Unique multiple paternity in the endangered big‐headed turtle (Platysternon megacephalum) in an ex situ population in South China

Understanding the mating system and reproductive strategies of an endangered species is critical to the success of captive breeding. The big‐headed turtle (Platysternon megacephalum) is one of the most threatened turtle species in the world. Captive breeding and reintroduction are necessary to re‐establish wild populations of P. megacephalum in some of its historical ranges in China, where the original populations have been extirpated. However, the captive breeding of P. megacephalum is very difficult and this may be due to its mysterious reproductive strategies and special behavior (e.g., aggressive temperament and territoriality). In this study, we achieved successful captive breeding of P. megacephalum by creating a habitat that mimics natural conditions and then investigated its mating system using microsatellite makers. A total of 16 clutches containing 79 eggs of P. megacephalum were collected, and 52 were hatched successfully over two breeding seasons. Of the 15 effective clutches, 6 clutches (40%) exhibited multiple paternity. There was no significant correlation between clutch size and multiple paternity, and no significant difference in hatching success between multiple‐sired and single‐sired clutches. However, there was significant correlation between male body size and the number of offspring, with higher‐ranked males contributing to more clutches. Our results provide the first evidence of multiple paternity and male hierarchy in P. megacephalum. These findings suggest that multiple paternity and male hierarchy should be considered in captive breeding programs for P. megacephalum, and creating a habitat that mimics natural conditions is an effctive way to achieve successful captive breeding and investigate the mating systems of this species.     

Home‐site fidelity and homing behavior of the big‐headed turtle Platysternon megacephalum

Site fidelity refers to the restriction of dispersal distance of an animal and its tendency to return to a stationary site. To our knowledge, the homing ability of freshwater turtles and their fidelity is reportedly very low in Asia. We examined mark–recapture data spanning a 4‐year period in Diaoluoshan National Nature Reserve, Hainan Province, China, to investigate the site fidelity and homing behavior of big‐headed turtles Platysternon megacephalum. A total of 11 big‐headed turtles were captured, and all individuals were used in this mark–recapture study. The site fidelity results showed that the adult big‐headed turtles (n = 4) had a 71.43% recapture rate in the original site after their release at the same site, whereas the juveniles (n = 1) showed lower recapture rates (0%). Moreover, the homing behavior results showed that the adults (n = 5) had an 83.33% homing rate after displacement. Adult big‐headed turtles were able to return to their initial capture sites (home) from 150 to 2,400 m away and precisely to their home sites from either upstream or downstream of their capture sites or even from other streams. However, none of the juveniles (n = 4) returned home, despite only being displaced 25–150 m away. These results indicated that the adult big‐headed turtles showed high fidelity to their home site and strong homing ability. In contrast, the juvenile turtles may show an opposite trend but further research is needed.     

Characterization of 11 microsatellite marker loci in the Malagasy big‐headed turtle (Erymnochelys madagascariensis)

The Malagasy big‐headed turtle (Erymnochelys madagascariensis) is the only Erymnochelys species living in lakes, rivers and watersheds of western Madagascar. This species is endangered due to over harvesting of natural populations for human consumption. Eleven nuclear microsatellite loci were isolated from a genomic DNA library derived from a free‐ranging Malagasy big‐headed turtle from the Beroboka Classified Forest, Madagascar. Population genetic parameters were estimated on 10 individuals sampled from Ampijoroa and Andranohobaka River, Madagascar, to determine marker utility and as preliminary baseline values to study future populations in these locations.     

Egg fertility among vasectomized and non‐vasectomized male resident Canada geese at the Wildlife Conservation Park/Bronx Zoo

In 1991, a vasectomy program was initiated at the Wildlife Conservation Park/Bronx Zoo to minimize the population growth of resident Canada geese (Branta canadensis). Sixty‐nine males were vasectomized over a 6‐year period. From 1994 to 1998, egg fertility was examined in females paired with vasectomized and non‐vasectomized geese. Of the 340 eggs laid by females paired with vasectomized males, 12% were fertile. In comparsion, of the 526 eggs laid by females paired with non‐vasectomized males, 90% were fertile. The vasectomy procedure was easier to perform on males captured during the breeding season than on those captured during molt owing to the enlarged size of the vas deferens. Where resident Canada goose populations are small and resources available, the implementation of a vasectomy program can be effective in reducing population growth. Zoo Biol 19:35–40, 2000. © 2000 Wiley‐Liss, Inc.     

Comparative study on the growth of juvenile Galapagos giant tortoises (Geochelone nigra) at the Charles Darwin Research Station (Galapagos Islands,Ecuador) and Zoo Zurich (Zurich,Switzerland)

In this study, the growth rates of a group of Galapagos giant tortoises raised in their natural habitat at the Charles Darwin Research Station (CDRS; Galapagos Islands, Ecuador) and a group of captive‐bred specimens (Zoo Zurich, Zurich, Switzerland) were compared for the first time. A great discrepancy in growth rates was observed after the first year. When the animals were 4 years old, the carapace in the Zurich specimens was approximately twice as long as that in the CDRS tortoises, and the Zurich animals weighed approximately 10 times more than the CDRS animals. The zoo diet was modified by a reduction in nutrients and an increase in fiber to produce a more natural growth rate. Zoo Biol 23:177‐183, 2004. © 2004 Wiley‐Liss, Inc.     

Successful care and propagation of the endangered amargosa vole (Microtus californicus scirpensis) in captivity

The Amargosa vole (Microtus californicus scirpensis) is a highlyendangered rodent endemic to a small stretch of the California portion of the Amargosa River basin in Inyo County's Mojave Desert. Although the Amargosa vole has survived in this naturally fragmented ecosystem for thousands of years, recent habitat degradation due to land development, water drainage, and marsh exploitation has further isolated the species and reduced its available habitat. As part of a conservation effort to preserve the species, a captive breeding population was established in 2014 to serve as an insurance colony and as a source of individuals to release into the wild as restored habitat becomes available. As this is the only captive colony for this species, there is little published information about appropriate care and husbandry for the Amargosa vole. Here we provide information about behavior, diet, reproduction, drug sensitivities, and diseases that affect successful captive care. We also provide recommendations for housing and disease management to preserve natural behaviors and defenses in captive‐born animals.     

Breeding history and husbandry of the Raggiana Bird-of-paradise (Paradisaea raggiana)

The Raggiana Bird-of-paradise (Paradisaea raggiana) has been held by the San Diego Zoo for more than 50 years, but the population remained in low numbers until the mid-1990s. A previous article published in 1997 documented the beginning of the rise in the population; however, no new information has been published since that time. Over the past 25 years, behavioral observations by animal staff have led to improvements in husbandry techniques, which includes artificial incubation of eggs and hand-rearing of chicks. The ability to simulate a lek with various housing arrangements, in which the males can display with each other, be given access to a female for copulation, and then be separated again has proven paramount for breeding success. Additionally, females are allowed mate choice, further mimicking natural behaviors observed by this species. The refinement of these methods has led to a greater number of fertile eggs as well as higher hatchability and survivability, which in turn has resulted in a significant increase in the captive population.     

Reproduction of varanid lizards (Reptilia: Squamata: Varanidae) at the Bronx Zoo

Captivity provides many opportunities for studying the reproductive biology of varanid lizards (Family: Varanidae; genus: Varanus). This article presents reproductive data for 12 varanid species maintained in captivity at the Bronx Zoo between 1977 and 2010. Five species, V. prasinus, V. beccarii, V. melinus, V. mertensi, and V. ornatus have successfully reproduced at the zoo, for which clutch, incubation, and hatchling data are presented, and compared with previously published values. Clutch, incubation, and hatchling measurements typically fell within the known ranges for each species, or represent minor range extensions. V. mertensi was the only species that reproduced seasonally (χ(2) = 9.061, P = 0.029). Five species multiclutched; individual V. mertensi and V. prasinus females produced as many as four clutches per year. The shortest intervals between successive clutches observed for V. kordensis (61 days), V. melinus (77 days), V. mertensi (51 days), and V. prasinus (68 days) represent the shortest known values for each species. Relative clutch mass (RCM) ranged from 0.187 to 0.437. A mean RCM of 0.370 ± 0.092 for V. prasinus is substantially higher than previously published values for the species. These results illustrate that when maintained under favorable conditions in captivity, some varanids are capable of remarkably high fecundities, rapid reproductive turnover rates, and sizeable maternal investments. Periodicals, Inc.     

Introducing an innovative semi‐captive environment for the Philippine tarsier (Tarsius syrichta)

In response to demands for research, captive breeding, and tourism, a semi‐captive environment was created for the Philippine tarsiers (Tarsius syrichta) in Corella, Bohol, Philippines. The 7600‐m² enclosure was continuous with the surrounding habitat, and utilized a unique predator control fence design and a lighting system to attract nocturnal insects. During 2 years of observation, the locations of over 500 tarsier sleeping sites were recorded. Tarsiers were found to prefer dense, low‐level vegetation in secondary forests, with perching sites averaging 2 m above the ground. Up to 10 tarsiers were observed within the enclosure at one time, which is a high density compared to densities based on home‐range estimates for wild tarsiers in the vicinity of the study site. In addition, the tarsiers were observed to be more social than previously reported. Zoo Biol 24:101–109, 2005. © 2005 Wiley‐Liss, Inc.     

Breeding biology of Orange‐breasted (Harpactes oreskios) and Red‐headed (H. erythrocephalus) trogons in Khao Yai National Park,Thailand

ABSTRACT As tropical habitats continue to be cleared or degraded, obtaining basic information about the ecology of birds in intact habitats is essential for understanding their life histories. We studied the breeding biology of Orange‐breasted Trogons (Harpactes oreskios) and Red‐headed Trogons (H. erythrocephalus) in Khao Yai National Park in Thailand from 2003 to 2009. Nests were in excavated cavities in well‐rotted stumps or other tree parts. Mean cavity heights were 2.1 m (N= 19) for Orange‐breasted Trogons and 2.0 m (N= 49) for Red‐headed Trogons. Eggs were laid every other day. For Orange‐breasted Trogons, the mean clutch size was 2.4 ± 0.1 (SE) eggs (N= 17); incubation periods for two nests were 17 and 18 d, respectively, and the nestling period ranged from 12 to at least 14 d (N= 4). For Red‐headed Trogons, the mean clutch size was 2.6 ± 0.1 eggs (N= 48), the mean incubation period was 18 d (N= 9), and the mean nestling period was 13.4 d (N= 5). In both species, both males and females excavated nest sites, incubated eggs, and brooded and provisioned nestlings. Only females incubated and brooded at night, and males provisioned nestlings more than females. Breeding seasons lasted from January to March for Orange‐breasted Trogons, and from late February to July for Red‐headed Trogons. Mayfield estimates of nest success were 8% and 9% for Orange‐breasted and Red‐headed trogons, respectively. Unusual for cavity nesters, nest failure due to predation was high and nestling periods short. The low nesting success is typical of many other tropical species, but considerably lower than reported for some Neotropical trogons, possibly due to the unenclosed structure of the nests of these Asian trogons.     

Captive breeding for reintroduction: influence of management practices and biological factors on survival of captive kaki (black stilt)

An important component of the restoration strategy for the critically endangered kaki or black stilt (Himantopus novaezelandiae) is captive breeding for release. Since 1981 1,879 eggs were collected from wild and captive pairs, with birds laying up to four clutches. Eggs were incubated artificially and most chicks reared by hand until released as juveniles (about 60 days) or sub‐adults (9–10 months). Because survival in captivity is a significant determinant of the number of birds available for release, we wished to identify sources of variation in mortality to assess potential impacts of management on productivity. Hatchability was 78% for captive‐laid eggs and 91% for wild‐laid eggs. Survival of hatched eggs was 82% by 10 months of age for both wild and captive birds. Most egg mortality occurred early in incubation and around hatching: the timing of mortality was unaffected by whether birds were captive or wild, hybrid or pure kaki, or when eggs were laid. Heavier hatchlings showed higher initial survival, as did chicks from wild parents. Hatchlings from fourth‐laid eggs showed lowest survival, even though hatchling mass tended to increase with hatch order. Survival of chicks subjected to major health interventions was 69% after 4 months. No differences in survival were found between different genders, hybrids and pure kaki, hand‐reared or parent‐reared birds, chicks hatching early or late in the season, different seasons, different‐sized groups of chicks, chicks reared in different brooders, juveniles kept in different aviaries, and chicks from subsequent clutches. Birds subjected to minor health interventions were equally likely to survive as healthy chicks (82%). Survival was high despite aggressive management (quadruple clutching and collecting late in the season). Differences between captive and wild birds suggest further improvements could be made to captive diet. Wide variation in hatchability between parent pairs substantiates the practice of breaking up poorly performing pairs. Zoo Biol 0:1–16, 2005. © 2005 Wiley‐Liss, Inc.     

Captive Husbandry and Socialization of the Red‐Billed Chough (Pyrrhocorax pyrrhocorax)

Since the 1970s, Paradise Park Wildlife Sanctuary in Cornwall, United Kingdom, has built up a captive flock of red‐billed choughs Pyrrhocorax pyrrhocorax and over 30 years has developed successful methods of keeping, breeding, and appropriately socializing them in captivity. A total of 77 nests reached the egg stage with 27 nests producing at least one young and 48 young fledging in total. Several components are important in achieving successful breeding and socialization. Provision of live food, especially ant's eggs and small mealworms and crickets, in the first days after hatching is essential, improving the condition of adults and survival of nestlings. Situating aviaries in quiet areas, away from public view, is important. Socialization in family groups during the winter months and allowing choughs to choose partners induces better compatibility. Introduction of nest cameras greatly improved young survival through early identification of health problems enabling treatment of young between hatching and 10‐days old, when mortality is otherwise highest, and enabling precautionary medication shortly after hatching. We show that clutch size increases significantly with female age and that direct intervention such as artificial egg incubation and hand rearing can be successful and worthwhile, but its requirement is reduced by closer monitoring. Red‐billed choughs provide a good model species to further develop captive management and release techniques that can then be applied to critically endangered species that show similar social and long‐learning behaviors. Captive breeding programs can play an important role in such work through provision of suitable birds and supporting avicultural expertise. Zoo Biol. 31:725‐735, 2012. © 2012 Wiley Periodicals, Inc.     

A Retrospective Study of Mortality in Varanid Lizards (Reptilia:Squamata:Varanidae) at the Bronx Zoo: Implications for Husbandry and Reproductive Management in Zoos

Varanid lizards have been maintained in zoological parks for more than a century, yet few studies to date have attempted to pinpoint significant health issues affecting their management or areas of captive husbandry that are in need of improvement. In an effort to identify and better understand some of the husbandry‐related challenges and health issues specifically affecting varanids in zoos, this study examined mortality in 16 species maintained at the Bronx Zoo between 1968 and 2009. Out of 108 records reviewed, complete necropsy reports were available for 85 individuals. Infection‐related processes including bacterial (15.3%), protozoal (12.9%), nematode (9.4%), and fungal (3.5%) infections accounted for the greatest number of deaths (47.1%). Noninfectious diseases including female reproductive disorders (7.1%), neoplasia (7.1%), gout (10.8%), and hemipenal prolapse (1.3%) accounted for 29.4% of deaths. Multiple disease agents were responsible for 5.9% of deaths, and a cause for death could not be determined for 17.7% of individuals. Reproductive complications accounted for 11.5% of female deaths, but were identified in 23.1% of females. Although not necessarily the cause for death, gout was present in 18.8% of individuals. Differences in mortality between species, genders, and origin (captive‐bred vs. wild‐caught) were also evaluated. The results of this study corroborate earlier findings that identify bacterial infections, neoplasia, female reproductive disorders, gout, and endoparasitism as major sources of mortality in captive varanids. In light of these results, we discuss potential etiologies and offer recommendations for improving captive management practices in zoos. Zoo Biol. 32:152–162, 2013. © 2012 Wiley Periodicals, Inc.     

Mitigating Chinese–Indian rhesus macaque (Macaca mulatta) hybridity at the California National Primate Research Center (CNPRC)

The effectiveness of abating hybridity in a rhesus breeding colony was evaluated. STR data from the 2006 to 2015 newborns were analyzed. Hybridity decreased over successive years. Birth cohorts retained high genetic variability without signs of inbreeding and differentiation. Hybridity was minimized without compromising overall genetic variability.     

The captive husbandry and reproduction of the pink-eared turtle (Emydura victoriae) at Perth Zoo

In 1997, Perth Zoo acquired six pink-eared turtles (Emydura victoriae) from the wild for display in the reptile facility. There is very little documented information on pink-eared turtles in captivity. This article looks at the reproductive biology, ecology, behavior, diet, and captive husbandry of the species. Eight clutches of eggs were documented over a 2-year period with an average clutch size of 10 eggs. Egg size was recorded with three clutches incubated to hatching. Ten hatchlings were maintained for a growth and development study. Measurements of weight, carapace length, width, height, and plastron length were recorded weekly for about 12 months, and then monthly for approximately 2 years. The data were analyzed and showed positive growth curves in all animals. Sexual dimorphism was observed after 20 weeks and sexual maturity in males observed after 2 years.     

Body size development of captive and free‐ranging Leopard tortoises (Geochelone pardalis)

The growth and weight development of Leopard tortoise hatchings (Geochelone pardalis) kept at the Al Wabra Wildlife Preservation (AWWP), Qatar, was observed for more than four years, and compared to data in literature for free‐ranging animals on body weight or carapace measurements. The results document a distinctively faster growth in the captive animals. Indications for the same phenomenon in other tortoise species (Galapagos giant tortoises, G. nigra; Spur‐thighed tortoises, Testudo graeca; Desert tortoises, Gopherus agassizi) were found in the literature. The cause of the high growth rate most likely is the constant provision with highly digestible food of low fiber content. Increased growth rates are suspected to have negative consequences such as obesity, high mortality, gastrointestinal illnesses, renal diseases, “pyramiding,” fibrous osteodystrophy or metabolic bone disease. The apparently widespread occurrence of high growth rates in intensively managed tortoises underlines how easily ectothermic animals can be oversupplemented with nutrients. Zoo Biol 29:517–525, 2010. © 2009 Wiley‐Liss, Inc.     

Reproductive biology and ecology of white‐winged trumpeters (Psophia leucoptera) and recommendations for the breeding of captive trumpeters

The reproductive biology and ecology of a wild population of white‐winged trumpeters (Psophia leucoptera) were studied in southeastern Peru from 1983 to 1987. Because little information is available about any of the trumpeter species and because trumpeters have proven difficult to breed in captivity, information relevant to breeding and management of captive trumpeters is reported in this paper. White‐winged trumpeters lived in territorial social groups that ranged in size from four to 13 individuals. A typical territorial group contained three adult males, two adult females, and several sexually immature offspring, but smaller temporary groups sometimes formed for the duration of the breeding season. Only the dominant female contributed eggs to the clutch, and all adult males in the group competed to obtain copulations with her. Eggs were laid in elevated nesting cavities and no nest was constructed. The average clutch size was three eggs and incubation was not begun until the final egg was laid. The dominant male and female shared most of the incubation duties, but subordinate males covered approximately 15% of the incubation shifts. Eggs hatched approximately 27 days after incubation was begun and chicks left the nesting cavity the day after they hatched. Chicks were completely dependent on older birds to feed them for their first 3 weeks and then gradually began to feed themselves more and more food. The subordinate adult males fed chicks the most food, the dominant male and female and older offspring fed chicks an intermediate amount, and the subordinate adult female fed chicks the least. Young chicks behaved aggressively toward each other but were separated by adults before they injured each other. If at least one chick from the clutch survived, trumpeters did not breed again until the beginning of the next breeding season the following year. Zoo Biol 19:65–84, 2000. © 2000 Wiley‐Liss, Inc.     

A lotic‐breeding salamander (Hynobius kimurae) modifies physiological and morphological traits during wintering

Unlike other migratory salamanders, Hynobius kimurae moves to aquatic hibernacula during fall. Does submergence into water during fall induce changes in physiological and morphological traits? We investigated whether such changes occur in both sexes from the entrance into the water (November) to the exit from the water (May) in the laboratory. Mean duration of stay in the water was 21.7 weeks in males and 19.0 weeks in females. Spermiation began 13.8 weeks after the males entered the water. Sperm storage lasted for 6.3 weeks. Spawning occurred 18.3 weeks after the females entered the water. Cloacae swelled greatly soon after the sexes entered the water. In males after entering the water, tail shape changed from sticklike to finlike. Although physiological and morphological traits in other species change simultaneously in both the submergence into water and the onset of breeding activity only during spring, such changes occurred in individual H. kimurae firstly during fall (shortly after entering the water) and secondly during spring (shortly after awaking from hibernation). This difference suggests that these two‐step changes during a prolonged period (fall–spring) are concentrated in a short period of aquatic‐breeding activity during spring in other species with terrestrial hibernation and associated reproductive cycles.     

Predicting release success of captive‐reared loggerhead shrikes (Lanius ludovicianus) using pre‐release behavior

We assessed whether behavioral markers could be used to evaluate pair compatibility and predict pair bond success of captive‐reared San Clemente loggerhead shrikes (Lanius ludovicianus mearnsi) released into the wild. Potential breeding pairs of shrikes were introduced at the Zoological Society of San Diego's captive‐breeding facility and then moved to release cages located in suitable but unoccupied habitat. Courting pairs were affected negatively by the disturbance of translocation to a new location and generally needed a few days to reinitiate pair bonding in the release enclosures. We separated and returned pairs to captivity when intra‐pair aggression or cessation of all courtship behavior occurred; all other pairs were released into the wild. The rate of nest approaches was the best marker to predict a successful release into the wild (i.e., pairs that remained near the release site and attempted to breed). Additionally, all experienced breeding pairs (i.e., pairs with males and females with prior captive breeding experience) exhibiting nesting behavior were successful, although previous experience alone does not ensure post‐release breeding. Results from this study indicate the importance of assessing behaviors of individuals paired for population augmentation. In using behavioral cues, identifying pairs with a low probability of success is possible, and replacing these pairs with individuals that have a higher likelihood of post‐release success can occur. This strategy will be important to efficiently restore imperiled populations of endangered species while working within temporal and financial constraints. Zoo Biol 0:1–12, 2005. © 2005 Wiley‐Liss, Inc.