Captive breeding and infant mortality in Asian elephants: A comparison between twenty western zoos and three eastern elephant centers

Poor reproductive success compromises the long-term viability of captive Asian elephant populations. A questionnaire was designed to assess the importance of reproductive behavior and husbandry factors on breeding success. This was circulated to a number of institutions, zoos, and circuses in Asia, Europe, and North America, all of which kept Asian elephants. The aims were to compare Asian elephant breeding success in different institutions, establish possible causes for any differences, and make recommendations for improving the welfare and breeding success of the animals. The results showed that breeding success in most of the zoos was notably lower and the percentages of stillbirths and infant mortality were relatively higher when compared with those of the institutions in Asia. Female elephants in zoos appeared to reach sexual maturity and reproduce earlier than those in the Asian establishments. However, zoo elephants produced fewer young per female. The different facilities and husbandry methods used are described. Recommendations are made for both short- and long-term changes that could be used to modify existing practices to improve the welfare and breeding success of captive Asian elephants. Zoo Biol 17:311–332, 1998. © 1998 Wiley-Liss, Inc.     

Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in Southern India

To eliminate abnormal behaviors in leopards (Panthera pardus), such as stereotypic pacing, by utilizing environmental enrichment techniques, a proper understanding of their behavior in captive environments is required. Hence there is a need for animal welfare studies in Indian zoos. The activity budgets of 16 leopards were recorded across four southern Indian zoos: Thiruvananthapuram Zoo, Arignar Anna Zoological Park, Shri Chamarajendra Zoological Gardens, and the Guindy Children's Park. Of the 16 study animals, 14 were studied on‐exhibit on zoo holidays as well as on days with visitors present, and all 16 individuals were studied off‐exhibit on other days with visitors present. The 11 behaviors recorded were categorized into active, resting, and stereotypic behaviors. Leopards exhibited higher levels of activity in the on‐exhibit enclosures on days with no visitors. Feeding time influenced the behavioral repertoire of all 14 leopards studied on‐exhibit. Lower proportions of resting were exhibited during the hours before feeding. The proportion of active behaviors differed significantly across zoos. Stereotypic pacing levels were not influenced by the presence of visitors or by feeding time, but was significantly influenced by enclosure features. Higher levels of stereotypic pacing were exhibited in off‐exhibit than on‐exhibit enclosures. Our study shows that the behavior of captive leopards is influenced by enclosure type, feeding regime, and the presence of visitors. Zoo Biol 21:585–595, 2002. © 2002 Wiley‐Liss, Inc.     

Optimal conditions for breeding of captive humboldt penguins (Spheniscus humboldti): A survey of British zoos

We surveyed 16 British zoos and bird gardens to assess the optimal conditions for breeding of captive Humboldt penguins (Spheniscus humboldti). We obtained information on population, enclosure, and husbandry characteristics and related these variables to three measures of per capita breeding success, namely, per capita egg productivity, chick productivity, and hatching success (measured as the proportion of eggs laid that hatched). All three fitness measures increased with an increasing number of breeding pairs and total population size but were not related to population density. Once the effect of number of breeding pairs was removed statistically, chick productivity was found to be highest when nesting boxes were lined with sand and gravel instead of alternative substrata such as twigs or vegetation. Hatching success increased with increasing pool size and was highest in enclosures with concrete floors. Adult mortality in zoos was generally low and appeared related to the use of chlorine in freshwater pools and to the presence of other penguin species in Humboldt penguin displays. Several enclosure and husbandry parameters were not variable enough to assess their impact on reproduction of captive Humboldt penguins. Recommendations for optimising conditions for captive breeding of Humboldt penguins include keeping as large a population as possible in a concrete enclosure with a large pool area, while providing sand and gravel as nesting material. Bird density may be important but we did not detect detrimental effects on breeding for densities up to 0.25 birds m^–2. Adult mortality can be minimised by exhibiting Humboldt penguins in single‐species display and avoiding chlorination of pool water. An experimental approach is recommended to confirm the results of this correlational study. Zoo Biol 20:545–555, 2001. © 2002 Wiley‐Liss, Inc.     

Social and spatial relationships in captive southern white rhinoceros (Ceratotherium simum simum)

Although critical to the conservation of white rhinoceros, captive breeding has proven challenging because of the poor and irregular reproductive health of many captive rhinos, and social interactions may play a significant role. This research investigated the social and spatial relationships of two captive groups of southern white rhinoceros (Ceratotherium simum simum) by examining the frequency of companion changes, the number of space maintenance vocalizations made per hour by each reproductively mature female, and dominant/subordinate interactions. The observed captive rhinos did not change their companionships during the study. They exhibited space maintenance vocalizations and display greater than once per hour, particularly when feeding. Females housed with four calves on 0.033 km² exhibited space maintenance vocalizations more frequently (X±SE = 6.19±0.199/hr) than females housed with one calf and more space (0.06 km², X±SE = 0.55±0.182/hr) and females housed without calves and more space (0.65 km², X±SE = 1.90±0.086/hr). Wider separation of food piles and of females with young calves is suggested to reduce the interpreted spatial stress. The presence of a large number of rhinos in restricted captive space resulted in the formation of herds with dominance hierarchies that were enforced during competition for food and shade. The most subordinate rhino in each of the herds exhibited unusual behaviors such as dung‐kicking and nonestrus urine squirting, and neither has ever reproduced. Suppression of subordinate rhinos might lead to social stress that could negatively impact reproductive success. Zoo Biol 26:487–502, 2007. © 2007 Wiley‐Liss, Inc.     

A versatile enzyme immunoassay for the determination of progestogens in feces and serum

The ability of zoos to monitor the reproductive status of their animals can vastly improve the effectiveness of husbandry/management practices, and noninvasive methods such as fecal steroid analysis are the easiest to apply in a zoo setting. Furthermore, enzyme immunoassay (EIA) is preferred to radioimmunoassay (RIA) as the method of quantifying hormones because EIAs do not involve the use, storage, and disposal of radioactive materials. However, progesterone is excreted in the feces as predominantly unconjugated metabolites (progestogens) and, until recently, antibodies able to cross‐react with a variety of progestogens were used primarily in RIAs. An EIA using a broad‐spectrum progestogen antibody is described and applied to serum and/or fecal samples from female African elephants, black rhinoceros, white rhinoceros, okapi, and hippopotami. The clear progestogen profiles generated in these species suggest that the described EIA would be as versatile as the RIA using the same antibody and could be a practical and economical alternative to RIAs for monitoring gonadal function via progestogen analysis in zoo species. Zoo Biol 20:227–236, 2001. © 2001 Wiley‐Liss, Inc.     

Ape behavior in two alternating environments: comparing exhibit and short‐term holding areas

In many facilities, primates are voluntarily transferred between different enclosures on a daily basis to facilitate animal husbandry and exhibit maintenance. This procedure is particularly relevant in the management of great apes living in zoos, where the requirements of functional management must be balanced with the desire to maintain enriching and naturalistic exhibit enclosures that benefit ape residents and attract the visiting public. In these settings, examinations of ape behavior and welfare typically focus exclusively on activity in the primary exhibit area. However, physical, social and sensory experiences unique to each area may shape different patterns of behavior. In the current study, zoo‐living chimpanzees and gorillas were moved each day from exhibit areas to off‐exhibit holding areas for a short duration as a part of regular management procedures. Behavioral data indicated species‐specific reactions to the holding area, including increased aggression and self‐directed behavior by chimpanzees and increased activity and prosocial behavior among gorilla subjects. Both species showed more feeding‐foraging behavior while in the exhibit enclosure. Results suggest that holding areas may not meet all behavior needs of captive great apes and demonstrate the importance of including all components of the captive enclosure in comprehensive analyses of great ape behavior and welfare. Am. J. Primatol. 72:951–959, 2010. © 2010 Wiley‐Liss, Inc.     

Effects of environmental enrichment on reproduction

Although there have been few demonstrations of a direct empirical relationship between environmental enrichment and reproductive success in captive animals, indirect and anecdotal evidence indicates the importance of physical and temporal complexity for reproduction. We discuss three major mechanisms through which environmental enrichment that specifically increases the complexity of an animal's surroundings may influence reproductive physiology and behavior: developmental processes, modulation of stress and arousal, and modification of social interactions. In complex environments developing animals learn that performing active behavior produces appropriate functional outcomes. Learning to control their environment influences their ability to adapt to novel situations, which may profoundly influence their reproductive behavior as adults in breeding situations. Chronic stress may compromise reproductive physiology and behavior; enrichment reduces stress by providing increased opportunity for behavioral coping responses. However, some degree of acute stress may be beneficial for reproduction by maintaining an animal's level of responsiveness to socio-sexual stimuli necessary for sexual arousal and reproductive activation. Finally, environmental enrichment may influence reproductive success by stabilizing social groups, reducing aggression and increasing affiliative and play behaviors. It is concluded that multi-variate multi-institutional behavioral research in zoos will play an increasingly important role in the successful captive propagation of many species by closely examining relationships between environmental variables and reproductive potential of individual animals. © 1994 Wiley-Liss, Inc.     

Reproduction and monogamy in captive flock of greater flamingos (Phoenicopterus Roseus)

Due to the great number of greater flamingos in captivity and their long life span, studying their behavior and welfare might be useful to improve the husbandry and breeding of this species in zoos. This study aimed to investigate factors affecting the breeding activity of captive greater flamingos (Phoenicopterus roseus) from 2012 to 2016. To estimate reproductive success, the number of pairs, eggs laid, and hatchlings were recorded. In addition, information on age, egg-laying history of the partners, and pair composition was collected. An increase in the number of pairs, eggs, and hatchlings was reported over the years. For each breeding season, there were pairs who laid more than once, especially in 2014 and 2015. Approximately 50% of pairs were monogamous between consecutive years; however, the percentage dropped gradually when comparing nonconsecutive years. Senescence and previous experience seemed to affect the reproductive success of the study flamingos. In conclusion, different factors can influence the reproduction of greater flamingos in zoos. All these factors are related to nonhuman animal welfare and need to be considered in developing and improving management practices.     

Factors influencing reproductive success and litter size in captive island foxes

A severe decline of island foxes (Urocyon littoralis) on the northern Channel Islands in the 1990s prompted the National Park Service to begin a captive breeding program to increase their numbers. Using detailed records of all the fox pairs (N = 267) that were part of the program on San Miguel, Santa Rosa, and Santa Cruz Islands from its inception in 2000 through 2007, we identified factors influencing the breeding success of pairs in captivity in the interest of formulating strategies that could increase captive productivity. We compiled a database of variables including litter size, reproductive success, distance to nearest occupied pen during the breeding season, subspecies, exposure, female age, male age, age difference, female and male origin (wild vs. captive born), same versus different origin, years paired, previous reproductive success by the pair, previous reproductive success by the female, mate aggression-related injuries, male previous involvement in a pair with mate aggression, and female previous involvement in a pair with mate aggression. We used multiple linear regression to identify factors predictive of litter size, and logistic regression to predict the probability of reproductive success. A larger inter-pen distance, older male age, less exposure, and a smaller intra-pair age difference positively affected litter size. The probabilities of reproductive success increased with fewer years paired and less exposure. Comparatively, pairs with wild born females (vs. captive born females), and previously successful pairs (vs. previously unsuccessful and new pairs) were most likely to be successful. These results indicate that the optimal situation was to pair wild-caught females with older males in sheltered pens that were as far from other pens as possible, to maintain successful pairs and repair unsuccessful ones. Published 2013. This article is a U.S. Government work and is in the public domain in the USA.     

Research in zoos: a growth area in conservation

Despite early menageries being the source of much useful biological information on anatomy and taxonomy, it is only more recently that the potential for research in zoos has been recongnized. Collections of captive animals are unique and irreplaceable resources for conservation; but without research in zoological parks, progress in conservation science would diminish. There is a flow of information from zoo researchers to field scientists that assists in providing new insights into species biology. Reciprocally, data collected in the field enhance efforts in captive breeding. This paper summarizes the new research initiatives undertaken in zoos, e.g., in the fields of reproductive and genetic technologies, and highlights their significance for conservation and management of threatened species. It is evident that zoo research has a vital role in linking in situ and ex situ conservation. This role needs to be expanded and developed to meet the challenge posed by expanding human and declining wildlife populations and ecosystems.     

Blood‐feeding ecology of mosquitoes in zoos

To determine if the unique host assemblages in zoos influence blood‐feeding by mosquitoes (Diptera: Culicidae), a sampling programme was conducted in Greenville and Riverbanks Zoos, South Carolina, U.S.A., from April 2009 to October 2010. A total of 4355 female mosquitoes of 14 species were collected, of which 106 individuals of nine species were blood‐fed. The most common taxa were Aedes albopictus (Skuse), Aedes triseriatus (Say), Anopheles punctipennis (Say), Culex erraticus (Dyar & Knab), Culex pipiens complex (L.) and Culex restuans (Theobald). Molecular analyses (cytochrome b) of bloodmeals revealed that mosquitoes fed on captive animals, humans and wildlife, and took mixed bloodmeals. Host species included one amphibian, 16 birds, 10 mammals (including humans) and two reptiles. Minimum dispersal distances after feeding on captive hosts ranged from 15.5 m to 327.0 m. Mosquito–host associations generally conformed to previous accounts, indicating that mosquito behaviour inside zoos reflects that outside zoos. However, novel variation in host use, including new, exotic host records, warrants further investigation. Zoos, thus, can be used as experiment environments in which to study mosquito behaviour, and the findings extrapolated to non‐zoo areas, while providing medical and veterinary benefits to zoo animals, employees and patrons.     

Breeding behavior in a flock of Chilean flamingos (Phoenicopterus chilensis) at Dublin zoo

The breeding behavior of a flock of Chilean flamingos was observed over a 3‐month period during the peak of breeding activity. This species’ habitat is becoming increasingly vulnerable, and concern has been raised over a decline in wild stocks numbers in the past two decades. Breeding programs in zoos have been established, but with limited success because little is known about the precise criteria and conditions required for breeding these animals. This study was undertaken to gain insight into the breeding behavior of captive Chilean flamingos. A catalogue of mating rituals, nest acquisition and defense, and egg incubation behavior was obtained. The results suggest that new additions to the colony may trigger breeding in the subsequent year and that rainfall has little effect on captive reproductive success. Individually identifiable flamingos were followed throughout the breeding season and detailed quantitative data on their nesting, copulation, and social interactions were obtained. Zoo Biol 19:227–237, 2000. © 2000 Wiley‐Liss, Inc.     

Serum and fecal steroid analysis of ovulation,pregnancy, and parturition in the black rhinoceros (Diceros bicornis)

Studies were conducted to determine: (1) if fecal hormone metabolite concentrations correlated with serum estrogen and progesterone concentrations, follicular activity and reproductive behavior in the black rhinoceros (Diceros bicornis) and (2) if threshold values of respective fecal metabolite concentrations correlated with pregnancy. Blood and fecal samples were collected, in conjunction with transrectal ultrasound and behavior observations, for an 18-month period from one black rhinoceros female. Subsequently, serial fecal samples were collected from 13 females in 10 zoos. Quantitative analysis of serum progesterone (P₄) and estradiol (E₂) was performed by radioimmunoassay (RIA): analysis of fecal estrogen metabolites (E) and fecal progesterone metabolites (P) were performed by enzyme immunoassay (EIA). Serum P₂ concentrations identified two luteal phase patterns and two nadirs which corresponded with behavioral estrus. Fecal E patterns indicated a sharp peak which corresponded with breeding. concentrations of fecal P illustrated identifiable nadirs and several peaks which corresponded to serum P₄ nadirs and luteal phases. Serum P₄ concentrations were not different between the luteal phase and pregnancy. Fecal P concentrations started to rise above luteal phase concentrations approximately 150 days postbreeding and remained elevated until immediately before parturition. Serum E₂ and fecal E concentrations rose and subsequently declined after parturition. In the fecal samples from seven pregnant females, fecal P concentrations were similarly elevated compared to six nonpregnant females. Results indicated that fecal steroid metabolites accurately reflected serum steroid hormone concentrations and that the measurement of P and E concentrations permitted the characterization of the estrous cycle, the diagnosis of pregnancy, and the onset of parturition. Zoo Biol 16:121–132, 1997. © 1997 Wiley-Liss, Inc.     

Observations on reproduction,hormones, copulatory behavior,and neonatal mortality in captive Lemur mongoz (Mongoose lemur)

This study examines correlates of reproduction in Lemur mongoz, an endangered prosimian primate with a history of poor captive reproduction. Male testicular growth and regression were quantified via testicular indices (TI). Although TIs could be used to predict male breeding condition, they were not indicators of ability to sire offspring. Serum estradiol (E₂) and progesterone (P) concentrations, along with vaginal cytology, were used to monitor female reproductive cyclicity. E₂ and P profiles showed no abnormalities. An elevation of E₂ with low P, approximately one estrous cycle length (31.4 days) prior to the onset of fertile cycles, was consistent with the phenomenon of ‘pseudoestrus’ observed in other lemur species. The copulatory pattern, consisting of thrusting, multiple intromissions, single or multiple ejaculations, and no copulatory lock, was more complex than expected for an animal with a supposedly monogamous mating system. The preference for natural arboreal substrata during copulation suggests that enclosure furnishings may influence copulatory behavior. A 30% neonatal mortality rate tempered recent success in breeding L. mongoz at the Duke University Primate Center (DUPC). Although infant sex and parity of the mother were not predictive of neonatal mortality, mother's natal status was, with captive-born females having a 67% infant mortality rate, compared with 15% in wild-caught females. Based on these observations, a number of factors, including housing, behavior, and photoperiod, may be relevant to successful captive propagation of L. mongoz. © 1992 Wiley-Liss, Inc.     

Variation in nature: its implications for zoo elephant management

Despite many advances in animal care and welfare over the past few decades, zoos have been criticized recently for the quality of their elephant management programs. More specifically, critics have argued that elephants live miserable lives in captivity and thus should not be kept in zoos. Poor health and reproductive success, they say, are the result of the combined impact of: a lack of exercise; exposure to cold temperatures and disease; and stress due to the use of “brutal” training techniques, chaining and inappropriate social environments. Everyone, including zoo professionals, seems to agree that improvements in zoo elephant management are necessary and appropriate. However, there is considerable disagreement on how to proceed and little information on which to base such decisions. One tactic that the critics have adopted in their efforts to promote change is their frequent reference to “nature” as a yardstick for gauging the adequacy of zoo animal management and care. An argument is made that direct zoo–wild comparisons are of questionable utility and may be invalid from a scientific perspective. Some critics talk about “nature” as if it represented a fixed set of rules by which captive managers must either abide by or risk diminishing the health and welfare of their charges. However, many aspects of elephant natural history vary greatly depending on prevailing environmental conditions and elephants may be much more flexible than many critics are giving them credit for. Thus, although zoo animal managers should look to nature for clues about how to best care for captive elephants, they should not feel constrained by them. This revelation is not intended as an excuse for poor elephant management or to support the status quo. On the contrary, a better approach is to develop realistic and biologically meaningful metrics that reflect the quality of elephant care and welfare and to use them to measure the success of evolving zoo elephant programs. Zoo Biol 25:161–171, 2006. © 2006 Wiley‐Liss, Inc.     

Preference for structural environmental features in captive lowland gorillas (Gorilla gorilla gorilla)

Increased interest in the behavioral effects of captive environments and advances in zoo design have resulted in a proliferation of “naturalistic” animal habitats. Although scientists have demonstrated that such exhibits have some positive effects on behavior, very little is known about the complex relationships between these specialized environments and behavior. This study sought to determine preferences for structural environmental features, such as slope and trees, exhibited by captive lowland gorillas (Gorilla gorilla gorilla). An average of 496 location scans were collected on each of 23 gorillas, housed in 6 groups. The results indicate that enclosure usage was significantly associated with the features of slope, nearness to holding facility, and presence of environmental components additional to substrate (e.g., tree or rock). In particular, areas with flat ground that were near the holding building and that included at least one component additional to substrate were preferred by all animals. © 1993 Wiley-Liss, Inc.     

Management parameters affecting the reproductive potential of captive,female black rhinoceros,Diceros bicornis

With deterioration of the wild population over the last two decades, captive reproduction of black rhinoceros has become a high priority for zoological gardens. Several reproductive parameters of female black rhinoceros were analyzed with data from the international studbook, and compared to data from field studies. These analyses yielded comparisons for ages of females at first calving, length of birth intervals, and span of reproductive life. The implications for rhino productivity are discussed, and some suggestions for increasing productivity are presented. © 1992 Wiley-Liss, Inc.     

Oceanographic drivers of offspring abundance may increase or decrease reproductive variance in a temperate marine fish

In species that reproduce into uncertain environments, the relationship between mean reproductive success (the abundance of new recruits) and the variance in reproductive success (whether adults contribute disproportionally more offspring) may not be straightforward because of stochastic environmental processes that create high variance in reproductive success among adults. In this study, we investigated the relationships between oceanography, reproductive success and reproductive variance in the black rockfish, Sebastes melanops, a long‐lived temperate reef fish with pelagic larvae. We quantified black rockfish recruitment, genetic diversity and growth rates from otolith microstructure over 5 years (2005–2009) during which oceanographic conditions differed. We used cross‐correlations to determine windows of time during which oceanographic variables were significantly correlated with the resulting abundance or genetic diversity of recruits. We found that warmer ocean temperatures were positively correlated with the abundance of recruits, as well as the effective number of breeders. In contrast, the strength of coastal upwelling during settlement was positively correlated with the annual abundance of new recruits, but was negatively correlated with the effective number of breeders. Larval growth rates were explained substantially more by temperature than by upwelling and suggested that temperature affected survival through growth, while upwelling affected survival through transport. Our results indicated that cold ocean temperatures and intense upwelling caused sweepstakes‐like processes to operate on black rockfish populations, despite high abundances of recruits. We propose that a decoupling of the mean and variance in reproductive success may be characteristic of organisms that reproduce into uncertain environments.