• Detailed monitoring of a small but recovering population reveals sublethal effects of disease and unexpected interactions with supplemental feeding

      Tollington, S.; Greenwood, A.; Jones, C.G.; Hoeck, Paquita; Chowrimootoo, A.; Smith, D.; Richards, H.; Tatayah, V.; Groombridge, J.J. (2015)
      Infectious diseases are widely recognized to have substantial impact on wildlife populations. These impacts are sometimes exacerbated in small endangered populations, and therefore, the success of conservation reintroductions to aid the recovery of such species can be seriously threatened by outbreaks of infectious disease. Intensive management strategies associated with conservation reintroductions can further compound these negative effects in such populations. Exploring the sublethal effects of disease outbreaks among natural populations is challenging and requires longitudinal, individual life‐history data on patterns of reproductive success and other indicators of individual fitness. Long‐term monitoring data concerning detailed reproductive information of the reintroduced Mauritius parakeet (Psittacula echo ) population collected before, during and after a disease outbreak was investigated. Deleterious effects of an outbreak of beak and feather disease virus (BFDV ) were revealed on hatch success, but these effects were remarkably short‐lived and disproportionately associated with breeding pairs which took supplemental food. Individual BFDV infection status was not predicted by any genetic, environmental or conservation management factors and was not associated with any of our measures of immune function, perhaps suggesting immunological impairment. Experimental immunostimulation using the PHA (phytohaemagglutinin assay) challenge technique did, however, provoke a significant cellular immune response. We illustrate the resilience of this bottlenecked and once critically endangered, island‐endemic species to an epidemic outbreak of BFDV and highlight the value of systematic monitoring in revealing inconspicuous but nonetheless substantial ecological interactions. Our study demonstrates that the emergence of such an infectious disease in a population ordinarily associated with increased susceptibility does not necessarily lead to deleterious impacts on population growth and that negative effects on reproductive fitness can be short‐lived.
    • Development of a case definition for clinical feline herpesvirus infection in cheetahs (acinonyx jubatus) housed in zoos

      Witte, Carmel L.; Lamberski, Nadine; Rideout, Bruce; Fields, Victoria; Teare, Cyd Shields; Barrie, Michael; Haefele, Holly; Junge, Randall; Murray, Suzan; Hungerford, Laura L. (2013)
      The identification of feline herpesvirus (FHV) infected cheetahs (Acinonyx jubatus) and characterization of shedding episodes is difficult due to nonspecific clinical signs and limitations of diagnostic tests. The goals of this study were to develop a case definition for clinical FHV and describe the distribution of signs. Medical records from six different zoologic institutions were reviewed to identify cheetahs with diagnostic test results confirming FHV….
    • 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.
    • Gastric pneumatosis with associated eosinophilic gastritis in four black and white ruffed lemurs (Varecia variegata variegata)

      Niederwerder, M.C.; Stalis, Ilse H.; Campbell, G.A.; Backues, K.A. (2013)
      Pneumatosis cystoides intestinalis (PCI) with associated eosinophilic inflammation was documented in the gastric tissues of four black and white ruffed lemurs (Varecia variegata variegata). Pneumatosis cystoides intestinalis is an uncommon disease described in humans and characterized by multilocular gas-filled cystic spaces located within the wall of the gastrointestinal tract. These cystic spaces can occur in any location along the gastrointestinal tract as well as within the associated connective and lymphatic tissues…
    • Lessons from a retrospective analysis of a 5-yr period of preshipment testing at San Diego Zoo: a risk-based approach to preshipment testing may benefit animal welfare

      Marinkovich, Matt; Wallace, Chelsea; Morris, Pat J.; Rideout, Bruce; Pye, Geoffrey W. (2016)
      ...An alternative disease risk-based approach, based on a comprehensive surveillance program including necropsy and preventive medicine examination testing and data, has been in practice since 2006 between the San Diego Zoo and San Diego Zoo Safari Park. A retrospective analysis, evaluating comprehensive necropsy data and preshipment testing over a 5-yr study period, was performed to determine the viability of this model for use with sending animals to other institutions. Animals (607 birds, 704 reptiles and amphibians, and 341 mammals) were shipped to 116 Association of Zoos and Aquariums (AZA)-accredited and 29 non–AZA-accredited institutions....
    • 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….
    • 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.
    • The i5K Initiative: Advancing arthropod genomics for knowledge, human health, agriculture, and the environment

      Evans, Jay D.; Brown, Susan J.; Hackett, Kevin J.; Robinson, Gene; Richards, Stephen; Lawson, Daniel; Elsik, Christine; Coddington, Jonathan; Edwards, Owain; Emrich, Scott; et al. (2013)
      Insects and their arthropod relatives including mites, spiders, and crustaceans play major roles in the world’s terrestrial, aquatic, and marine ecosystems. Arthropods compete with humans for food and transmit devastating diseases. They also comprise the most diverse and successful branch of metazoan evolution, with millions of extant species. Here, we describe an international effort to guide arthropod genomic efforts, from species prioritization to methodology and informatics. The 5000 arthropod genomes initiative (i5K) community met formally in 2012 to discuss a roadmap for sequencing and analyzing 5000 high-priority arthropods and is continuing this effort via pilot projects, the development of standard operating procedures, and training of students and career scientists. With university, governmental, and industry support, the i5K Consortium aspires to deliver sequences and analytical tools for each of the arthropod branches and each of the species having beneficial and negative effects on humankind.
    • 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.