WILDLIFE HEALTH AND THE NORTH AMERICAN MODEL OF WILDLIFE CONSERVATION.

The management of wildlife in the United States and Canada, including the monitoring and maintenance of the health of wildlife populations and the ecosystems on which they depend, are conducted under a set of principles that aim for sustainable use. This set of principles is known as the North American Model of Wildlife Conservation (the Model), and it guides wildlife management and conservation decisions in both countries. The purpose of this perspective is to highlight how wildlife health is an important part of the Model and is vital to its future. It is proposed that wildlife health and the Model support one another. First, the history and fundamental ideas of a public trust that shaped the Model are reviewed. Next, wildlife health is defined and examples are offered that highlight how the Model supports wildlife health and how health affects the Model, as well as the limitations or threats if one moves away from the Model's defining principles. Finally, controversies surrounding the Model are reviewed and a perspective on the future is offered, based in large part on the work of Aldo Leopold. Leopold's thinking about health of the land and its organisms was well ahead of its time, and the scientific underpinnings of his writings in making the case for wildlife health and the Model are recounted. As a simple addendum to Leopold's land ethic, a plea for a health ethic is called for, whereby healthy wildlife and healthy landscapes are an obligation of the Model and modern society because health "tends to preserve the integrity, stability and beauty of the biotic community."41.

Hydrologic and vegetative removal of Cryptosporidium parvum, Giardia lamblia, and Toxoplasma gondii Surrogate microspheres in coastal wetlands.

Constructed wetland systems are used to reduce pollutants and pathogens in wastewater effluent, but comparatively little is known about pathogen transport through natural wetland habitats. Fecal protozoans, including Cryptosporidium parvum, Giardia lamblia, and Toxoplasma gondii, are waterborne pathogens of humans and animals, which are carried by surface waters from land-based sources into coastal waters. This study evaluated key factors of coastal wetlands for the reduction of protozoal parasites in surface waters using settling column and recirculating mesocosm tank experiments. Settling column experiments evaluated the effects of salinity, temperature, and water type ("pure" versus "environmental") on the vertical settling velocities of C. parvum, G. lamblia, and T. gondii surrogates, with salinity and water type found to significantly affect settling of the parasites. The mesocosm tank experiments evaluated the effects of salinity, flow rate, and vegetation parameters on parasite and surrogate counts, with increased salinity and the presence of vegetation found to be significant factors for removal of parasites in a unidirectional transport wetland system. Overall, this study highlights the importance of water type, salinity, and vegetation parameters for pathogen transport within wetland systems, with implications for wetland management, restoration efforts, and coastal water quality.

Self-mating in the definitive host potentiates clonal outbreaks of the apicomplexan parasites Sarcocystis neurona and Toxoplasma gondii.

Tissue-encysting coccidia, including Toxoplasma gondii and Sarcocystis neurona, are heterogamous parasites with sexual and asexual life stages in definitive and intermediate hosts, respectively. During its sexual life stage, T. gondii reproduces either by genetic out-crossing or via clonal amplification of a single strain through self-mating. Out-crossing has been experimentally verified as a potent mechanism capable of producing offspring possessing a range of adaptive and virulence potentials. In contrast, selfing and other life history traits, such as asexual expansion of tissue-cysts by oral transmission among intermediate hosts, have been proposed to explain the genetic basis for the clonal population structure of T. gondii. In this study, we investigated the contributing roles self-mating and sexual recombination play in nature to maintain clonal population structures and produce or expand parasite clones capable of causing disease epidemics for two tissue encysting parasites. We applied high-resolution genotyping against strains isolated from a T. gondii waterborne outbreak that caused symptomatic disease in 155 immune-competent people in Brazil and a S. neurona outbreak that resulted in a mass mortality event in Southern sea otters. In both cases, a single, genetically distinct clone was found infecting outbreak-exposed individuals. Furthermore, the T. gondii outbreak clone was one of several apparently recombinant progeny recovered from the local environment. Since oocysts or sporocysts were the infectious form implicated in each outbreak, the expansion of the epidemic clone can be explained by self-mating. The results also show that out-crossing preceded selfing to produce the virulent T. gondii clone. For the tissue encysting coccidia, self-mating exists as a key adaptation potentiating the epidemic expansion and transmission of newly emerged parasite clones that can profoundly shape parasite population genetic structures or cause devastating disease outbreaks.

Genotypic characterization of Streptococcus infantarius subsp. coli isolates from sea otters with infective endocarditis and/or septicemia and from environmental mussel samples.

Pulsed-field gel electrophoresis (PFGE) was used to type 128 Streptococcus infantarius subsp. coli isolates from sea otters and mussels. Six SmaI PFGE groups were detected, with one predominant group representing 57% of the isolates collected over a wide geographic region. Several sea otter and mussel isolates were highly related, suggesting that an environmental infection source is possible.

Prevalence, environmental loading, and molecular characterization of Cryptosporidium and Giardia isolates from domestic and wild animals along the Central California Coast.

The risk of disease transmission from waterborne protozoa is often dependent on the origin (e.g., domestic animals versus wildlife), overall parasite load in contaminated waterways, and parasite genotype, with infections being linked to runoff or direct deposition of domestic animal and wildlife feces. Fecal samples collected from domestic animals and wildlife along the central California coast were screened to (i) compare the prevalence and associated risk factors for fecal shedding of Cryptosporidium and Giardia species parasites, (ii) evaluate the relative importance of animal host groups that contribute to pathogen loading in coastal ecosystems, and (iii) characterize zoonotic and host-specific genotypes. Overall, 6% of fecal samples tested during 2007 to 2010 were positive for Cryptosporidium oocysts and 15% were positive for Giardia cysts. Animal host group and age class were significantly associated with detection of Cryptosporidium and Giardia parasites in animal feces. Fecal loading analysis revealed that infected beef cattle potentially contribute the greatest parasite load relative to other host groups, followed by wild canids. Beef cattle, however, shed host-specific, minimally zoonotic Cryptosporidium and Giardia duodenalis genotypes, whereas wild canids shed potentially zoonotic genotypes, including G. duodenalis assemblages A and B. Given that the parasite genotypes detected in cattle were not zoonotic, the public health risk posed by protozoan parasite shedding in cattle feces may be lower than that posed by other animals, such as wild canids, that routinely shed zoonotic genotypes.

Longitudinal Poisson regression to evaluate the epidemiology of Cryptosporidium, Giardia, and fecal indicator bacteria in coastal California wetlands.

Fecal pathogen contamination of watersheds worldwide is increasingly recognized, and natural wetlands may have an important role in mitigating fecal pathogen pollution flowing downstream. Given that waterborne protozoa, such as Cryptosporidium and Giardia, are transported within surface waters, this study evaluated associations between fecal protozoa and various wetland-specific and environmental risk factors. This study focused on three distinct coastal California wetlands: (i) a tidally influenced slough bordered by urban and agricultural areas, (ii) a seasonal wetland adjacent to a dairy, and (iii) a constructed wetland that receives agricultural runoff. Wetland type, seasonality, rainfall, and various water quality parameters were evaluated using longitudinal Poisson regression to model effects on concentrations of protozoa and indicator bacteria (Escherichia coli and total coliform). Among wetland types, the dairy wetland exhibited the highest protozoal and bacterial concentrations, and despite significant reductions in microbe concentrations, the wetland could still be seen to influence water quality in the downstream tidal wetland. Additionally, recent rainfall events were associated with higher protozoal and bacterial counts in wetland water samples across all wetland types. Notably, detection of E. coli concentrations greater than a 400 most probable number (MPN) per 100 ml was associated with higher Cryptosporidium oocyst and Giardia cyst concentrations. These findings show that natural wetlands draining agricultural and livestock operation runoff into human-utilized waterways should be considered potential sources of pathogens and that wetlands can be instrumental in reducing pathogen loads to downstream waters.

Prey choice and habitat use drive sea otter pathogen exposure in a resource-limited coastal system.

The processes promoting disease in wild animal populations are highly complex, yet identifying these processes is critically important for conservation when disease is limiting a population. By combining field studies with epidemiologic tools, we evaluated the relationship between key factors impeding southern sea otter (Enhydra lutris nereis) population growth: disease and resource limitation. This threatened population has struggled to recover despite protection, so we followed radio-tagged sea otters and evaluated infection with 2 disease-causing protozoal pathogens, Toxoplasma gondii and Sarcocystis neurona, to reveal risks that increased the likelihood of pathogen exposure. We identified patterns of pathogen infection that are linked to individual animal behavior, prey choice, and habitat use. We detected a high-risk spatial cluster of S. neurona infections in otters with home ranges in southern Monterey Bay and a coastal segment near San Simeon and Cambria where otters had high levels of infection with T. gondii. We found that otters feeding on abalone, which is the preferred prey in a resource-abundant marine ecosystem, had a very low risk of infection with either pathogen, whereas otters consuming small marine snails were more likely to be infected with T. gondii. Individual dietary specialization in sea otters is an adaptive mechanism for coping with limited food resources along central coastal California. High levels of infection with protozoal pathogens may be an adverse consequence of dietary specialization in this threatened species, with both depleted resources and disease working synergistically to limit recovery.

Hospice in a zoologic medicine setting.

Forty years ago, Dr. Elizabeth Kubler-Ross in her landmark book On death and dying observed "maybe at the end of our days, when we have worked and given, enjoyed ourselves and suffered, we are going back to the stage that we started out with and the circle of life is closed." Just as human life expectancy has steadily increased over the last 4 or 5 decades, animal life expectancy has increased, including that of zoologic species. With this has come a need for humans to openly and frankly deal with end-of-life issues for themselves and for their animals, including those in zoos. By necessity, zoos have been dealing with problems such as aggressive pain management and triage, and efforts to incorporate end-of-life care into zoologic medicine. But these efforts have yet to include formal acknowledgment that they are a basic form of hospice. Hospice for humans, and now for companion animals, includes much more than pain relief and geriatric care. This article reviews the concepts and basic practices of hospice and the closely related field of palliative care, their relatively recent application to companion animal care, potential applications to zoologic medicine, and the ways this could provide opportunities for personal growth of zoo visitors and staff, including veterinary staff.

Complication associated with abdominal surgical implantation of a radio transmitter in an American badger (Taxidea taxus).

Radio telemetry has greatly advanced the understanding of wild animal ecology. Telemetry studies must ensure that placement of transmitters does not influence the health and behavior of study animals. Here, 10 American badgers (Taxidea taxus) were implanted with beeswax-coated abdominal radio transmitters under general anesthesia and tracked for an average of 14 mo. Behavior and movements of all badgers indicated successful short-term recovery from implantation; however, three mortalities were observed between 5 mo and 15 mo after capture. Cause of death could not be determined for two badgers due to decomposition of the carcasses. A third badger that was recovered in good postmortem condition died from sepsis secondary to a transmitter-related omental torsion. This study indicates that there is some risk associated with abdominally implanted radio transmitters in badgers. Future studies involving implanted transmitters in mammals should focus on identifying safe and effective telemetry devices that do not affect the health of study animals. American badger, omental adhesion, peritoneal implant, telemetry, Taxidea taxus.

Canine distemper vaccination is a safe and useful preventive procedure for southern sea otters (Enhydra lutra nereis).

From 2002 to 2006, eight captive southern sea otters (Enhydra lutris nereis) at research and display institutions in California at risk of exposure to potentially lethal morbiliviruses were vaccinated with a commercial recombinant poxvirus vectored canine distemper (CD) vaccine. Serum-neutralizing (SN) antibody responses were followed for several years. The goal of this study was to determine whether 1) CD vaccination was a safe preventive medicine procedure for this species; 2) sea otters produce detectable SN antibodies in response to vaccination with this product; and 3) if this type of vaccination might be useful in response to a morbilivirus disease outbreak in free-ranging sea otters. Results indicate that a commercial recombinant vaccine is safe, provokes a measurable SN antibody response, and that vaccination may provide some protection from infection for free-ranging sea otters. It also resulted in the reevaluation of CD serology data that were previously published for free-ranging sea otters. Canine distemper, Enhydra lutris nereis, morbilivirus, sea otter, serology, vaccination.

Sea otters in a dirty ocean.

The connection between the health of humans, animals, and the environments in which they live have been well recognized and have recently been referred to as one health, one medicine. An example of the interconnectedness of human, animal, and ecosystem health is provided by the situation facing southern sea otters off the US Pacific coast.

Evaluation of cardiac lesions and risk factors associated with myocarditis and dilated cardiomyopathy in southern sea otters (Enhydra lutris nereis).

OBJECTIVE: To describe cardiac lesions and identify risk factors associated with myocarditis and dilated cardiomyopathy (DCM) in beach-cast southern sea otters. ANIMALS: Free-ranging southern sea otters. PROCEDURE: Sea otters were necropsied at the Marine Wildlife Veterinary Care and Research Center from 1998 through 2001. Microscopic and gross necropsy findings were used to classify sea otters as myocarditis or DCM case otters or control otters. Univariate, multivariate, and spatial analytical techniques were used to evaluate associations among myocarditis; DCM; common sea otter pathogens; and potential infectious, toxic, and nutritional causes. RESULTS: Clusters of sea otters with myocarditis and DCM were identified in the southern aspect of the sea otter range from May to November 2000. Risk factors for myocarditis included age, good body condition, and exposure to domoic acid and Sarcocystis neurona. Myocarditis associated with domoic acid occurred predominantly in the southern part of the range, whereas myocarditis associated with S. neurona occurred in the northern part of the range. Age and suspected previous exposure to domoic acid were identified as major risk factors for DCM. A sample of otters with DCM had significantly lower concentrations of myocardial L-carnitine than control and myocarditis case otters. CONCLUSIONS AND CLINICAL RELEVANCE: Cardiac disease is an important cause of death in southern sea otters. Domoic acid toxicosis and infection with S. neurona are likely to be 2 important causes of myocarditis in sea otters. Domoic acid-induced myocarditis appears to progress to DCM, and depletion of myocardial L-carnitine may play a key role in this pathogenesis.

Measurement of serum immunoglobulin concentration in killer whales and sea otters by radial immunodiffusion.

Killer whales and sea otters maintained in captivity are the subjects of routine health monitoring programs, and interest in immunologic studies in sea otters has been rising recently in response to potential impacts from infectious disease and environmental pollution on the threatened southern sea otter population. Development of species-specific reagents for immunologic studies in these two marine mammals is currently in its infancy. In this study, killer whale and sea otter immunoglobulin-specific polyclonal antibodies were generated, and used to develop tests for serum Ig concentration in the killer whale (Orcinus orca) and the southern (Enhydra lutris nereis) and northern sea otter (Enhydra lutris lutris). Killer whale serum IgG was purified using caprylic acid/ammonium sulfate precipitation. Sea otter plasma IgG was purified using protein-A-agarose. Polyclonal anti-Ig antisera were produced in rabbits, and specificity confirmed by immunoelectrophoresis. Radial immunodiffusion was used to measure Ig concentration in serum or plasma samples derived from 21 captive killer whales, 18 wild and 4 captive southern sea otters and 15 wild and 4 captive northern sea otters grouped by age. Mean killer whale serum Ig concentration (+/-95% confidence interval) ranged from 15.04 +/- 3.97 g/l for animals aged 0-5 years to 26.65 +/- 9.8 g/l for animals aged >10 years. Mean sea otter serum Ig concentration (+/-95% confidence interval) ranged from 28.39 +/- 11.00 g/l for southern sub-adults to 32.76 +/- 11.58 g/l for southern adults. No significant difference in serum Ig concentration was found between southern and northern sea otters. Serum Ig concentrations in two northern sea otter pups were low compared to those of adult sea otters. The two serum Ig quantitation assays produced were highly specific and reproducible and will be useful additions to the limited number of tests available for immune function in these marine mammal species.

Opportunistic research and sampling combined with fisheries and wildlife management actions or crisis response.

Currently most of the activities of state, federal, first nation, and private conservation agencies, including management of and field research on free-ranging wildlife, are not regulated under the Animal Welfare Act (AWA) and thus not subject to National Institutes of Health guidelines or routine institutional animal care and use committee (IACUC) review. However, every day thousands of fish and wildlife management activities occur across North America that provide an opportunity to take observations, measurements, biological specimens, or samples that may have research value. Most of these opportunities are secondary to ongoing and often mandated wildlife management or conservation actions. Strange as it may seem to the academic and research community, the full research potentials of these opportunities are rarely utilized. IACUCs and research institutions should strive to facilitate such research, which by its very nature is often more opportunistic than designed. They can do this by ensuring that their policies do not unnecessarily impede the rapid research responses needed, or over burden researchers with inappropriate reporting requirements designed for laboratory research. The most prominent reasons for failures to utilize wildlife research opportunities include lack of the following: personnel and expertise to collect and use the information; preparation for inevitable (or predictable) events (e.g., oil spills); resources to preserve and curate specimens; a mandate to conduct research; and recognition of the value in data or sample collection. IACUC support of open protocols and generic sampling plans can go a long way toward improving the development of useful knowledge from animals that will otherwise be lost. Opportunities to sample wildlife are categorized generally as dead sampling (road kill surveys, harvest sampling, lethal collection, and "die-offs"); live sampling (handling for marking, relocation or restocking; and captures for field or biological studies); and crisis response (e.g., population salvage operations or oil spills). Examples of the many unique situations in each category serve to illustrate how valuable research and sampling can be accomplished opportunistically. Several unique limitations of sample collection situation are described. It is recommended that IACUCs have mechanisms in place to facilitate good research in all of these circumstances.

Molecular and antigenic characterization of Bordetella bronchiseptica isolated from a wild southern sea otter (Enhydra lutris nereis) with severe suppurative bronchopneumonia.

Bordetella bronchiseptica was isolated in pure culture from the lung, abdomen, and intestine of a wild free-ranging southern sea otter (Enhydra lutris nereis) with severe, suppurative bronchopneumonia. Immunohistochemistry, using antiserum raised to B. bronchiseptica, revealed strong positive staining of bacteria attached to bronchial ciliated epithelia as well as scattered positive staining in affected alveoli. Western blot analysis demonstrated that virulence factors, filamentous hemagglutinin, pertactin, and adenylate cyclase toxin are produced by the sea otter B. bronchiseptica isolate. Ribotype analysis using Pvu II restriction digests indicated that this isolate is most similar to strains commonly obtained in domestic dogs and cats.

Profiles of polychlorinated biphenyl congeners, organochlorine pesticides, and butyltins in southern sea otters and their prey.

Concentrations of organochlorine pesticides, polychlorinated biphenyl (PCB) congeners, and butyltins were measured in sea otters and selected prey species (invertebrates) collected from the California (USA) coast. Polychlorinated biphenyls, DDTs (sum of p,p'-dichlorodiphenyldichloroethylene [p,p'-DDE], p,p'-dichlorodiphenyldichloroethane [p,p'-DDD], and p,p'-DDT), and butyltins were the major contaminants found in sea otters and their prey. Lipid-normalized concentrations of PCBs and DDT in sea otter livers were 60- and 240-fold greater than those found in the prey. Great biomagnification of PCBs and DDT in sea otters is suggested to result from their high per-capita intake of diet compared with those of other marine mammals. Profiles of PCB congeners in sea otters and prey species suggest a great capacity of sea otters to biotransform lower-chlorinated congeners. Sea otters seem to possess a greater ability than cetaceans to metabolize PCBs. The 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents of non- and mono-ortho PCBs in sea otters and certain prey species were at or above the theoretical threshold for toxic effects.

Fat soluble vitamins in blood and tissues of free-ranging and captive rhinoceros.

Several disease syndromes in captive rhinoceroses have been linked to low vitamin status. Blood samples from captive and free-ranging black (Diceros bicornis) and white rhinoceros (Ceratotherium simum) and tissue samples of captive individuals from four rhinoceros species were analysed for vitamins A and E. Circulating vitamin A levels measured as retinol for free-ranging versus captive black and white rhinoceros were 0.04 (+/- 0.03 SD) vs. 0.08 (+/- 0.08) and 0.07 (+/- 0.04) vs. 0.06 (+/- 0.02) microgram/ml, respectively. Circulating vitamin E levels measured as alpha-tocopherol were 0.58 (+/- 0.30) vs. 0.84 (+/- 0.96) and 0.62 (+/- 0.48) vs. 0.77 (+/- 0.32) microgram/ml, respectively. In contrast to earlier findings, there was no significant difference in vitamin E concentration between captive and free-ranging black rhinoceros. When the samples of captive black rhinoceros were grouped into those taken before 1990 and after 1990, however, those collected before 1990 had significantly lower (P < 0.001) vitamin E levels (0.46 +/- 0.83 microgram/ml) and those collected in 1990 or later significantly higher (P < 0.001) vitamin E levels (1.03 +/- 1.04 micrograms/ml) than the captive population as a whole. This is probably due to increased dietary supplementation. There were significant differences in circulating vitamin concentrations in black rhinoceroses from different regions in the wild. Serum 25-hydroxy (OH) vitamin D3 averaged 55.7 ng/ml in free-ranging rhinoceroses; no carotenoids were detected in any blood samples. Captive black and white rhinoceroses appear to be adequately supplemented in vitamin A and E. Captive Indian rhinoceroses (Rhinoceros unicornis) had significantly lower vitamin A concentrations in blood (P < 0.001) and higher vitamin A concentrations in liver tissue samples (P < 0.001) than other rhinoceros species. Equine requirements are not recommended as a model for rhinoceros vitamin requirements.

Clinical pathology and assessment of pathogen exposure in southern and Alaskan sea otters.

The southern sea otter (Enhydra lutris nereis) population in California (USA) and the Alaskan sea otter (E. lutris kenyoni) population in the Aleutian Islands (USA) chain have recently declined. In order to evaluate disease as a contributing factor to the declines, health assessments of these two sea otter populations were conducted by evaluating hematologic and/or serum biochemical values and exposure to six marine and terrestrial pathogens using blood collected during ongoing studies from 1995 through 2000. Samples from 72 free-ranging Alaskan, 78 free-ranging southern, and (for pathogen exposure only) 41 debilitated southern sea otters in rehabilitation facilities were evaluated and compared to investigate regional differences. Serum chemistry and hematology values did not indicate a specific disease process as a cause for the declines. Statistically significant differences were found between free-ranging adult southern and Alaskan population mean serum levels of creatinine kinase, alkaline phosphatase, alanine aminotransferase, aspartate aminotransferase, calcium, cholesterol, creatinine, glucose, phosphorous, total bilirubin, blood urea nitrogen, and sodium. These were likely due to varying parasite loads, contaminant exposures, and physiologic or nutrition statuses. No free-ranging sea otters had signs of disease at capture, and prevalences of exposure to calicivirus, Brucella spp., and Leptospira spp. were low. The high prevalence (35%) of antibodies to Toxoplasma gondii in free-ranging southern sea otters, lack of antibodies to this parasite in Alaskan sea otters, and the pathogen's propensity to cause mortality in southern sea otters suggests that this parasite may be important to sea otter population dynamics in California but not in Alaska. The evidence for exposure to pathogens of public health importance (e.g., Leptospira spp., T. gondii) in the southern sea otter population, and the naïveté of both populations to other pathogens (e.g., morbillivirus and Coccidiodes immitis) may have important implications for their management and recovery.