Common ringtail possum (Pseudocheirus peregrinus) as a management model for the Pseudocheiridae: Reproductive scope,behavior, and biomedical values on a browse-free diet

The purposes of this study were to determine 1) the life history characteristics of a captive colony of the arboreal folivore Pseudocheirus peregrinus maintained on a browse free diet under enhanced laboratory conditions, 2) the direction and magnitude of life history differences from wild population values, and 3) the feasibility of developing captive colonies of this and related species for conservation and research programs. Rates of reproduction, growth, and development; demographic trends; behavioral patterns pertinent to exhibition; and management and medical techniques are reported. Fecundity was 67% greater than that of wild populations and there was an approximate four-fold increase in the rate of offspring survival to sexual maturity. These trends were due largely to reduced post-pouch emergence mortality and the decay of reproductive seasonality. The results indicate that a properly designed “artificial” diet can support significantly enhanced reproduction in a trophic specialist. Other demographic, developmental, and behavioral measures found to be consistent with those reported from wild populations indicate that there was no significant life history distortion caused by the management regime. Empirical data are presented showing that the common ringtail is nocturnal, has low rates of activity, and has specific space and substrate preferences. These results suggest ways in which the animals' physical environment can be manipulated to improve exhibition. We conclude that the reproductive rates of other ringtail possum species might also be enhanced under comparable management conditions.     

Reproduction of the mongoose lemur (Lemur mongoz) in captivity

Responses to questionnaires sent to 20 institutions holding Lemur mongoz did not reveal which aspects of management or husbandry could account for reproductive failure in the captive population, but allowed some qualitative comparisons with data compiled for captive and wild animals. In general, reproduction has occurred initially among wild-caught specimens before tapering off, and rarely occurs in the captive F₁ generation. Data compiled by the International Species Inventory System and the International Zoo Yearbook revealed an aging captive population with no recent reproduction. No aspect of group composition, activity patterns, seasonal light regime, reproductive cycles, or diet could be linked to the lack of reproduction; and among lemurs subjected to the same conditions, some were known to reproduce while others did not. Lack of knowledge about this species and the threat of extinction for both captive and wild populations make an investigation of reproductive biology imperative. Recommendations for a research program are given.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

Use of behavioral measures to assess reproductive status in maned wolves (Chrysocyon brachyurus)

Captive breeding efforts of the threatened maned wolf (Chrysocyon brachyurus) have been plagued by a lack of reliable reproduction and a high rate of neonatal mortality. A particular problem for animal managers has been the ability to detect pregnancy in a noninvasive manner. Pseudopregnancies are common, and many staff hours are expended preparing for a birth that may not occur. The objectives of our study were to document changes in behavior during the breeding season in captive maned wolves in order to determine if behaviors other than sexual (i.e., copulation) could be used to distinguish nonbreeding from breeding pairs and, further, whether successful breeding pairs (young born) could be distinguished behaviorally from breeding pairs that did not produce young (pseudopregnant). Between 1988 and 1994, behavioral data were collected during the annual reproductive season from 52 maned wolf pairings (27 males, 26 females) housed at 17 North American institutions. Breeding animals showed significant increases in rates of affiliative behaviors (approach, friendly) and the amount of time spent in close association (social) during the estrous period, compared to pre- and post-estrous periods. In contrast, the behavior of nonbreeding pairs varied little throughout the breeding season. Discriminant function analysis (DFA) showed that several behavioral measurements during certain reproductive periods were useful in discriminating between nonbreeding and breeding animals (rates of friendly and social behavior for males, marking and social behavior for females). Unsuccessful (pseudopregnant) and successful breeding pairs could be further distinguished on the basis of agonistic and approach behavior frequencies (successful females showed higher rates of agonistic and lower rates of approach behavior during certain periods; successful males had higher rates of both behaviors). Discriminant equations for key behavioral measurements and examples of their practical application are presented. DFA provides animal managers with an effective, noninvasive technique for assessing the reproductive status of maned wolf pairs. © 1996 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.     

Reproductive biology of captive female Eurasian lynx, Lynx lynx

Studies on wild Eurasian lynx (Lynx lynx) have revealed variation in reproduction between areas, years and individuals. In order to explore potential causes for this variation other than food supply, we analysed data from captive lynx, which provide conditions with minimal environmental variation as all were fed ad libitum. Data from 37 individual female lynx were available from 20 zoos in Norway, Sweden, Finland, Switzerland and the Czech Republic. Data on 177 reproductive events (where a male was available to the female at mating time) are presented. Of these events, 85% resulted in litters being born. Average litter size was 1.95, with a variation from 1 to 4. The mean birth date was 26th May, and sex ratio was not significantly different from parity. The probability of reproduction was related to age, with fewer litters produced by the very young (2–3-year old), and no sign of a senescence effect. However, a clear effect of senescence on litter size was evident. The captive lynx did not have higher reproductive rates than wild lynx, indicating that either factors other than food supply are driving the variation in wild lynx reproduction, or that a factor such as stress may be causing additional variation in the captive population.     

Female reproduction bears no survival cost in captivity for gray mouse lemurs

The survival cost of reproduction has been revealed in many free‐ranging vertebrates. However, recent studies on captive populations failed to detect this cost. Theoretically, this lack of survival/reproduction trade‐off is expected when resources are not limiting, but these studies may have failed to detect the cost, as they may not have fully accounted for potential confounding effects, in particular interindividual heterogeneity. Here, we investigated the effects of current and past reproductive effort on later survival in captive females of a small primate, the gray mouse lemur. Survival analyses showed no cost of reproduction in females; and the pattern was even in the opposite direction: the higher the reproductive effort, the higher the chances of survival until the next reproductive event. These conclusions hold even while accounting for interindividual heterogeneity. In agreement with aforementioned studies on captive vertebrates, these results remind us that reproduction is expected to be traded against body maintenance and the survival prospect only when resources are so limiting that they induce an allocation trade‐off. Thus, the cost of reproduction has a major extrinsic component driven by environmental conditions.     

Life span,reproductive output,and reproductive opportunity in captive Goeldi's monkeys (Callimico goeldii)

In the absence of long‐term field studies, demographic and reproductive records from animals housed in zoos and research laboratories are a valuable tool for the study of life history variables relating to reproduction. In this study, we analyzed studbook records of more than 2,000 individuals born over a 40‐year period (1965–2004) to describe life history patterns of captive Goeldi's monkeys (Callimico goeldii) housed in North America and Europe. Using Kaplan–Meier survival analysis methods, we found the mean life span to be 5.5 years. The rate of infant mortality, defined as death before 30 days, was approximately 30%, with European animals being more likely to survive infancy than North American animals. When individuals surviving at least 1.5 years are considered, lifetime reproductive output averaged 3.5 offspring, yet more than one‐third of individuals did not produce any offspring. Using a smaller dataset of individuals with known pairing histories, we developed a measure of opportunity for reproduction (OFR), which represented the total time an individual was known to be housed with a potential mate. For both sexes, we found that the correlation between OFR and number of offspring produced was much higher than the correlation between life span and number of offspring produced. This result highlights the importance of taking into account an individual's OFR. As a whole, our findings help characterize the life histories of captive Goeldi's monkeys and emphasize the impact management practices may have on reproductive success. Zoo Biol 29:1–15, 2010. © 2009 Wiley‐Liss, Inc.     

Evidence for social enhancement of reproduction in two Eulemur species

Across the past 20 years, captive reproduction has declined steeply in mongoose lemurs (Eulemur mongoz) and has been only moderately successful in black lemurs (E. macaco). At the same time, reproduction has been so successful in brown lemurs (E. fulvus) that contraception has been used since 1987 to limit captive numbers. No obvious cause for the differential reproductive success has been identified. Our experience with a pair of unrelated mongoose lemurs at the Philadelphia Zoological Garden suggested that they reproduced in only those years when they were caged in close proximity to another nonreproductive, full-sibling pair of mongoose lemurs. Examination of the worldwide pattern of captive reproduction by Eulemur species during the past two decades revealed that female black and mongoose lemurs housed in institutions with either additional conspecific males or additional conspecific pairs had a higher rate of reproduction than those maintained as an isolated pair. Black lemurs also had higher rates of reproduction when additional conspecific females were present. No similar pattern was found for brown lemurs or for two comparable mammals, the pudu (Pudu pudu) and the okapi (Okapia johnstoni). The evidence presented for the black and mongoose lemurs supports the existence of the Allee effect in these two species, namely, that reproduction is enhanced by the presence of conspecifics. © 1996 Wiley-Liss, Inc.     

Use of positive reinforcement training in the management of species for reproduction

Positive reinforcement training holds great potential for enhancing the management of species for reproduction. This paper reviews a wide range of animal training activities and resultant benefits which could have application to captive reproduction programs. Recognized benefits fall into several categories. Basic animal care can be improved through voluntary cooperation by the animals with veterinary procedures and routine husbandry activities. The quality and quantity of physiological data collected for research can be improved through voluntary cooperation by the animal subjects with sample collection. Positive social interaction and reproductive behavior can be increased and aggressive behavior reduced through employment of a specialized training regime called cooperative feeding. Good success has been reported with special training programs to facilitate introduction of new members into primate social groups, while mixed results have been obtained in efforts to use training to enhance maternal skills. Finally, a discussion of both direct and indirect enhancement of psychological well-being through the use of positive reinforcement training is presented. While positive reinforcement training techniques will not be useful in every situation, information developed to date strongly suggests that these techniques should be given serious consideration when developing comprehensive programs for the management of species for reproduction. © 1994 Wiley-Liss, Inc.     

Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion

We examine and discuss evidence of contrasting differences in fertility patterns between captive and wild female chimpanzees, Pan troglodytes, as they age; in the wild females reproduce in their 40s, but captive studies suggest that menopause occurs around that time. Thus, despite the increased longevity generally observed in captive populations reproductive life span is shortened. We outline a hypothesis to explain the apparent differential pace of reproductive decline observed between wild and captive populations. The breeding schedules of captive primates may contribute to accelerated reproductive senescence because continuous cycling in captive animals results in early depletion of the ovarian stock and premature senescence. Available evidence supports the hypothesis that women with patterns of high oocyte loss experience earlier menopause. Chimpanzees in captivity live longer, and thus, similar to humans, they may experience follicular depletion that precedes death by many years. In captivity, chimpanzees typically have an early age at menarche and first birth, shorter interbirth intervals associated with short lactational periods as young mature faster, and nursery rearing, which allows mothers to begin cycling earlier. Variables typical of wild chimpanzee populations, including late age at menarche and first birth, long interbirth intervals associated with prolonged lactational periods, and a long period of female infertility after immigration, spare ovulations and may be responsible for the later age at reproductive termination. Finally, we describe and discuss the timing of specific reproductive landmarks that occur as female chimpanzees age, distinguishing between functional menopause (age at last birth) and operational menopause (end of cycling). Am. J. Primatol. 71:271–282, 2009. © 2008 Wiley‐Liss, Inc.     

Fitness consequences of ecological constraints and implications for the evolution of sociality in an incipiently social bee

Ecological constraints such as resource limitation, unfavourable weather conditions, and parasite pressure have long been considered some of the most important selective pressures for the evolution of sociality. In the present study, we assess the fitness consequences of these three ecological factors on reproductive success of solitary nests and social colonies in the socially polymorphic small carpenter bee, Ceratina australensis, based on 982 nests collected over four reproductive periods. Nest site limitation was predicted to decrease opportunities for independent nest initiation and increase the frequency of social nesting. Nest sites were not limiting in this species and the frequency of social nesting was consistent across the four brood‐rearing periods studied. Unfavourable weather was predicted to lower the frequency of female dispersal from their natal nests and to limit the brood‐rearing season; this would increase the frequency and fitness of social colonies. Daily temperature and precipitation accumulation varied between seasons but were not correlated with reproductive success in this bee. Increased parasite pressure is predicted to increase the frequency and fitness of social colonies because solitary bees must leave the nest unattended during foraging bouts and are less able to defend the nest against parasites. Severe parasitism by a chalcid wasp (Eurytoma sp.) resulted in low reproductive success and total nest failure in solitary nests. Social colonies had higher reproductive success and were never extirpated by parasites. The high frequency of solitary nests suggests that this is the optimal strategy. However, social colonies have a selective advantage over solitary nesting females during periods of extreme parasite pressure, and we suggest that social nesting represents a form of bet‐hedging against unpredictable fluctuations in parasite number. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 57–67.     

ORIGINAL ARTICLE: Medical and surgical management of reproductive neoplasia in two western lowland gorillas (Gorilla gorilla gorilla)

Background Reports of female reproductive tract neoplasia are infrequent in great apes. Methods Two captive‐born, female western lowland gorillas (Gorilla gorilla gorilla) housed at the North Carolina Zoological Park were diagnosed with reproductive neoplasia. Results The first gorilla had uterine endometrial thickening and uterine fibroids diagnosed during a routine annual examination. Subsequently, the animal underwent several uterine curettage procedures in an attempt to debulk the uterine mass. Biopsy results indicated uterine adenocarcinoma. The animal was treated with an ovariohysterectomy followed by a combination of megestrol acetate and medroxyprogesterone acetate. The second gorilla was diagnosed with squamous cell carcinoma of the vagina, cervix, and uterus after presenting for intermittent vaginal bleeding of 1‐month duration. This animal underwent palliative radiation therapy, receiving two rounds of radiation treatment 8 weeks apart. Conclusions The following report describes the diagnosis and management of the two cases.     

Reproductive seasonality in captive wild ruminants: implications for biogeographical adaptation,photoperiodic control,and life history

Many ruminant species show seasonal patterns of reproduction. Causes for this are widely debated, and include adaptations to seasonal availability of resources (with cues either from body condition in more tropical, or from photoperiodism in higher latitude habitats) and/or defence strategies against predators. Conclusions so far are limited to datasets with less than 30 species. Here, we use a dataset on 110 wild ruminant species kept in captivity in temperate‐zone zoos to describe their reproductive patterns quantitatively [determining the birth peak breadth (BPB) as the number of days in which 80% of all births occur]; then we link this pattern to various biological characteristics [latitude of origin, mother‐young‐relationship (hider/follower), proportion of grass in the natural diet (grazer/browser), sexual size dimorphism/mating system], and compare it with reports for free‐ranging animals. When comparing taxonomic subgroups, variance in BPB is highly correlated to the minimum, but not the maximum BPB, suggesting that a high BPB (i.e. an aseasonal reproductive pattern) is the plesiomorphic character in ruminants. Globally, latitude of natural origin is highly correlated to the BPB observed in captivity, supporting an overruling impact of photoperiodism on ruminant reproduction. Feeding type has no additional influence; the hider/follower dichotomy, associated with the anti‐predator strategy of ‘swamping’, has additional influence in the subset of African species only. Sexual size dimorphism and mating system are marginally associated with the BPB, potentially indicating a facilitation of polygamy under seasonal conditions. The difference in the calculated Julian date of conception between captive populations and that reported for free‐ranging ones corresponds to the one expected if absolute day length was the main trigger in highly seasonal species: calculated day length at the time of conception between free‐ranging and captive populations followed a y = x relationship. Only 11 species (all originating from lower latitudes) were considered to change their reproductive pattern distinctively between the wild and captivity, with 10 becoming less seasonal (but not aseasonal) in human care, indicating that seasonality observed in the wild was partly resource‐associated. Only one species (Antidorcas marsupialis) became more seasonal in captivity, presumably because resource availability in the wild overrules the innate photoperiodic response. Reproductive seasonality explains additional variance in the body mass–gestation period relationship, with more seasonal species having shorter gestation periods for their body size. We conclude that photoperiodism, and in particular absolute day length, are genetically fixed triggers for reproduction that may be malleable to some extent by body condition, and that plasticity in gestation length is an important facilitator that may partly explain the success of ruminant radiation to high latitudes. Evidence for an anti‐predator strategy involving seasonal reproduction is limited to African species. Reproductive seasonality following rainfall patterns may not be an adaptation to give birth in periods of high resource availability but an adaptation to allow conception only at times of good body condition.     

A comparative study of insect abundance and reproductive success of barn swallows Hirundo rustica in two urban habitats

Few studies have quantified the relative reproductive success of passerines in urban habitats. I studied food availability and reproductive success of barn swallows Hirundo rustica in two urban habitats during 2012–2015. Barn swallows breeding in the town center experienced lower insect densities than those in the town periphery. Lower food availability resulted in reduced feeding rates per capita, lower nestling body mass, longer nestling periods, longer inter‐clutch intervals, fewer first and second brood fledglings and a lower total number of fledglings produced during the breeding season in comparison to barn swallows breeding in the town periphery. I hypothesize that the lower intra‐specific competition for nest sites and fitness advantages linked to the solitary breeding in urban habitats balanced the apparent costs of reproduction in more urbanized habitats.     

Ultrasonography: an important tool in captive breeding management in elephants and rhinoceroses

Nearly two decades ago, modern wildlife medicine started to gradually use the advantages of the non-invasive ultrasonography, which was already well established in human and classical veterinary medicine. For more than one decade now, the application of imaging ultrasound for reproductive assessments and as a supportive tool during assisted reproduction procedures such as artificial insemination (AI) in elephants and rhinoceroses has dramatically improved the breeding success in captive breeding programmes. The opportunity for identifying potential breeding candidates on the basis of their reproductive health status is widely used for natural mating or for AI, today. The longitudinal sonographic monitoring of pathological processes on the internal female genital tract allowed the identification of pathogenetic causes for the rapid infertility development in older nulliparous females. The factors causing temporary infertility in captive male elephants and rhinoceroses were also identified by the use of ultrasound. Today, ultrasonography is the golden standard for reproductive assessments in megavertebrates such as elephants and rhinoceroses in captive management settings and also in the wild.     

Reproduction in the slender loris (Loris tardigradus malabaricus)

A breeding colony of slender lorises (Loris tardigradus malabaricus) was studied to obtain data for comparison with other prosimian species, to contribute reproductive information for improving management of captive lorises, and to resolve some uncertainties in the literature regarding reproduction in the slender loris. At the Duke University Primate Center, a female slender loris reached sexual maturity at approximately ten months of age and conceived at one year of age. The length of the estrous cycle was 29–40 days, with copulation occurring over two consecutive days during estrus. Gestation length was 166–169 days. Litter size for each six births was one. Conception did not occur during an immediate post-partum estrus, but four months after birth, resulting in a 9 1/2-month interbirth interval. There was no evidence of reproductive seasonality. Lactation lasted between five and seven months. Reproductive rates of slender lorises are among the lowest of primates less than 500 g. Differences in reproductive parameters may exist between different subspecies of slender lorises.     

Spatial segregation in the reproductive activity of Neotropical fish species as an indicator of the migratory trait

This study focused on the distribution of fish with high reproductive activity along a basin, using a 430 km stretch of the Cuiabá River in Brazil as a model. The main objective of this study was to identify those fish that migrate long distances for reproduction, among all the basin species. Thus, a set of working criteria are proposed to classify species according to their reproductive behaviour (i.e., reproductive activity and distribution). Samplings were performed in the Cuiabá River basin, encompassing several environments (river, channels and lakes) during the reproductive periods (between October and February), from 2000 to 2004. Species occurrence (presence and absence – proxy of distribution) across the basin and index of reproductive activity values were used as criteria to identify the species that perform long-distance longitudinal migrations for reproduction. The study confirmed the classification of long-distance longitudinal migration species; nonetheless, some species were not classified as described in the literature. The proposed sequential criteria have proven to be effective in the classification of long-distance longitudinal migrations species and certainly contribute to filling some existing knowledge gaps of reproductive traits. This classification is of fundamental importance in planning new dam projects, in decision making and in the development of management and conservation actions for the ichthyofauna.     

Population structure change of Salpa thompsoni from austral mid-summer to autumn

Changes in the population structure of Salpa thompsoni from austral mid-summer to autumn off the Adelie Coast, Antarctica, were examined using cluster analysis based on reproductive states. S. thompsoni was the dominant macrozooplankton species through the research periods although the abundance decreased markedly in autumn. In both summer and autumn we identified three geographically coherent subpopulations, which were considered to be either a mating swarm or physical aggregation. Many aggregate forms with an empty (dead) embryo were observed, and the ratio of newborn solitary forms decreased in autumn, indicating sexual reproduction of the salps was deactivated. The significant reduction in size of mature solitaries suggested that the capacity of asexual reproduction was also reduced in autumn. In addition to water temperature decline, the phytoplankton shortage (which was partly caused by high grazing pressure of S. thompsoni during summer) might be the factor causing decline in their own population size in autumn. Accepted: 25 May 1999