Twenty-one white-rumped shamas (19 necropsied, 2 biopsied) ( Copsychus malabaricus ) housed at the San Diego Zoo between 1992 and 2020 were diagnosed with Isospora infection based on evaluation of histologic sections. Review of these cases revealed a consistent histologic lesion characterized by nodular aggregates of atypical epithelioid macrophages containing few intracytoplasmic protozoa, with or without lymphocytic infiltrates. Of the 19 necropsied cases, 16 (84%) had systemic lesions variably affecting the liver, spleen, gastrointestinal tract, lung, pancreas, connective tissues, or bone marrow, while all 21 diagnosed cases had skin involvement. The findings suggest that white-rumped shamas have a unique inflammatory response to isosporosis with a predilection for the skin. Skin may be a diagnostically sensitive sampling site for histologic diagnosis of Isospora in this species. Keywords avian , apicomplexan , , , infectious disease , , , passerine birds
Twenty-one white-rumped shamas (19 necropsied, 2 biopsied) ( Copsychus malabaricus) housed at the San Diego Zoo between 1992 and 2020 were diagnosed with Isospora infection based on evaluation of histologic sections. Review of these cases revealed a consistent histologic lesion characterized by nodular aggregates of atypical epithelioid macrophages containing few intracytoplasmic protozoa, with or without lymphocytic infiltrates. Of the 19 necropsied cases, 16 (84%) had systemic lesions variably affecting the liver, spleen, gastrointestinal tract, lung, pancreas, connective tissues, or bone marrow, while all 21 diagnosed cases had skin involvement. The findings suggest that white-rumped shamas have a unique inflammatory response to isosporosis with a predilection for the skin. Skin may be a diagnostically sensitive sampling site for histologic diagnosis of Isospora in this species.
Parthenogenesis is a relatively rare event in birds, documented in unfertilized eggs from columbid, galliform, and passerine females with no access to males. In the critically endangered California condor, parentage analysis conducted utilizing polymorphic microsatellite loci has identified two instances of parthenogenetic development from the eggs of two females in the captive breeding program, each continuously housed with a reproductively capable male with whom they had produced offspring. Paternal genetic contribution to the two chicks was excluded. Both parthenotes possessed the expected male ZZ sex chromosomes and were homozygous for all evaluated markers inherited from their dams. These findings represent the first molecular marker-based identification of facultative parthenogenesis in an avian species, notably of females in regular contact with fertile males, and add to the phylogenetic breadth of vertebrate taxa documented to have reproduced via asexual reproduction.
Over the past 30 years, the California condor (Gymnogyps californianus) population has rebounded from 22 individuals to over 200 birds living in the wild. Historical impacts to the population have been largely anthropogenic. In this study, we explore mortality and cause of death data from condors that died during the years 2010-2014 and compare these to mortality data described by Rideout et al. in 2012, covering the years 1992-2009. In addition, morphologic and genetic analysis of the contents of the upper gastrointestinal (GI) tract was performed on the 2010-2014 condor mortalities to determine animal origins of the last meal eaten. The maximum population at risk within this time frame was 329 birds. During this time, 88 condors died and underwent post-mortem examination, and 41 birds were lost to tracking efforts and presumed dead (crude mortality rate of 39%; 129/329). A cause of death was determined for 66 of the 88 necropsied birds. Lead toxicosis remained a significant negative factor in condor population recovery, being related to the deaths of 37 adult and juvenile condors (proportional mortality rate 56%). Compared to condors succumbing to other causes of death, cattle were less often part of the last meal of lead-intoxicated condors. Based on these data, continued efforts to mitigate the impact of lead on California condors should be pursued.
Ten red ruffed lemurs (Varecia rubra)-two adult females and their eight offspring-were evaluated in this case series. Two adult females were diagnosed with chronic, latent toxoplasmosis based on serologic testing. The first female lemur had two successive pregnancies. The first pregnancy resulted in transplacental transmission of Toxoplasma gondii. The only surviving offspring was diagnosed with congenital toxoplasmosis based on serologic testing and compatible ophthalmic lesions. The two deceased offspring had disseminated nonsuppurative inflammation and intralesional protozoal organisms consistent with T. gondii, which was confirmed by polymerase chain reaction. The second pregnancy did not result in transplacental transmission. The second chronically infected adult female lemur had one pregnancy that resulted in a single stillborn fetus without evidence of transplacental transmission of T. gondii. Treatment with trimethoprim-sulfamethoxazole and folinic acid was administered to the first adult female and one offspring, but no treatment was given to the second adult female. All surviving lemurs had no further complications associated with toxoplasmosis. This case series demonstrates that chronic, latent infection of reproductive female red ruffed lemurs with T. gondii may result in variable outcomes: (1) transplacental transmission with disseminated fetal infection and stillbirth, (2) transplacental transmission with congenital infection and survival, or (3) lack of transplacental transmission and healthy offspring. Information gained from these cases may help guide recommendations for breeding of this critically endangered species.
Over the past 30 years, the California condor (Gymnogyps californianus) population has rebounded from 22 individuals to more than 200 birds living in the wild. Historical impacts on the population have been mostly anthropogenic. In this study, we explore mortality and cause of death data from condors that died during the years 2010–2014 and compare these to mortality data described by Rideout et al. in 2012, covering the years 1992–2009. Also, morphologic and genetic analysis of the upper gastrointestinal (GI) tract contents was performed on the 2010–2014 condor mortalities to determine animal origins of the last meal eaten. The maximum population at risk within this time frame was 329 birds. During this time, 88 condors died and underwent postmortem examination, and 41 birds were lost to tracking efforts and presumed dead (39% crude mortality rate; 129/329). A cause of death was determined for 66 of the 88 necropsied birds. Lead toxicosis remained a significant negative factor in condor population recovery, being related to the deaths of 37 adult and juvenile condors (56% proportional mortality rate). Cattle were less often part of the last meal of lead-intoxicated condors than condors that succumbed to other causes of death. Based on these data, continued efforts to mitigate the impact of lead on California condors should be pursued.
A 3-year-old female Bruce's green pigeon (Treron waalia) was presented with granulomatous inflammation of the cere and underlying tissues with osteomyelitis and bone proliferation of the dorsal premaxilla. Biopsy and culture revealed the presence of Mycobacterium avium-intracellulare complex, and multi-antimicrobial treatment was initiated with clarithromycin, ethambutol, rifabutin, and enrofloxacin. The cere lesion improved and no evidence of systemic granulomas was observed over 4 months of treatment, although leukocytosis and monocytosis persisted. Five months after discontinuation of antibiotic therapy, the white blood cell count had normalized, but distal beak irregularities and partial recurrence of the mass were present. The bird died 15 months after discontinuation of antibiotic therapy and necropsy revealed no evidence of active mycobacteriosis of the beak or cere. This report documents an unusual clinical presentation of mycobacteriosis, in addition to its successful resolution.
An adult nematode was grossly identified in the meninges of a Malayan sambar (Rusa unicolor equina), with numerous microfilariae associated with encephalitis and vasculitis on histopathology. The nematode was confirmed to be Elaeophora schneideri by sequencing a portion of the 18S rRNA gene. Our report highlights the potential for aberrant migration of E. schneideri in exotic deer species and the use of advanced testing to specifically identify this metazoan parasite, avoiding misidentification of Parelaphostrongylus tenuis.
Leucaena (Leucaena leucocephala) is a leguminous tree that is nutritious forage for domestic livestock when ingested in limited amounts. Unfortunately, leucaena contains mimosine, a plant amino acid, that can be toxic when ingested at higher concentrations. Reported toxic effects include alopecia (fur loss), poor body condition, infertility, low birth weight, thyroid gland dysfunction, and organ toxicity. Originally native to Mexico and Central America, leucaena has been introduced throughout the tropics, including Berenty Reserve, Madagascar where it was planted as supplemental browse for livestock. In Berenty, a seasonal syndrome of alopecia in ringtailed lemurs (Lemur catta) is associated with eating leucaena. Although much is known about the toxic effects of leucaena and mimosine on domestic animals and humans, the systemic effects on wildlife had not been studied. In a comparison of lemurs that include leucaena in their diet and those that do not, we found that animals that ingest leucaena absorb mimosine but that ingestion does not affect body condition, cause kidney or liver toxicity, or affect the intestinal tract. Alopecia is due to mimosine's interference of the hair follicle cycle. Leucaena ingestion is associated with higher serum albumin, α‐tocopherol, and thyroxine concentrations, suggesting that leucaena may provide some nutritional benefit and that lemurs can detoxify and convert mimosine to a thyroid stimulating metabolite. The primary conservation consequence of leucaena ingestion at Berenty may be increased infant mortality due to the infants' inability cling to their alopecic mothers. The widespread introduction of leucaena throughout the tropics and its rapid spread in secondary forest conditions mean that many other leaf‐eating mammals may be including this tree in their diet. Thus, exposure to leucaena should be considered when wildlife health is being evaluated, and the potential effects on wildlife health should be considered when contemplating leucaena introduction into or near wildlife habitat. Am. J. Primatol. 77:633–641, 2015. © 2015 Wiley Periodicals, Inc.
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. The exact cause of this disease is unknown. The four black and white ruffed lemurs described in this case series were captive born and had been housed in zoological institutions at two separate locations. Three of the four cases were female lemurs, and two of the affected lemurs were directly related. The individual disease presentations spanned a 5-yr time period. Two lemurs presented dead with no premonitory signs, whereas the other two lemurs presented with clinical signs of gastrointestinal disease and nonspecific signs of weakness. Gastric pneumatosis, diagnosed either grossly or histopathologically in each of these four lemurs, is described as a subset of PCI in which cystic spaces are localized to the stomach wall. Significant eosinophilic inflammatory infiltrate was identified on histopathology of gastric tissues and found to be associated with the cystic lesions in each lemur. No classic etiology, such as a fungal infection or a parasitic infection, was identified as the cause of the eosinophilic gastritis. This case series demonstrates that gastric pneumatosis with associated eosinophilic gastritis may be a significant gastrointestinal disease in black and white ruffed lemurs.
A16-yr-old male koala (Phascolarctos cinereus) presented for nonspecific signs of illness and weight loss. Despite 2 mo of diagnostics and supportive care, the koala's health declined and euthanasia was elected. On histopathologic examination, lesions containing fungal organisms morphologically consistent with coccidioidomycosis were found in the lung, liver, spleen, kidney, lymph node, heart, eye, and bone marrow. Although disseminated infection was present, the koala was IgM and IgG seronegative for Coccidioides spp. 1 mo prior to euthanasia.
We document causes of death in free-ranging California Condors (Gymnogyps californianus) from the inception of the reintroduction program in 1992 through December 2009 to identify current and historic mortality factors that might interfere with establishment of self-sustaining populations in the wild. A total of 135 deaths occurred from October 1992 (the first post-release death) through December 2009, from a maximum population-at-risk of 352 birds, for a cumulative crude mortality rate of 38%. A definitive cause of death was determined for 76 of the 98 submitted cases, 70%(53/76) of which were attributed to anthropogenic causes. Trash ingestion was the most important mortality factor in nestlings (proportional mortality rate [PMR] 73%; 8/11), while lead toxicosis was the most important factor in juveniles (PMR 26%; 13/50) and adults (PMR 67%; 10/15). These results demonstrate that the leading causes of death at all California Condor release sites are anthropogenic. The mortality factors thought to be important in the decline of the historic California Condor population, particularly lead poisoning, remain the most important documented mortality factors today. Without effective mitigation, these factors can be expected to have the same effects on the sustainability of the wild populations as they have in the past.
When the fi rst patients with ILI in households were unvaccinated, ILI was observed in 59 of 136 children, yielding an SAR b0 of 43.4%.Among 6 exposures caused by vaccinated fi rst patients, ILI developed in 1 person, yielding an SAR b1 of 16.7%.Although not signifi cant (p = 0.40), the reduction in infectiousness by vaccination was estimated to be 1 -SAR b1 /SAR b0 = 61.6%(95% CI -132.3% to 93.6%).The SAR 01 was 0% (i.e., 1 exposure to an unvaccinated person caused by a vaccinated fi rst patient did not result in infl uenza).Limiting the defi nition of infl uenza to confi rmed cases, all 8 exposures to vaccinated persons did not result in infl uenza, and SAR 0b and SAR 1b were 10.8% and 0%, respectively.Similarly, all 5 exposures caused by vaccinated fi rst patients did not result in confi rmed cases, and SAR b0 and SAR b1 were 10.5% and 0%, respectively.Although the CIs of the estimates included zero because of the small sample size, the expected reductions in susceptibility and infectiousness were 75.0% and 61.6%, respectively, which is consistent with fi ndings from a meta-analysis of vaccine effi cacy against seasonal infl uenza (9).Two limitations must be noted, namely, estimates based on nonrandom samples and a case defi nition that relied on symptoms of case-patients.The former point cannot be explicitly addressed by a retrospective study design, but we enforced strict inclusion criteria for analyses and limited our study to healthy children.Accounting for the latter point (e.g., serologic diagnosis to capture symptomatic and asymptomatic cases) could yield slightly higher estimates than ours, provided that vaccination reduces the probability of clinical illness if infection occurs.Thus, despite these limitations and a critical need for further studies that include estimations of effectiveness (10), our results provide insight into the effects of vaccination in reducing risks for infection and clinical attack among children exposed to pandemic (H1N1) 2009 virus in their households.
reported. Badgers and binturong have been housed in zoological gardens for decades without incidence of infl uenza. Increased surveillance for infl uenza by the scientifi c community during the pandemic may have resulted in the novel recognition of infection in these species. Alternatively, the current pandemic (H1N1) 2009 virus may have a broader host range and stronger virulence than viruses in the past. Pandemic (H1N1) 2009 was fi rst detected in humans in March 2009 and reached pandemic levels by June of that year, rapidly establishing a rich pool for the development of genetic variants. Naturally acquired disease has now been described in 10 animal species, and experimental infection has been reported in an additional 2 animals (mice and cynomolgus macaques) (9). The ubiquity of pandemic (H1N1) 2009 and its ability to infect a diverse range of hosts is worrisome for the health of wildlife and for the possibility of creating additional reservoirs that could alter the evolution of subtype H1N1 viruses by applying varied selection pressures and establishing new ways of generating unique reassortant strains.
Objective —To characterize infection patterns and identify factors associated with avian mycobacteriosis among zoo birds that were housed with infected enclosure mates. Design —Matched case-control study. Animals —79 birds with avian mycobacteriosis (cases) and 316 nondiseased birds (controls) of similar age and taxonomic group that were present in the bird collection of the Zoological Society of San Diego from 1991 through 2005. Procedures —Inventory and necropsy records from all eligible, exposed birds (n = 2,413) were examined to determine disease incidence and prevalence in the exposed cohort. Cases were matched in a 1:4 ratio to randomly selected controls of similar age and taxonomic grouping. Risk factors for mycobacteriosis (demographic, temporal, enclosure, and exposure characteristics as well as translocation history) were evaluated with univariate and multivariable conditional logistic regression analyses. Results —Disease prevalence and incidence were estimated at 3.5% and 8 cases/1,000 bird-years at risk, respectively. In the multivariable model, cases were more likely to have been imported into the collection, exposed to mycobacteriosis at a young age, exposed to the same bird species, and exposed in small enclosures than were controls. Odds for disease increased with an increasing amount of time spent with other disease-positive birds. Conclusions and Clinical Relevance —The low incidence of mycobacteriosis and the risk factors identified suggested that mycobacteria may not be easily transmitted through direct contact with infected enclosure mates. Identification of risk factors for avian mycobacteriosis will help guide future management of this disease in zoo bird populations.
The objective of the current study was to identify factors associated with avian mycobacteriosis in zoo birds. Inventory data, population health records. and necropsy data from eligible birds in the Zoological Society of San Diego's (ZSSD) collection from 1991-2005 (n = 13,976) were Used to describe disease incidence, prevalence, and postmortem findings. A matched case-control study was then conducted to identify factors describing demographic, temporal, and enclosure characteristics, along with move and exposure histories. Cases (disease-positive birds; n = 167) were matched in a 1:7 ratio with controls (disease-negative birds; n = 1169) of similar age and taxonomic groupings. Potential risk factors were evaluated using univariate and multivariable conditional logistic regression. Disease prevalence and incidence were estimated for the study period at 1.2% and 3 cases/1,000 bird-years at risk), respectively. Lesion characteristics and order prevalence are described. In the multivariable model, case birds were more likely to have been previously housed with a bird with mycobacterial disease involving, the intestinal tract (odds ratio [OR] = 5.6, P < 0.01) or involving only nonintestinal sites (OR 2.0, P < 0.01). Cases were more likely to have been imported into the collection than hatched at the ZSSD (OR 4.2 P < 0.01). Cases were moved among ZSSD e]enclosures more than controls (OR = 1.1 for each additional move, P < 0.01). Findings will help guide future management of this disease for zoo bird populations.
OBJECTIVE:To assess serum iron and ferritin concentrations, total iron-binding capacity, and transferrin saturation as indicators of iron metabolic status in 3 genera of lemurs and determine whether these variables are useful for screening for iron overload.DESIGN:Cross-sectional study.ANIMALS:11 ring-tailed lemurs (Lemur catta), 11 black lemurs (Eulemur macaco macaco), and 11 red-ruffed lemurs (Varecia rubra).PROCEDURES:Blood samples were collected weekly for 3 weeks and assayed for serum iron and ferritin concentrations and total iron-binding capacity. Liver biopsy specimens were evaluated histologically and assayed for total iron, nonheme iron, and trace mineral concentrations. Deposition of iron was scored on Prussian blue-stained slides.RESULTS:Hepatic iron content ranged from 497 to 12,800 Pg/g dry weight (median, 2,165 Pg/g). Differences were seen in mean hepatic iron content across genera, with ruffed lemurs having the highest concentrations and ring-tailed lemurs having the lowest. Iron accumulation in the liver was mild, and cellular pathologic changes associated with iron storage disease were not detected in any lemur. Ferritin concentration was the only variable that correlated significantly with hepatic iron content in all 3 genera of lemurs; however, both transferrin saturation and serum iron concentration were correlated with hepatic iron concentration in ring-tailed and ruffed lemurs.CONCLUSIONS AND CLINICAL RELEVANCE:Serum ferritin concentration was the only variable that was consistently correlated with hepatic iron content in all 3 genera. Mean hepatic iron content varied across genera, suggesting that the propensity for lemurs to develop iron overload in captivity may vary across taxa.
Haemoproteus spp. are ancient apicomplexan hemoparasites that have undergone extensive coevolution with their natural hosts and are typically species specific, with inapparent or minimal pathogenicity. A promiscuous genotype of Haemoproteus capable of undergoing host switching on a familial level was identified. This protozoan caused severe disease with high mortality in 6 species of exotic passerine birds housed in California at the San Diego Zoo's Wild Animal Park: Surinam crested oropendola ( Psarocolius decumanus decumanus), Guianan turquoise tanager ( Tangara mexicana mexicana), blue-necked tanager ( Tangara cyanicollis caeruleocephala, Guianan red-capped cardinal ( Paroaria gularis gularis), magnificent bird of paradise ( Diphyllodes magnificus hunsteini), and superb bird of paradise ( Lophorina superba). The birds had few or no clinical signs. Necropsy findings consisted of hemocoelom and irregularly scattered areas of hemorrhage and hepatocellular necrosis. Affected areas of liver contained solitary protozoal megaloschizonts in varied states of degeneration and peripheral nonsuppurative inflammation. No other parasite life stages were found in parenchymal organs or blood smears. Polymerase chain reaction using consensus primers for an avian malarial mitochondrial cytochrome B gene segment was positive in all cases. Sequencing and BLAST analysis identified the protozoan as a Haemoproteus sp. related to Haemoproteus spp. found in asymptomatic passerine birds native to North America. In situ hybridization was performed in 3 animals with a mitochondrial cytochrome B probe and was positive only in megaloschizonts. These findings suggest the recognition of a genotype of Haemoproteus that exhibits high levels of host infidelity and causes severe disease in captive birds exotic to North America.
Rapid assessment of immune status in neonatal ruminants of endangered species facilitates early intervention in cases of inadequate passive transfer of maternal immunoglobulins. Serum gamma-glutamyltransferase (GGT) was used to evaluate suspected passive transfer status in 25 North Indian muntjac (Muntiacus muntjak vaginalis), 45 Cretan goats (Capra algagrus cretica), 20 white-lipped deer (Cervus albirostris), 25 Mhorr gazelles (Gazella dama mhorr), and 31 Soemmerring's gazelles (Gazella soemmerringi soemmerringi). Serum GGT, measured within 48 hr of birth, was compared with clinical condition at 5 days of age. Neonatal Soemmerring's and Mhorr gazelles with GGT > 600 U/L were likely to survive without medical intervention, whereas GGT < 400 U/L was a good indicator that the gazelle neonate would need medical intervention. Neonatal muntjac with GGT > 200 U/L were also likely to survive without medical intervention. Because there is no gold standard for evaluating passive transfer status in neonatal nondomestic ruminants, it is recommended to evaluate the results of more than one diagnostic test, as well as clinical condition, in considering health status and disposition of neonatal ruminants of endangered species.
ABSTRACT In the winter of 2002, an outbreak of mycoplasma infection in Vaal rhebok (Pelea capreolus) originating from South Africa occurred 15 weeks after their arrival in San Diego, Calif. Three rhebok developed inappetence, weight loss, lethargy, signs related to pulmonary or arthral dysfunction, and sepsis. All three rhebok died or were euthanized. Primary postmortem findings were erosive tracheitis, pleuropneumonia, regional cellulitis, and necrotizing lymphadenitis. Mycoplasmas were detected in numerous tissues by electron microscopy, immunohistochemistry, and PCR. The three deceased rhebok were coinfected with ovine herpesvirus-2, and two animals additionally had a novel gammaherpesvirus. However, no lesions indicative of herpesvirus were seen microscopically in any animal. The rheboks' mycoplasmas were characterized at the level of the 16S rRNA gene, the 16S-23S intergenic spacer region, and the fructose biphosphate aldolase gene. Denaturing gradient gel electrophoresis was carried out to address the possibility of infection with multiple strains. Two of the deceased rhebok were infected with a single strain of Mycoplasma capricolum subsp. capricolum, and the third animal had a single, unique strain most closely related to Mycoplasma mycoides subsp. mycoides large-colony. A PCR survey of DNA samples from 46 other ruminant species demonstrated the presence of several species of mycoplasmas in the mycoides cluster, including a strain of M. capricolum subsp. capricolum identical to that found in two of the rhebok. These findings demonstrate the pervasiveness of mycoplasmas in the mycoides cluster in small ruminants and the potential for interspecies transmission and disease when different animal taxa come in contact.