immune responses. In principle, natural selection leads to exquisite adaptation and therefore cytokine responsiveness that optimally balances the benefits of defense against its costs (e.g., immunopathology suffered and resources expended). Here, we illustrate how evolutionary biology can predict such optima and also help to explain when/why individuals exhibit apparently maladaptive immunopathological responses. Ultimately, we argue that the evolutionary legacies of multicellularity and life-history strategy, in addition to our coevolution with symbionts and our demographic history, together explain human susceptibility to overzealous, pathology-inducing cytokine responses. Evolutionary insight thereby complements molecular/cellular mechanistic insights into immunopathology.
... Sometimes, animals in captivity exhibit abnormal behaviour such stereotypies (Vaz et al., 2017) or aggressiveness ( Salas et al., 2016) due to poor welfare, as behaviour is an animal's ''first line of defence'' in response to environmental change, i.e., what animals do to interact with, respond to, and control their environment (Mench, 1998). Moreover, in literature, the pathologies affecting captive animals have been shown to be different from the ones affecting wild populations (Seeley et al., 2016;Strong et al., 2016). ...
Article
Full-text available
Background The zoo is a unique environment in which to study animals. Zoos have a long history of research into aspects of animal biology, even if this was not the primary purpose for which they were established. The data collected from zoo animals can have a great biological relevance and it can tell us more about what these animals are like outside the captive environment. In order to ensure the health of all captive animals, it is important to perform a post-mortem examination on all the animals that die in captivity. Methods The causes of mortality of two hundred and eighty two mammals which died between 2004 and 2015 in three different Italian zoos (a Biopark, a Safari Park and a private conservation center) have been investigated. Results Post mortem findings have been evaluated reporting the cause of death, zoo type, year and animal category. The animals frequently died from infectious diseases, in particular the causes of death in ruminants were mostly related to gastro-intestinal pathologies. pulmonary diseases were also very common in each of the zoos in the study. Moreover, death was sometimes attributable to traumas, as a result of fighting between conspecifics or during mating. Cases of genetic diseases and malformations have also been registered. Discussion This research was a confirmation of how conservation, histology and pathology are all connected through individual animals. These areas of expertise are extremely important to ensure the survival of rare and endangered species and to learn more about their morphological and physiological conditions. They are also useful to control pathologies, parasites and illnesses that can have a great impact on the species in captivity. Finally, this study underlines the importance of a close collaboration between veterinarians, zoo biologists and pathologists. Necropsy findings can help conservationists to determine how to support wild animal populations.
... The etiology remains unclear in most cases and it would seem that protein-rich nutrition possibly favours the condition. Moreover, acquired infectious (such as leptospirosis) or noninfectious (such as autoimmune) diseases or congenital factors might be involved [45,89,90]. Mild bacterial or viral infections are primarily suspected of causing the inflammation. ...
Article
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... Dingo Lymphoma, thymoma, lipoma of subcutis, fibromatous epulis, perianal adenoma, sebaceous adenoma, squamous cell carcinoma, bronchial adenoma Ladds (2009) Canis mesomelas Black-backed jackal Osteoma, hemangiosarcoma Chu et al. (2012) Canis rufus Red wolf Adenocarcinoma, carcinomas Snyder and Ratcliffe (1966); Seeley et al. (2016) Capra hircus Domestic goat Lymphoma Ratcliffe (1933) Cercopithecus aethiops African green monkey Hepatoma, mixed hepatocellular and cholangiocellular carcinoma, uterine leiomyoma Porter et al. (2004); Chu et al. (2012) Cercopithecus diana Diana monkey Cholangiocarcinoma Porter et al. (2004) Cercopithecus mitis Blue monkey Biliary adenoma/cystadenoma Porter et al. (2004) ...
Chapter
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Neoplasia has been recorded in the vast majority of metazoans. The frequent occurrence of cancer in multicellular organisms suggests that neoplasia, similar to pathogens/parasites, may have a significant negative impact on host fitness in the wild. This is supported by the fact that wildlife cancers have recently been shown to result in significantly increased levels of mortality and concomitant reduction in fitness. By thorough searches of the available literature we provide a comprehensive and an updated list of cancer prevalence and etiology in the wild. We were, however, unable to find data on nontransmissible cancer prevalence in invertebrates and consequently this chapter focuses on cancer in wild vertebrates. Although single cases of cancer are frequently encountered in the wildlife, we were only able to retrieve robust data on cancer prevalence for 31 vertebrate species (12 fish, 3 amphibians, 2 reptiles, 2 birds, and 12 mammals). Cancer prevalence among these vertebrates ranged from as low as 0.2% observed in Canada geese (Branta canadensis) to more than 50% recorded in both Santa Catalina Island foxes (Urocyon littoralis catalinae) and Cape mountain zebras (Equus zebra zebra). The high prevalence recorded in some vertebrates strongly suggests that cancer in wildlife may indeed carry significant fitness costs. In spite of this, the low number of published comprehensive studies clearly shows that so far cancer in wildlife has received insufficient attention by biologists. We hope that this chapter will act as a catalyst for further studies focusing on the impact of cancer in wild animals. The chapter additionally compares cancer recorded in French zoological parks to those obtained at other zoological parks. Finally, we provide an updated list of cancer recorded as single cases in the wild, as well as in captive animals.
... Though the importance of viable ex situ populations for both maned and red wolves is becoming increasingly apparent, both species suffer health (Phillips & Scheck 1991, Gilioli & Silva 2000 and reproductive difficulties (Ginsberg 1994, Rodden et al. 1996, Rabon 2011, Johnson et al. 2014). Gastrointestinal disease is a major factor in mortalities in both red and maned wolves and has a high prevalence in both ex situ populations (Acton et al. 2000, Maia & Gouveia 2002, Stirling et al. 2008, Seeley et al. 2016. ...
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Neoplasia has been recorded in the vast majority of metazoans. The frequent occurrence of cancer in multicellular organisms suggests that neoplasia, similar to pathogens/parasites, may have a significant negative impact on host fitness in the wild. This is supported by the fact that wildlife cancers have recently been shown to result in significantly increased levels of mortality and concomitant reduction in fitness. By thorough searches of the available literature we provide a comprehensive and an updated list of cancer prevalence and etiology in the wild. We were, however, unable to find data on nontransmissible cancer prevalence in invertebrates and consequently this chapter focuses on cancer in wild vertebrates. Although single cases of cancer are frequently encountered in the wildlife, we were only able to retrieve robust data on cancer prevalence for 31 vertebrate species (12 fish, 3 amphibians, 2 reptiles, 2 birds, and 12 mammals). Cancer prevalence among these vertebrates ranged from as low as 0.2% observed in Canada geese (Branta canadensis) to more than 50% recorded in both Santa Catalina Island foxes (Urocyon littoralis catalinae) and Cape mountain zebras (Equus zebra zebra). The high prevalence recorded in some vertebrates strongly suggests that cancer in wildlife may indeed carry significant fitness costs. In spite of this, the low number of published comprehensive studies clearly shows that so far cancer in wildlife has received insufficient attention by biologists. We hope that this chapter will act as a catalyst for further studies focusing on the impact of cancer in wild animals. The chapter additionally compares cancer recorded in French zoological parks to those obtained at other zoological parks. Finally, we provide an updated list of cancer recorded as single cases in the wild, as well as in captive animals.
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