• A comparison of walking rates Between wild and zoo African elephants

      Miller, Lance J.; Chase, Michael J.; Hacker, Charlotte E. (2016)
      The goal of the current study was to compare the walking rates of elephants in the wild versus elephants in zoos to determine if elephants are walking similar distances relative to their wild counterparts. Eleven wild elephants throughout different habitats and locations in Botswana were compared to 8 elephants at the San Diego Zoo Safari Park. Direct comparisons revealed no significant difference in average walking rates of zoo elephants when compared with wild elephants….
    • Clinical challenge. Renal adenocarcinoma in a spitting cobra

      Belasco-Zeitz, Marianne; Pye, Geoffrey W.; Burns, Rachel E.; Pessier, Allan P. (2013)
      A 16-yr-old, male red spitting cobra (Naja pallida) (weight, 1.9 kg) presented with caudal coelomic swelling…. Blood from a male sibling (weight, 1.35 kg) was collected for comparison purposes and was reported with WBC < 5,000 × 106 cells/μl; uric acid, 6.4 mg/dl; calcium, 14.8 mg/dl; phosphorous, 6.6 mg/dl; total protein, 6.9 g/dl; and globulins, 4.2 g/dl…
    • Conservation genomics of threatened animal species

      Steiner, Cynthia C.; Putnam, Andrea S.; Hoeck, Paquita E. A.; Ryder, Oliver A. (2013)
      The genomics era has opened up exciting possibilities in the field of conservation biology by enabling genomic analyses of threatened species that previously were limited to model organisms. Next-generation sequencing (NGS) and the collection of genome-wide data allow for more robust studies of the demographic history of populations and adaptive variation associated with fitness and local adaptation.…
    • Detection of neopterin in the urine of captive and wild platyrrhines

      Sacco, Alexandra J.; Mayhew, Jessica A.; Watsa, Mrinalini; Erkenswick, Gideon; Binder, April K. (Springer Science and Business Media LLC, 2020)
      Background: Non-invasive biomarkers can facilitate health assessments in wild primate populations by reducing the need for direct access to animals. Neopterin is a biomarker that is a product of the cell-mediated immune response, with high levels being indicative of poor survival expectations in some cases. The measurement of urinary neopterin concentration (UNC) has been validated as a method for monitoring cell-mediated immune system activation in multiple catarrhine species, but to date there is no study testing its utility in the urine of platyrrhine species. In this study, we collected urine samples across three platyrrhine families including small captive populations of Leontopithecus rosalia and Pithecia pithecia, and larger wild populations of Leontocebus weddelli, Saguinus imperator, Alouatta seniculus, and Plecturocebus toppini, to evaluate a commercial enzyme-linked immunosorbent assay (ELISA) for the measurement of urinary neopterin in platyrrhines. Results: Our results revealed measured UNC fell within the sensitivity range of the assay in all urine samples collected from captive and wild platyrrhine study species via commercial ELISA, and results from several dilutions met expectations. We found significant differences in the mean UNC across all study species. Most notably, we observed higher UNC in the wild population of L. weddelli which is known to have two filarial nematode infections compared to S. imperator, which only have one. Conclusion: Our study confirms that neopterin is measurable via commercial ELISA in urine collected from captive and wild individuals of six genera of platyrrhines across three different families. These findings promote the future utility of UNC as a promising biomarker for field primatologists conducting research in Latin America to non-invasively evaluate cell-mediated immune system activation from urine. Keywords: Neopterin, Health monitoring, Platyrrhines, Immune function, Biomarker
    • Diverse captive non-human primates with phytanic acid-deficient diets rich in plant products have substantial phytanic acid levels in their red blood cells

      Moser, Ann B.; Hey, Jody; Dranchak, Patricia K.; Karaman, Mazen W.; Zhao, Junsong; Cox, Laura A.; Ryder, Oliver A.; Hacia, Joseph G. (2013)
      Background Humans and rodents with impaired phytanic acid (PA) metabolism can accumulate toxic stores of PA that have deleterious effects on multiple organ systems. Ruminants and certain fish obtain PA from the microbial degradation of dietary chlorophyll and/or through chlorophyll-derived precursors. In contrast, humans cannot derive PA from chlorophyll and instead normally obtain it only from meat, dairy, and fish products. Results Captive apes and Old world monkeys had significantly higher red blood cell (RBC) PA levels relative to humans when all subjects were fed PA-deficient diets. Given the adverse health effects resulting from PA over accumulation, we investigated the molecular evolution of thirteen PA metabolism genes in apes, Old world monkeys, and New world monkeys. All non-human primate (NHP) orthologs are predicted to encode full-length proteins with the marmoset Phyh gene containing a rare, but functional, GA splice donor dinucleotide. Acox2, Scp2, and Pecr sequences had amino acid positions with accelerated substitution rates while Amacr had significant variation in evolutionary rates in apes relative to other primates. Conclusions Unlike humans, diverse captive NHPs with PA-deficient diets rich in plant products have substantial RBC PA levels. The favored hypothesis is that NHPs can derive significant amounts of PA from the degradation of ingested chlorophyll through gut fermentation. If correct, this raises the possibility that RBC PA levels could serve as a biomarker for evaluating the digestive health of captive NHPs. Furthermore, the evolutionary rates of the several genes relevant to PA metabolism provide candidate genetic adaptations to NHP diets.
    • Duration of maternal antibodies against canine distemper virus and hendra virus in pteropid bats

      Epstein, Jonathan H.; Baker, Michelle L.; Zambrana-Torrelio, Carlos; Middleton, Deborah; Barr, Jennifer A.; DuBovi, Edward; Boyd, Victoria; Pope, Brian; Todd, Shawn; Crameri, Gary; et al. (2013)
      Old World frugivorous bats have been identified as natural hosts for emerging zoonotic viruses of significant public health concern, including henipaviruses (Nipah and Hendra virus), Ebola virus, and Marburg virus. Epidemiological studies of these viruses in bats often utilize serology to describe viral dynamics, with particular attention paid to juveniles, whose birth increases the overall susceptibility of the population to a viral outbreak once maternal immunity wanes. However, little is understood about bat immunology, including the duration of maternal antibodies in neonates. Understanding duration of maternally derived immunity is critical for characterizing viral dynamics in bat populations, which may help assess the risk of spillover to humans. We conducted two separate studies of pregnant Pteropus bat species and their offspring to measure the half-life and duration of antibodies to 1) canine distemper virus antigen in vaccinated captive Pteropus hypomelanus; and 2) Hendra virus in wild-caught, naturally infected Pteropus alecto. Both of these pteropid bat species are known reservoirs for henipaviruses. We found that in both species, antibodies were transferred from dam to pup. In P. hypomelanus pups, titers against CDV waned over a mean period of 228.6 days (95% CI: 185.4–271.8) and had a mean terminal phase half-life of 96.0 days (CI 95%: 30.7–299.7). In P. alecto pups, antibodies waned over 255.13 days (95% CI: 221.0–289.3) and had a mean terminal phase half-life of 52.24 days (CI 95%: 33.76–80.83). Each species showed a duration of transferred maternal immunity of between 7.5 and 8.5 months, which was longer than has been previously estimated. These data will allow for more accurate interpretation of age-related Henipavirus serological data collected from wild pteropid bats.
    • Efficacy of treatment and long-term follow-up of Batrachochytrium dendrobatidis PCR-positive anurans following itraconazole bath treatment

      Georoff, Timothy A.; Moore, Robert P.; Rodriguez, Carlos; Pessier, Allan P.; Newton, Alisa L.; McAloose, Denise; Calle, Paul P. (2013)
      All anuran specimens in the Wildlife Conservation Society's collections testing positive for Batrachochytrium dendrobatidis (Bd) were treated with itraconazole and then studied after treatment to assess the long-term effects of itraconazole and the drug's effectiveness in eliminating Bd carriers. Twenty-four individuals and eight colonies of 11 different species (75 total specimens) tested positive for Bd via polymerase chain reaction (PCR) on multicollection survey. All positive individuals and colonies were treated with a 0.01% itraconazole bath solution and retested for Bd via one of two PCR methodologies within 14 days of treatment completion, and all were negative for Bd. A total of 64 animals received secondary follow-up PCR testing at the time of death, 6–8 mo, or 12–15 mo post-treatment. Fourteen animals (14/64, 21.9%) were PCR positive for Bd on second follow-up. The highest percentage positive at second recheck were green-and-black poison dart frogs (Dendrobates auratus; 5/5 specimens, 100%), followed by red-eyed tree frogs (Agalychnis callidryas; 4/11, 36.4%), grey tree frogs (Hyla versicolor; 1/3, 33.3%), and green tree frogs (Hyla cinera; 3/11, 27.3%). Re-testing by PCR performed on 26/28 individuals that died during the study indicated 11/26 (42.3%) were positive (all via DNA extracted from formalin-fixed paraffin-embedded skin sections). However, there was no histologic evidence of chytridiomycosis in any of 27/28 individuals. The small number of deceased animals and effects of postmortem autolysis limited the ability to determine statistical trends in the pathology data, but none of the necropsied specimens showed evidence of itraconazole toxicity. Problems with itraconazole may be species dependent, and this report expands the list of species that can tolerate treatment. Although itraconazole is effective for clearance of most individuals infected with Bd, results of the study suggest that repeat itraconazole treatment and follow-up diagnostics may be required to ensure that subclinical infections are eliminated in amphibian collections.
    • Fat-soluble vitamin and mineral comparisons between zoo-based and free-ranging koalas (phascolarctos cinereus)

      Schmidt, Debra A.; Pye, Geoffrey W.; Hamlin-Andrus, Chris C.; Ellis, William A.; Ellersieck, Mark R.; Chen, Tai C.; Holick, Michael F. (2013)
      As part of a health investigation on koalas at San Diego Zoo, serum samples were analyzed from 18 free-ranging and 22 zoo-based koalas, Phascolarctos cinereus. Serum concentrations of calcium, chloride, cobalt, copper, iron, magnesium, manganese, molybdenum, phosphorus, potassium, selenium, sodium, zinc, and vitamins A, E, and 25(OH)D3 were quantified....
    • Foraging behavior, contaminant exposure risk, and the stress response in wild California condors (Gymnogyps californianus)

      Glucs, Zeka E.; Smith, Donald R.; Tubbs, Christopher W.; Bakker, Victoria J.; Wolstenholme, Rachel; Dudus, Kristina; Burnett, Joseph; Clark, Melissa; Clark, Michael; Finkelstein, Myra E. (2020)
      Wild California condors (Gymnogyps californianus) are frequently exposed to lead via lead-based ammunition ingestion, and recent studies indicate significant exposure to organochlorines (e.g. dichlorodiphenyldichloroethylene (DDE) and polychlorinated biphenyls (PCBs)) for condors feeding on beach-cast marine mammals. We investigated the influence of contaminant exposure on condor glucocorticoid response through comparisons between wild and captive populations and identified modifiers of glucocorticoid release….
    • Health risks from lead-based ammunition in the environment

      Bellinger, David C.; Burger, Joanna; Cade, Tom J.; Cory-Slechta, Deborah A.; Finkelstein, Myra; Hu, Howard; Kosnett, Michael; Landrigan, Philip J.; Lanphear, Bruce; Pokras, Mark A.; et al. (2013)
      ...No rational deliberation about the use of lead-based ammunition can ignore the overwhelming evidence for the toxic effects of lead, or that the discharge of lead bullets and shot into the environment poses significant risks of lead exposure to humans and wildlife. Given the availability of non-lead ammunition for shooting and hunting (Thomas 2013), the use of lead-based ammunition that introduces lead into the environment can be reduced and eventually eliminated. This seems to be a reasonable and equitable action to protect the health of humans and wildlife....
    • Hepatitis and splenitis due to systemic tetratrichomoniasis in an American white pelican (Pelecanus erythrorhynchos)

      Burns, Rachel E.; Braun, Josephine; Armién, Aníbal G.; Rideout, Bruce (2013)
      A free-ranging, young adult, female American white pelican (Pelecanus erythrorhynchos), found dead on the grounds of the San Diego Zoo Safari Park in Southern California, had severe multifocal to coalescing necrotizing hepatitis and splenitis on postmortem examination. Histologically, within the large areas of necrosis were myriad pleomorphic, 5–20 µm in diameter, protozoal organisms with 1 to multiple nuclei. Ultrastructurally, the organisms were consistent with a trichomonad flagellate. Polymerase chain reaction and sequencing of the small subunit ribosomal RNA gene identified nucleotide sequences with 99% identity to Tetratrichomonas gallinarum, which is a common inhabitant of the intestinal tract of galliform and anseriform birds that has occasionally been associated with disease, including typhlitis and hepatitis. Damage to the cecal mucosa in the pelican from trematodes and secondary bacterial infection could have allowed invasion and systemic dissemination of the organism. Exposure of the pelican to a variety of native and exotic anseriform and galliform birds at the zoological institution could have led to cross-species infection and severe manifestation of disease in a novel host.
    • Lead in ammunition: A persistent threat to health and conservation

      Johnson, C. K.; Kelly, T. R.; Rideout, Bruce (2013)
      Many scavenging bird populations have experienced abrupt declines across the globe, and intensive recovery activities have been necessary to sustain several species, including the critically endangered California condor (Gymnogyps californianus). Exposure to lead from lead-based ammunition is widespread in condors and lead toxicosis presents an immediate threat to condor recovery, accounting for the highest proportion of adult mortality….
    • Pathogenesis, diagnosis, and treatment of amphibian chytridiomycosis

      Baitchman, Eric J.; Pessier, Allan P. (2013)
      Amphibian chytridiomycosis, caused by the chytridiomycete fungus, Batrachochytrium dendrobatidis (Bd), is responsible for a global pandemic that has dramatically reduced global amphibian populations and diversity. Species declines, extirpations, and extinctions attributed to chytridiomycosis have occurred in Australia, Europe, Latin America, and the United States….
    • Proximate causes of the red face of the bald uakari monkey (Cacajao calvus)

      Mayor, P.; Mamani, J.; Montes, D.; González-Crespo, C.; Sebastián, M. A.; Bowler, Mark (2015)
      In social species, such as primates, facial appearances transmit a variety of social signals. Although it is suggested that the intense red colour of the face of the bald uakari monkey might be an indicator of health, this hypothesis still has not been verified. This study describes the histological structure of the skin of the face in the bald uakari, compared with other non-red neotropical primates, to better understand the maintenance of its colour. The facial skin of the bald uakari monkey is characterized by a thinner epidermis, absence of melanin pigments and a high density of vascular capillaries that spread below the epidermis. These vascular capillaries are larger and more tortuous than in other neotropical primates. The skin of the face of the bald uakari monkey allows a direct external assessment of haematological status, suggesting that the colour of the face would be an honest indicator of health, but could also signal sexual or behavioural states.
    • Rigorous wildlife disease surveillance

      Watsa, Mrinalini; Wildlife Disease Surveillance Focus Group; Erkenswick, G.; Prost, S.; Davis, Elizabeth Oneita; Moore, Caroline; Kubiski, Steven V.; Witte, Carmel L.; Ogden, R.; Meredith, A.; et al. (2020)
      Evidence suggests that zoonotic (animal origin) coronaviruses have caused three recent emerging infectious disease (EID) outbreaks: severe acute respiratory syndrome (SARS), Middle East respiratory syndrome (MERS), and the current coronavirus disease 2019 (COVID-19) pandemic. In the search for an intermediate host for SARS coronavirus 2 (SARS-CoV-2, which causes COVID-19), studies have identified SARS-CoV-2–like strains in bats (1) and pangolins (2), but these do not contain the same polybasic cleavage site that is present in SARS-CoV-2 (3). It is unknown what the intermediate host for this spillover event was because to date there are no international or national conventions on pathogen screening associated with animals, animal products, or their movements, and capacity for EID diagnostics is limited along much of the human-wildlife interface....
    • Seroepidemiologic survey of potential pathogens in obligate and facultative scavenging avian species in California

      Straub, Mary H.; Kelly, Terra R.; Rideout, Bruce; Eng, Curtis; Wynne, Janna; Braun, Josephine; Johnson, Christine K. (2015)
      Throughout the world, populations of scavenger birds are declining rapidly with some populations already on the brink of extinction. Much of the current research into the factors contributing to these declines has focused on exposure to drug residues, lead, and other toxins. Despite increased monitoring of these declining populations, little is known about infectious diseases affecting scavenger bird species. To assess potential infectious disease risks to both obligate and facultative scavenger bird species, we performed a serosurvey for eleven potential pathogens in three species of scavenging birds in California: the California condor (Gymnogyps californianus), turkey vulture (Cathartes aura) and golden eagle (Aquila chrysaetos). California condors were seropositive for avian adenovirus, infectious bronchitis virus, Mycoplasma gallisepticum, avian paramyxovirus-2, West Nile virus (WNV) and Toxoplasma gondii. Golden eagles were seropositive for avian adenovirus, Chlamydophila psittaci and Toxoplasma gondii, and turkey vultures were seropositive for avian adenovirus, Chlamydophila psittaci, avian paramyxovirus-1, Toxoplasma gondii and WNV. Risk factor analyses indicated that rearing site and original release location were significantly associated with a positive serologic titer to WNV among free-flying condors. This study provides preliminary baseline data on infectious disease exposure in these populations for aiding in early disease detection and provides potentially critical information for conservation of the endangered California condor as it continues to expand its range and encounter new infectious disease threats.
    • Spatiotemporal network structure among “friends of friends” reveals contagious disease process

      Witte, Carmel L.; Hungerford, Laura L.; Rideout, Bruce; Papendick, Rebecca; Fowler, James H. (2020)
      Disease transmission can be identified in a social network from the structural patterns of contact. However, it is difficult to separate contagious processes from those driven by homophily, and multiple pathways of transmission or inexact information on the timing of infection can obscure the detection of true transmission events. Here, we analyze the dynamic social network of a large, and near-complete population of 16,430 zoo birds tracked daily over 22 years to test a novel “friends-of-friends” strategy for detecting contagion in a social network. The results show that cases of avian mycobacteriosis were significantly clustered among pairs of birds that had been in direct contact. However, since these clusters might result due to correlated traits or a shared environment, we also analyzed pairs of birds that had never been in direct contact but were indirectly connected in the network via other birds. The disease was also significantly clustered among these friends of friends and a reverse-time placebo test shows that homophily could not be causing the clustering. These results provide empirical evidence that at least some avian mycobacteriosis infections are transmitted between birds, and provide new methods for detecting contagious processes in large-scale global network structures with indirect contacts, even when transmission pathways, timing of cases, or etiologic agents are unknown.
    • Survey of Plasmodium spp. in free-ranging neotropical primates from the Brazilian Amazon region impacted by anthropogenic actions

      Bueno, Marina G.; Rohe, Fabio; Kirchgatter, Karin; Di Santi, Silvia M. F.; Guimarães, Lilian O.; Witte, Carmel L.; Costa-Nascimento, Maria J.; Toniolo, Christina R. C.; Catão-Dias, José Luiz (2013)
      This study investigated Plasmodium spp. infection in free-ranging neotropical primates from Brazilian Amazon regions under the impact of major anthropogenic actions. Blood samples from 19 new world primates were collected and analyzed with microscopic and molecular procedures. The prevalence of Plasmodium infection was 21.0% (4/19) and PCR positive samples were identified as P. brasilianum. Considering the social-economic changes that the Amazon is facing, the prevalence of P. brasilianum infection highlights the necessity to closely monitor the movement of both human and non-human primate populations, in order to mitigate pathogen exposure and the introduction of new agents into previously naïve areas.
    • Tumoral calcinosis form of hydroxyapatite deposition disease in related red-bellied short-necked turtles, Emydura subglobosa

      Burns, Rachel E.; Bicknese, Elizabeth; Westropp, J. L.; Shiraki, R.; Stalis, Ilse H. (2013)
      Ten of 12 red-bellied short-necked turtles from a single clutch presented at 9 months of age with multiple white to tan nodules on their feet. Histologically, the nodules were composed of large periarticular deposits of mineralized crystalline material that extended into the joint spaces of interphalangeal joints and was surrounded by granulomatous inflammation and fibrosis. Crystallographic analysis determined the material to be apatite (calcium phosphate hydroxide) consistent with the tumoral calcinosis form of hydroxyapatite deposition disease (HADD). HADD has previously been described in aquatic turtles and rarely lizards and must be differentiated from gout in reptiles. A cause for the tumoral calcinosis lesions in these turtles could not be determined; however, based on previous reports in this species, a species-specific predilection, in conjunction with unknown environmental factors, is suspected. The use of the terms HADD, pseudogout (calcium pyrophosphate crystal deposition disease), and calcinosiscircumscripta has been inconsistent, creating confusion in the literature.