Smithsonian's National Zoological Park Research Articles

Adipose tissue torsion with localized lymphangiectasia in a Rio Cauca caecilian Typhlonectes natans.

A female Rio Cauca caecilian Typhlonectes natans (estimated as between 10 and 18 years of age) housed at the Smithsonian National Zoological Park in Washington, D.C., developed progressive severe coelomic effusion over a 4-week period. The coelomic effusion was diagnosed via radiographs and ultrasound, and a sample of the fluid was obtained for analysis, which revealed a low-protein transudate suggestive of inflammation. As the coelomic effusion progressed, the caecilian became tachypneic, hyporexic, and lethargic. The caecilian was started on antibiotics and a diet trial, but signs continued despite therapy. An exploratory celiotomy was performed, which revealed adipose tissue torsion with local lymphangiectasia and a presumptive biliary cyst. Surgical correction was unable to be achieved due to concern for fatal hemorrhage, as the vasculature associated with the torsion was severely distended. Due to the severity of the torsion and associated risks, the caecilian was euthanized intraoperatively and subsequently necropsied for histologic evaluation. After reviewing the caecilian's presentation and the progression of disease, it is suspected that the severe coelomic effusion was secondary to lymphangiectasia, which occurred subsequent to the adipose tissue torsion. This is the first reported case of adipose tissue torsion and associated clinical disease in an aquatic caecilian and should be a differential for progressive coelomic effusion in this species.

RETROSPECTIVE REVIEW OF OPHIDIOMYCOSIS (OPHIDIOMYCES OPHIODIICOLA) AT THE SMITHSONIAN'S NATIONAL ZOOLOGICAL PARK (1983-2017).

A retrospective review of systemic or localized mycotic infections in captive snakes confirmed via biopsy or necropsy from 1983 to 2017 was performed at the Smithsonian's National Zoological Park. Quantitative polymerase chain reaction (qPCR) confirmed infection with Ophidiomyces ophiodiicola (Oo) in 36.8% (n = 14) of the 38 mycotic infections. Infections with Oo were evenly distributed over the 35-y period and lacked a sex predilection. There was a period prevalence of 4.5% of completed snake necropsy or biopsy cases that were Oo positive. Species affected included green anaconda (Eunectes murinus, n = 4), garden tree boa (Corallus hortulanus, n = 1), false water cobra (Hydrodynastes gigas, n = 5), yellow anaconda (Eunectes notaeus, n = 1), eastern milksnake (Lampropeltis triangulum, n = 1), Brazilian rainbow boa (Epicrates cenchria cenchria, n = 1), and eastern diamondback rattlesnake (Crotalus adamanteus, n = 1). Histopathology demonstrated one or more of the following: heterophilic to necrotizing epidermitis with or without granulomatous dermatitis (n = 12), granulomatous pneumonia (n = 5), granulomatous endophthalmitis (n = 1), and subcutaneous-intramuscular fungal granuloma (n = 1). This study documents the presence of ophidiomycosis in a captive collection for almost 40 years, despite current literature designating it a recently emerging pathogen.

Macronutrient composition of olive baboon (Papio anubis) milk: A comparison to rhesus macaque (Macaca mulatta) milk.

This study was designed to (1) characterize the macronutrient composition of olive baboon (Papio anubis) milk, (2) compare baboon milk composition to that of rhesus macaques (Macaca mulatta), and (3) evaluate the association between the proportion of milk energy derived from protein and relative growth rate within anthropoid primates. A single milk sample was collected from each of eight lactating olive baboons ranging between 47- and 129-days postparturition and six rhesus macaques from 15- to 92-days living at the same institution under identical management conditions. Macronutrient composition (water, fat, protein sugar, and ash) was determined using standard techniques developed at the Nutrition Laboratory at the Smithsonian National Zoological Park. Baboon milk on average contained 86.0% ± 0.6% water, 4.7% ± 0.5% fat, 1.6% ± 0.04% protein, 7.3% ± 0.07% sugar, and 0.165% ± 0.007% ash. Baboon milk gross energy (GE) averaged 0.81 ± 0.04 kcal/g with 51.9% ± 2.6% from fat, 11.8% ± 0.7% from protein, and 36.2% ± 2.0% from sugar. Baboon milk demonstrated strong similarity to milk composition of the closely phylogenetically related rhesus macaque (86.1% ± 0.3% water, 4.1% ± 0.4% fat, 1.69% ± 0.05% protein, 7.71% ± 0.08% sugar, 0.19% ± 0.01% ash, and 0.78 kcal/g). There was no statistical difference between baboon and macaque milk in the proportions of energy from fat, sugar, and protein. Baboon milk can be described as a high sugar, moderate fat, and low protein milk with moderate energy density, which is consistent with their lactation strategy characterized by frequent, on-demand nursing and relatively slow life history compared to nonprimate mammal taxa. The milk energy from protein of both baboon and macaque (12.8% ± 0.3%) milk was intermediate between the protein milk energy of platyrrhine (19.3%-23.2%) and hominoid (8.9%-12.6%) primates, consistent with their relative growth rates also being intermediate. Compared to these cercopithecid monkeys, platyrrhine primates have both higher relative growth rates and higher milk energy from protein, while apes tend to be lower in both.

Macronutrient composition of milk from two captive African elephant (Loxodonta africana) cows.

We assayed 31 milk samples collected from two African elephant cows housed at the Indianapolis Zoo across lactation (birth to calf age 973 days) for macronutrient composition (water, fat, protein, sugar, gross energy [GE], ash, calcium, and phosphorus). All assays were performed at the Smithsonian National Zoological Park Nutrition Laboratory, Washington, DC (SNZP) using standard methods developed at SNZP. Milk constituents are expressed on a weight-per-weight basis (%) and as a proportion each constituent contributes to milk energy. Calf weights were recorded, and growth rate calculated. The macronutrient composition of the African elephant milk samples was compared to previously published results for Asian elephants using analysis of covariance. African elephant milk is similar to Asian elephant milk, being moderately high in fat and energy and low in sugar. The mean values across lactation (excluding colostrum; n = 28) are 5.6 ± 0.3% crude protein, 3.1 ± 0.3% sugar, 13.0 ± 1.0% fat, and GE of 1.63 ± 0.10 kcal/g. Milk composition did not differ between cows. Milk composition significantly changed over lactation; fat and protein increased, and sugar decreased with calf age, comparable to previously reported data for African and Asian elephant milk. The proportion of milk energy from fat increased and that from sugar decreased over lactation, but the energy from protein was relatively constant. Protein contributed a higher proportion of energy to African elephant milk compared to Asian elephant milk (20.6% vs. 17.0%, p = .001). Despite this, calf growth rate was similar between the species, with the calves in this study gaining about 0.8 kg/day for the first 6 months.

Impacts of the season and reproductive status on fecal reproductive and adrenocortical steroid metabolites in zoo Cuban crocodiles (Crocodylus rhombifer).

Conservation strategies for crocodilians often include captive breeding to create stable assurance populations. Evaluating adrenal and gonadal hormone patterns can provide animal managers with data to more effectively monitor animal welfare and reproductive status. This study evaluated the effects of season (breeding, nesting, or off), sex (male and female), and reproductive status of females (egg-laying/housed with a male or non-laying/housed solo) on concentrations of fecal glucocorticoid metabolite (FGM), fecal androgen metabolite (FAM), and fecal progestogen metabolite (FPM) in seven Cuban crocodiles, Crocodylus rhombifer, at the Smithsonian's National Zoological Park. Overall, seasonal changes in FGM and FPM concentrations were only observed in egg-laying females; FGM and FPM concentrations were both higher during the nesting season compared to the breeding and off seasons. Seasonal changes in FAM concentrations were only observed in males; males had higher FAM concentrations during the breeding and nesting seasons compared to the off season. Future studies investigating the use of fecal hormone metabolites in crocodilians are necessary to understand differences between individuals and species, to further elucidate the interactions between hormones and environmental factors, such as social housing, and to develop long-term datasets for the management of this species.

Nest location preferences in zoo-housed orangutans

Nest building is an advanced and complex activity that wild orangutans engage in, yet they do so on a daily basis and with potential safety consequences. Like their wild counterparts, zoo-housed orangutans also make nests when given adequate materials, yet comparatively little research has documented the nesting habits of captive orangutans, including potential social and environmental influences of nest site selections. We documented the night nesting behavior of six adult orangutans housed at the Smithsonian's National Zoological Park (NZP), identifying preferred nest locations and proximity to conspecifics, comparing observed patterns to those reported in a nest behavior survey of orangutan facilities throughout the Association of Zoos and Aquariums (AZA). Survey results reveal that in addition to several universal patterns of nesting behaviors, as in the wild, the sharing of night nests by captive adult orangutans occurs only rarely (2 of 31 surveyed facilities). Data collected at NZP indicate that night nearest neighbor associations among nesting conspecifics may be a useful proxy for actual nearest neighbor data taken during daytime social interactions and may offer a more feasible alternative for determining social relationships among large groups of socially housed orangutans.

Improved capture of stable flies (Diptera: Muscidae) by placement of knight stick sticky fly traps protected by electric fence inside animal exhibit yards at the Smithsonian's National Zoological Park.

Stable flies are noxious blood-feeding pests of exotic animals at zoological parks, inflicting painful bites, and causing discomfort to animals. Stable fly management is difficult because of the flies' tendency to remain on the host animals only when feeding. Non-toxic traps can be efficient but traps placed around exhibit perimeters captured fewer-than-expected numbers of flies. By surrounding traps with square electric fence enclosures, traps could be placed in the exhibits with the host animals and compared with an equal number of traps placed along perimeter fences. During a 21-week study, traps inside exhibits captured 5× more stable flies than traps placed along exhibit perimeters. Traps inside exhibits tended to show more fluctuations in fly populations than traps along perimeters. The increased numbers of flies captured using this technique should provide relief from this pestiferous fly and greatly improve animal health and welfare. We believe this to be the first study where traps were used to capture stable flies in exhibit yards at a zoological park.

Crocodilian perivitelline membrane-bound sperm detection.

Advanced reproductive technologies (ART's) are often employed with various taxa to enhance captive breeding programs and maintain genetic diversity. Perivitelline membrane-bound (PVM-bound) sperm detection has previously been demonstrated in avian and chelonian species as a useful technique for breeding management. In the absence of embryotic development within an egg, this technique can detect the presence of sperm trapped on the oocyte membrane confirming breeding, male reproductive status, and pair compatibility. PVM-bound sperm were successfully detected in three clutches of Cuban crocodile (Crocodylus rhombifer) eggs at the Smithsonian's National Zoological Park (NZP) for the first time in any crocodilian species. PVM-bound sperm were detected in fresh and incubated C. rhombifer eggs, as well as eggs that were developing (banded) and those that were not (not banded). The results of this study showed significant differences in average sperm densities per egg between clutches (p = 0.001). Additionally, there was not a significant difference within clutches between eggs that banded and those that did not band (Clutch A, p = 0.505; Clutch B, p = 0.665; Clutch C, p = 0.266). The results of this study demonstrate the necessity to microscopically examine eggs that do not develop (do not band), to determine if sperm is present, which can help animal managers problem solve reproductive shortcomings. PVM-bound sperm detection could be a useful technique in assessing crocodilian breeding programs, as well as have potential uses in studies assessing sperm storage, artificial insemination, and artificial incubation.

Age, fertility and reproductive behavior in cuban crocodiles, Crocodylus rhombifer, at the Smithsonian's National Zoological Park.

The Smithsonian's National Zoological Park (NZP) has a long history with Cuban crocodiles, Crocodylus rhombifer, beginning in 1900's when the first animals arrived at the NZP. Today, the Zoo has two breeding groups of C. rhombifer and has observed and analyzed reproductive behavior and fertility rates over the last three years. Fertility rates were determined initially by observing the formation of an opaque band that forms on the shell of a fertile egg, called banding. The fertility rates by banding were later compared to the observation made after opening the eggs to verify fertility. In addition to tracking fertility, nesting and agonistic behavior were also observed. Several notable observations were documented over the same period. These included a male predating a nesting female's eggs, increased aggression between two females housed together, the continued development of a partially banded egg, and the discovery of 19 additional egg shells post oviposition by both females in the enclosure. Here we discuss the nest phenology, fertility and behavior of the five exhibited C. rhombifer at the Smithsonian's National Zoological Park over a 3-year period. Zoo Biol. 34:278-284, 2015. © 2015 Wiley Periodicals Inc.

The kinematics of the California sea lion foreflipper during forward swimming

To determine the two-dimensional kinematics of the California sea lion foreflipper during thrust generation, a digital, high-definition video is obtained using a non-research female sea lion at the Smithsonian National Zoological Park in Washington, DC. The observational videos are used to extract maneuvers of interest—forward acceleration from rest using the foreflippers and banked turns. Single camera videos are analyzed to digitize the flipper during the motions using 10 points spanning root to tip in each frame. Digitized shapes were then fitted with an empirical function that quantitatively allows for both comparison between different claps, and for extracting kinematic data. The resulting function shows a high degree of curvature (with a camber of up to 32%). Analysis of sea lion acceleration from rest shows thrust production in the range of – and maximum flipper angular velocity (for rotation about the shoulder joint) as high as . Analysis of turning maneuvers indicate extreme agility and precision of movement driven by the foreflipper surfaces.

Video-graphic study of the behaviour of juvenile Brown kiwiApteryx mantellifemales at Smithsonian National Zoological Park, Washington, DC

The kiwi, indigenous to New Zealand, is a small flightless bird that is unique in the avian world. Detailed studies in kiwi behaviour are limited because of the nocturnal nature of the species. In this study, two juvenile Brown kiwi Apteryx mantelli chicks were monitored using a video camera for about 24 hours over a period of 2 months. Primarily, this study focused on the budgeting of 26 distinct behaviours during different time periods. Many of the behaviours, such as ‘feeding’, ‘drinking’ and ‘probing’, had similar totals, compared with other behaviours, such as ‘aggression’, ‘stretching body’ and ‘jumping’, which were predominantly expressed by one individual. Certain behaviours, such as ‘pacing’, ‘running’ and ‘jumping’, were often seen more frequently at certain time periods. Territoriality, including changes pertaining to the individual and their size of territory, was also noted as the observations progressed. This study provides a better understanding of the behaviour of Brown kiwi chicks in terms of budgeting different behaviours and interactions between juvenile ♀♀.

The Relationship between Environmental Factors and Flamingo Aggression Examined via Internet Resources

This study sought to examine the relationship between weather and aggression in Caribbean flamingos by utilising a novel observation method. Previous research has shown evidence of increased levels of aggression during periods of warmer weather in a wide range of species including humans. We observed the captive flock of Caribbean flamingos at the Smithsonian National Zoological Park (Washington, DC, USA) by means of a web cam, and correlated the observed instances of aggression with eight different weather variables gathered via www.weather.com . Results evidenced significant positive correlations between aggression and several variables including: temperature [ r (38) = 0.31, P = 0.048], “feels like” [ r (38) = 0.31, P = 0.049], and UV-index [ r (38) = 0.35, P = 0.025]; and a multiple linear regression (stepwise) suggested that UV-index is a significant predictor of aggressive instances, thus highlighting the relationship between such environmental factors and flamingo aggression. Evidence has been found of a relationships between UV light and aggression in other species, and the results of the present study suggest a similar relationship in flamingos. Employing webcams may allow researchers to obtain larger samples to be included in the study of aggression or to examine this and other behaviors in a wider variety of captive animals.

RETROSPECTIVE ANALYSIS OF MORTALITIES IN ELEPHANT SHREWS (MACROSCELIDIDAE) AND TREE SHREWS (TUPAIIDAE) AT THE SMITHSONIAN NATIONAL ZOOLOGICAL PARK, USA

Investigations into the cause of mortality and other important findings at necropsy were made into two families of small mammals at the Smithsonian National Zoological Park (SNZP; USA). Necropsy reports from 1976 through 2008 were reviewed for all elephant shrews in family Macroscelididae (n = 118) and all tree shrews in family Tupaiidae (n = 90) that lived for greater than 30 days at the SNZP. Causes of mortality were classified by body system and etiology to identify prevalent diseases and trends across demographics for each family. In elephant shrews, gastrointestinal disease (n = 18) and respiratory disease (n = 22) were important causes of mortality with an increased prevalence of pneumonia in adult males. Trauma was a common cause of mortality in tree shrews (n = 22). Cryptococcosis was an important cause of mortality in both families (n = 8 elephant shrews; n = 13 tree shrews). Bacterial infections, often systemic at time of mortality, were also common (n = 16 elephant shrews; n = 17 tree shrews). Arteriosclerosis was a common comorbid pathology noted at necropsy in certain populations, seen only in Elephantulus rufescens in the family Macroscelididae (n = 22) and in only males in the family Tupaiidae (n = 11). Gongylonemiasis was seen commonly in tree shrews (n = 15), as a comorbid finding, or in 5 cases directly leading to mortality. Awareness of the prevalence of these diseases can help guide prevention and intervention strategies.

Approaches to Understanding and Managing Pacing in Sloth Bears in a Zoological Setting

A significant challenge for animal care staff in zoos is the prevention or reduction of stereotypic behaviors in the animals they manage. Zoo professionals work to create opportunities for animals to demonstrate species-typical behaviors and to teach visitors about the natural behaviors of the animals on exhibit. Therefore the expression of stereotypic behavior presents a multi-disciplinary problem. Behavioral researchers have repeatedly examined stereotypic behavior in zoological settings to determine successful approaches to address this challenge. Three investigations of pacing in two adult male sloth bears (Melursus ursinus) at Smithsonian's National Zoological Park are presented here. In addition, a case report detailing observations of the rapid onset of an intense stereotypy in a young male sloth bear is included. The first study investigates the effects of five different enrichment strategies on pacing behavior in an adult male with a long history of pacing. The second is a two-year study examining seasonal changes and the effects of social companionship on pacing when the same adult male was housed with a breeding female, a non-breeding (contracepted) female, or a young male. In the third study, we present preliminary data on the effects of the selective serotonin re-uptake inhibitor, fluoxetine, as an adjunct pharmacological treatment for pacing. And finally, our case report details the development an intense stereotypy in a young male sloth bear just after he is weaned and separated from his mother. The findings reveal that the causes, degree, and effective management of even a single observed behavior such as pacing within even a single species can vary greatly by individual and circumstance, highlighting the need for individualized assessment and management plans.

Molecular Reproduction & Development: Volume 77, Issue 5

AbstractClouded leopard (Neofelis nebulosa) male cub born at the Smithsonian's National Zoological Park. Rampant habitat loss in Southeast Asia and poaching are threatening the clouded leopard population. Successful breeding programs (for future reintroductions) have benefited from basic reproductive studies conducted in this species for several years (see Wildt et al., this issue). (Photo courtesy of Mehgan Murphy, Smithsonian's National Zoological Park).

Redefining Our Relationship with Elephants

Redefining Our Relationship with Elephants

Novel Environmental Enrichment May Provide a Tool for Rapid Assessment of Animal Personality: A Case Study With Giant Pandas (Ailuropoda melanoleuca)

Historically, the assessment of nonhuman animal personality has included a variety of methods—from direct behavioral observations in a variety of test situations to assessments provided by animal caretakers or trainers. Careful observation of how animals in zoos interact with novel enrichment may provide reliable insight into their personality. This study sought to describe a process for evaluating whether different methods of assessing personality result in similar conclusions. The study exposed 4 giant pandas at the Smithsonian National Zoological Park and Zoo Atlanta to 10 novel enrichment items and recorded their behavior. Keepers also rated each panda on 23 behavioral characteristics on a survey. The study obtained individual behavior profiles for each panda. Significant differences across individuals in both the novel enrichment trials and keeper surveys formed the basis for the profiles. These methods also provided some insight into differences between the sexes that—based on the natural history of giant pandas—are qualitatively similar to what would be expected. The study found some consistency between assessment methods. However, there is a need for further study to validate these measures in a larger sample of giant pandas.

Oviduct Adenocarcinoma in Some Species of Captive Snakes

This article reports 5 cases of oviduct adenocarcinoma in adult captive snakes from Smithsonian's National Zoological Park. This neoplasm was found in 1 of each of the following species: emerald tree boa (Corallus caninus), Amazonian tree boa (Corallus enydris enydris), Burmese rock python (Python molurus bivittatus), Northern pine snake (Pituophis melanoleucus melanoleucus), and corn snake (Elaphe guttata). Grossly, tan to red firm masses were found within oviducts in 3 cases. In an additional 2 cases, the primary tumor was detected only histologically. Microscopically, neoplasms were papillary, and often extended transmurally. The neoplastic cells were polygonal and organized in acini or cords, with often abundant fibrovascular stroma. Hemorrhages and necrosis were present in all cases. Inflammation, myxomatous material, desmoplasia, and bacteria were often observed. Histologic evidence of metastasis was present in all cases. Solid metastases were seen in all animals except the Northern pine snake and involved several organs including the liver, lung, and heart. Emboli of neoplastic cells were observed in all animals but the Burmese rock python and corn snake.

NEW DISPLAY BEHAVIOR IN MALE KORI BUSTARD (ARDEOTIS KORI STRUTHIUNCULUS)

Abstract Kori Bustards (Ardeotis kori) are polygynous and males display singly or in loose lek formations to females during the breeding season. A new display, head tossing, has been observed on repeated occasions by five different males (all Ardeotis kori struthiunculus) in the Smithsonian National Zoological Park, Dallas Zoo, and San Diego Wild Animal Park. This display has not been reported for A. k. kori or in any other Ardeotis species. Trained behavior watchers recorded detailed observations of a male bustard's booming behavior and frequency in 2004 and 2005; over the 2 years they collected 407 hrs of booming data. Head tossing occurred when the male rapidly threw his head backward onto his back. The head tossing display further exposed the white neck feathers and the motion of head tossing was extremely visible. Head tossing was followed by a cessation of booming or was a transition between additional booming sessions. Head tossing primarily occurred at the end of a six-boom calling bout (90% of th...

MORTALITY OF CAPTIVE BLACK-FOOTED FERRETS (MUSTELA NIGRIPES) AT SMITHSONIAN'S NATIONAL ZOOLOGICAL PARK, 1989–2004

Black-footed ferret (Mustela nigripes) mortality was investigated retrospectively based on the pathology records of 107 captive animals held at Smithsonian's National Zoological Park from 1989 to 2004. The majority of deaths in neonates were due to cannibalism (n = 42; 64.6%) and maternal trauma (n = 11; 16.9%); both of these causes of mortality decreased during the study period. Prior to 2001, juvenile mortality was most often caused by gastrointestinal disease (n = 11; 52.4%), including coccidiosis, salmonellosis, and clostridium infection. In 2001, improvements in husbandry, hygiene, and medical treatment led to decreases in juvenile mortality associated with gastrointestinal disease. The most common causes of death in adult ferrets were renal or neoplastic disease. The etiology of the high prevalence of renal disease in the last 4 yr of the study is unknown; it was not associated with increasing age or inbreeding. Improved hygiene and vigilant monitoring for signs of gastrointestinal and renal disease will continue to improve the success of the captive propagation of this species.