Chemical contraceptive impacts on cyclic progesterone and sexual behavior in zoo-housed Western lowland gorillas.

For regularly cycling primates in captivity, chemical contraceptives can be used to reduce the likelihood of unintentional offspring, but the effects on cyclic progesterone and sexual behavior have not been well studied in gorillas (Gorilla gorilla gorilla). As zoos are invested in maintaining naturalistic behaviors and physiology, this is an important aspect of gorilla physical and mental health. We examined how exposure to combination and progestin-only oral birth control pills altered cyclic progesterone and timing of sexual behaviors in four female gorillas at four institutions compared to cycling controls. Hormonal data were collected using fecal steroid metabolites as detected by enzyme immunoassay. Behavioral data were collected via one-zero sampling done by keeper staff. All methods of oral contraceptive eliminated the ovarian cycle, with fecal progestogens being maintained below baselines in cycling control individuals. There was also no evidence of any cyclic patterning in endogenous progesterone, suggesting that the methods tested do not allow for detection of a recovery of endogenous progesterone during a short no-pill period. We also found that the oral contraceptives altered the timing of behavioral displays when compared to cycling control individuals but was not directly related to any fluctuations in endogenous progesterone. This study reveals a need for additional research on contraceptive use in gorillas and reinforces that sexual behavior in gorillas is both hormonally and socially mediated.

Comparing Data Collection Tools for Zoo Management Decision-Making: A Case Study Examining Behavioral Measures of Humboldt Penguin Bond Strength.

Systematic data collection has become increasingly important in zoos as it facilitates evidence-based decision-making. Here, we describe the results of a two-year study on exhibit use and pair-bonding in a colony of Humboldt penguins. We used two different data collection apps to evaluate their effectiveness and suitability for evaluating pair-bond strength. Data were collected using instantaneous scan sampling and all-occurrence sampling 2-3 times per week for 2 years for a total of nearly 240 h of observation (19 h with one system and 219 h with the other system). The activity patterns (in particular, time spent in the water) differed amongst penguins and between the two data collection tools. Patterns of courtship-related behaviors varied tremendously across individuals. The longer pairs had been bonded, the more time they spent in close proximity. We highlight two important considerations for institutions aiming to collect such systematic data. First, it is critical to interpret all findings in context by incorporating husbandry details and keeper insights to highlight explanations that may not be readily apparent from the data. Second, one must explore all aspects of any data collection system before committing to its use-system setup, ease of data collection, format and accessibility of exported data. Not doing so may negate the value of systematic data collection by limiting the use and interpretability of the data.

Cortisol metabolites vary with environmental conditions, predation risk, and human shields in a wild primate, Cercopithecus albogularis.

Environmental challenges are often associated with physiological changes in wildlife that allow animals to maintain homeostasis. Among these, scarcity in resources, and risks from predators, competitors, and humans can all result in psychological and physiological stress. Yet, for habituated species, it is not clear whether this relationship with humans still holds to a lesser degree or is outweighed by the benefits of human presence - such as serving as a buffer from competitors or predators. We investigated how human presence and environmental challenges such as resource availability, weather, predation, and competition may be associated with variation in fecal cortisol metabolite levels (FCMs) in a group of samango monkeys (Cercopithecus albogularis) in the Soutpansberg Mountains, South Africa. FCMs can often broadly track environmental challenges and perturbations. Initially, we employed an exploratory analysis comparing candidate models representing biological hypotheses and found that those incorporating information on human presence had less weight than models for food availability, thermoregulation, and water scarcity. When we examined a subset of the data that included information on intergroup competition and predator alarm calls, we found that FCMs were higher on the day following potential predator encounters but not competitive interactions. As observer numbers increased, responses to predators flattened, indicating that the presence of several humans might deter predators and/or affect samangos' perception of danger - yet we could not distinguish between these possibilities. Together, these results suggest that ecological perturbations track with FCMs in this study population and challenge long-held assumptions that human presence has negligible effects on habituated study animals.

Characterization of Cycling in a Hoolock Gibbon (Hoolock leuconedys).

Here we examine the patterns of reproductive hormones (progesterone and estrone-3 glucuronide, or E1G) in one female hoolock gibbon (Hoolock leuconedys) housed at the Gibbon Conservation Center, throughout the maturation period. Three hundred forty-five fecal samples were collected from the individual over a 5-year period (2012-2017) beginning at the age of 6 years and ending at the age of 11. The average measured progesterone concentration increased from 19.572 ± 1.706 ng/g feces in 2012 to 107.922 ± 12.094 ng/g feces in 2016/17 (p < 0.00001). The average measured estrogen value increased from 1.234 ± 0.063 ng/g feces in 2012 to 2.783 ± 0.274 ng/g feces in 2016/17 (p < 0.00001). This was accompanied by the emergence of a clear hormonal cycling pattern in the 2016/17 samples that was absent in all earlier samples. These data are consistent with the known sexual maturation period for other gibbon species, which typically occurs between the ages of 6 and 8 but shows some variation. To our knowledge, this is the first hormonal study and first data on cycle length for a hoolock gibbon.

Behavioral Implications of the Complete Absence of Guests on a Zoo-Housed Gorilla Troop.

Research conducted on the effects that zoo visitors have on primate behavior has yielded inconsistent patterns. This study aims to contribute to the growing body of literature regarding visitor effects on zoo-housed primate's activity budgets, with the purpose of quantifying the behavioral variability under two conditions: guest presence and guest absence. Due to the COVID-19 pandemic, many zoos were closed to the public for varying lengths of time. The Buffalo Zoo was closed to guests for an 18-week period including the summer of 2020, which allowed us to effectively control for zoo guest presence. This case report compares data on the zoo's gorilla troop from the same time period in 2019. We found inconsistent results, similar to prior studies conducted with zoo-housed gorilla troops. Most gorillas were observed foraging less and exhibiting more inactivity in 2020, whereas the adult male silverback showed the opposite pattern. Abnormal or undesirable behaviors were performed less frequently when guests were absent however, these differences were not significant. We encourage others to compare behavior patterns during the pandemic shutdown to add to our knowledge base of visitor effects. We suggest that researchers do not try and generalize their individual and troop results to the entire population of gorillas in managed care, as both intrinsic and extrinsic factors contribute to individual differences in behavioral response.

Anthropogenic influences on primate antipredator behavior and implications for research and conservation.

Predation risk affects prey species' behavior, even in the absence of a direct threat, but human-induced environmental change may disturb ecologically significant predator-prey interactions. Here, we propose various ways in which knowledge of antipredator tactics, behavioral risk effects, and primate-predator interactions could assist in identifying human-caused disruption to natural systems. Using behavior to evaluate primate responses to the ongoing environmental change should be a potentially effective way to make species conservation more predictive by identifying issues before a more dramatic population declines. A key challenge here is that studies of predation on primates often use data collected via direct observations of habituated animals and human presence can deter carnivores and influence subjects' perception of risk. Hence, we also review various indirect data collection methods to evaluate their effectiveness in identifying where environmental change threatens wild species, while also minimizing observer bias.

Gibbon Aggression During Introductions: An International Survey.

Little is known regarding the prevalence of aggression seen during introductions of captive gibbons (Hylobatidae). In this study, an online survey was developed to quantify and collect contextual details regarding the frequency and types of aggression seen during introductions of captive gibbons (Hylobatidae). Nineteen percent of institutions (17 institutions) reported observing aggression, and 6 of these institutions recorded multiple instances of aggression, though a vast majority of these cases resulted in mild injuries or none at all. The female was the primary aggressor in 23% of cases, the male was the primary aggressor in 58% of cases, and both were the primary aggressor in 1 case. Although these aggressive interactions were often not associated with a known cause, 27% of cases were associated with food displacement. In most cases, management changes, including trying new pairings, greatly reduced situational aggression, suggesting that individual personalities may play a factor in aggression. These data begin to explain the extent of aggression observed in captive gibbons; future studies will address possible correlations with aggression and introduction techniques.

Music for the birds: effects of auditory enrichment on captive bird species.

With the increase of mixed species exhibits in zoos, targeting enrichment for individual species may be problematic. Often, mammals may be the primary targets of enrichment, yet other species that share their environment (such as birds) will unavoidably be exposed to the enrichment as well. The purpose of this study was to determine if (1) auditory stimuli designed for enrichment of primates influenced the behavior of captive birds in the zoo setting, and (2) if the specific type of auditory enrichment impacted bird behavior. Three different African bird species were observed at the Buffalo Zoo during exposure to natural sounds, classical music and rock music. The results revealed that the average frequency of flying in all three bird species increased with naturalistic sounds and decreased with rock music (F = 7.63, df = 3,6, P = 0.018); vocalizations for two of the three species (Superb Starlings and Mousebirds) increased (F = 18.61, df = 2,6, P = 0.0027) in response to all auditory stimuli, however one species (Lady Ross's Turacos) increased frequency of duetting only in response to rock music (X(2) = 18.5, df = 2, P < 0.0001). Auditory enrichment implemented for large mammals may influence behavior in non-target species as well, in this case leading to increased activity by birds.

The effects of auditory enrichment on gorillas.

Several studies have demonstrated that auditory enrichment can reduce stereotypic behaviors in captive animals. The purpose of this study was to determine the relative effectiveness of three different types of auditory enrichment-naturalistic sounds, classical music, and rock music-in reducing stereotypic behavior displayed by Western lowland gorillas (Gorilla gorilla gorilla). Three gorillas (one adult male, two adult females) were observed at the Buffalo Zoo for a total of 24 hr per music trial. A control observation period, during which no sounds were presented, was also included. Each music trial consisted of a total of three weeks with a 1-week control period in between each music type. The results reveal a decrease in stereotypic behaviors from the control period to naturalistic sounds. The naturalistic sounds also affected patterns of several other behaviors including locomotion. In contrast, stereotypy increased in the presence of classical and rock music. These results suggest that auditory enrichment, which is not commonly used in zoos in a systematic way, can be easily utilized by keepers to help decrease stereotypic behavior, but the nature of the stimulus, as well as the differential responses of individual animals, need to be considered.

Hormonal and behavioral patterns of reproduction in female hylobatids.

Ovarian cyclicity, reproductive behavior, and gestation length were characterized in female hylobatids using non-invasive fecal steroid analyses and behavioral data. Progestagen metabolites were quantified in fecal samples collected for 3 months from seven females housed at seven North American zoological institutions. Mean (±SEM) ovarian cycle length was 23.1±1.5 days (seven females; 22 cycles) and was similar across individuals and species (range: 15.3-27.3 days). Gestation length in white-cheeked gibbons was 191±7.0 days (n=2), and female-initiated reproductive behavior occurred throughout the ovarian cycle for each individual. This was the first study of its kind to use fecal hormone metabolite analysis in combination with behavioral observations to characterize female reproductive traits for various hylobatid species. These results contribute to our general knowledge of the basic biology of hylobatids, highlight the importance of evaluating both hormonal and behavioral information, and assist the management and breeding of zoo-housed populations of these endangered primates to support overall conservation efforts.

The ABO blood group is a trans-species polymorphism in primates.

The ABO histo-blood group, the critical determinant of transfusion incompatibility, was the first genetic polymorphism discovered in humans. Remarkably, ABO antigens are also polymorphic in many other primates, with the same two amino acid changes responsible for A and B specificity in all species sequenced to date. Whether this recurrence of A and B antigens is the result of an ancient polymorphism maintained across species or due to numerous, more recent instances of convergent evolution has been debated for decades, with a current consensus in support of convergent evolution. We show instead that genetic variation data in humans and gibbons as well as in Old World monkeys are inconsistent with a model of convergent evolution and support the hypothesis of an ancient, multiallelic polymorphism of which some alleles are shared by descent among species. These results demonstrate that the A and B blood groups result from a trans-species polymorphism among distantly related species and has remained under balancing selection for tens of millions of years-to date, the only such example in hominoids and Old World monkeys outside of the major histocompatibility complex.

Use of buckets as tools by Western lowland gorillas.

While all great apes have been documented to use tools, gorillas are arguably the least proficient tool users. In 2009, a Western lowland gorilla (Gorilla gorilla gorilla) at the Buffalo Zoo was observed using a bucket, which had been provided as part of normal enrichment, as a tool to collect water. We conducted a brief, ad libitum investigation to confirm the validity of the initial observation. We then carried out a systematic investigation of the behavior in 2010. We collected 72 hr of videotaped data and tested the null hypothesis that the gorillas did not differ in their prevalence of engaging in bucket-use behaviors. We documented that all four adult gorillas in the group used buckets as drinking tools; however, there was significant individual variation in frequency and type of use of buckets. Four of the eight behaviors showed significant variation among individuals. The silverback male and the youngest adult female contacted and held the bucket significantly more than the remaining two adult females. The young female carried and drank from the bucket significantly more than any other individual. Furthermore, she was observed to fill the bucket with water four of the six times during which this behavior was observed. These data provide evidence of the ability of gorillas to utilize tools, given the appropriate environmental conditions. We continue to explore the abilities of gorillas to recognize the functionality of buckets as tools.

Effects of combination birth control on estrous behavior in captive western lowland gorillas, Gorilla gorilla gorilla.

Combination birth control pills (CBC) are one of the most common birth control methods used for western lowland gorillas (Gorilla gorilla gorilla) housed in zoos. Since zoos are interested in maintaining as many natural behaviors as possible, it is important to know how contraception may affect social and sexual interactions among group members. Although some data are available regarding the influence of the pill on sexual behavior in human females, no data are available on its effects on gorilla estrous behavior. We examined temporal trends of estrous, aggressive, affiliative, and activity budget data in four females on CBC at the Lincoln Park Zoo in Chicago, IL. Behavioral data were collected using point sampling, all-occurrence records, and one-zero sampling. Estrous behavior occurred in less than 1% of observations. Using all-occurrence and one-zero sampling, estrous behavior occurred more frequently in week one of the cycle than any other week. The focal females exhibited affiliative, aggressive, and activity budget data evenly across their cycles. There were also no temporal trends in proximity to the silverback. Females varied by the types of estrous behavior they exhibited. We give a hormonal explanation for the prevalence of estrous behaviors in week one, and recommendations for effective behavioral sampling of gorilla estrous behavior.

The effectiveness of indigestible markers for identifying individual animal feces and their prevalence of use in North American zoos.

Techniques for analyzing hormone metabolites in animal excreta have created many opportunities for noninvasive monitoring of health, reproduction, and welfare in zoo animals, but can be difficult to implement when individual samples are not readily identifiable in animal groups. A common approach to this problem is to feed animals an indigestible marker that subsequently appears in feces, but there has been little systematic research on the use of such "fecal markers." First, we used an online survey to assess the prevalence of fecal marker use in North American zoological institutions. Second, we conducted a series of experimental tests utilizing commonly employed fecal markers in a variety of typical zoo taxa to determine the: (1) effectiveness of several markers to accurately distinguish samples in a variety of species, (2) minimum quantity of marker needed for detection, and (3) length of time between ingestion and detection in the feces. The majority of the 45 institutions that completed the survey reported using fecal markers with their collections. The survey also revealed that the most frequently used markers are seeds/grains and food colorants, with the former generally used in Carnivora and the latter in Primates. Our experimental data confirmed the success of these taxa/marker combinations and also revealed that food colorants function as markers in a variety of avian, reptilian, and mammalian species. Our data describe successful fecal markers for a wide variety of zoo taxa and should, therefore, be useful for zoological managers and researchers needing to employ fecal markers in future investigations.

Sex ratio bias in managed populations of hylobatids.

A number of explanations have been proposed for the occurrence of sex ratio bias in primates, including the Trivers-Willard hypothesis on differential investment, local resource competition or enhancement as a result of sex-biased dispersal, dominance-related advantages conferred on one sex but not the other, and the fragile male hypothesis. However, none of these theories was thought to be applicable to monogamous primate species. Here, we examine data on zoo-housed populations of three hylobatid species to test the null hypothesis of equal sex ratio. We analyzed over 40 years of demographic data on Nomascus leucogenys, Hylobates lar and Symphalangus syndactylus. We identified a strong male-biased birth sex ratio in N. leucogenys. Male infant mortality was consistently higher than female infant mortality for N. leucogenys, but this difference was not significant. We found that prime-age N. leucogenys females (aged 13-20) produced significantly more male offspring than female offspring, and young S. syndactylus females (<13 years) produced significantly more female offspring. Recent field evidence of more flexible mating systems in H. lar and S. syndactylus may also be occurring in N. leucogenys. However, N. leucogenys has not been well studied in the wild. Ecological differences among species may further contribute to these observed patterns.

Behavioral monitoring in zoos and aquariums: a tool for guiding husbandry and directing research.

Behavioral monitoring is the scientific collection of animal behavior data to understand normal patterns of behavior and changes in these patterns. This tool is underutilized in the zoo industry although it can be an effective indicator of many potential problems that compromise zoo animal well-being. We suggest that a behavioral monitoring program should be a core component of a zoological institution's care program. We detail the benefits of such a program and describe its components. We provide guidelines for implementing such a program and make recommendations that will help institutions to employ behavioral monitoring programs with reasonable expense. We argue that the benefits of such a program, primarily increased detection of rising or potential problems, far outweigh the minor costs of implementation.

Perimenopause and menopause: documenting life changes in aging female gorillas.

As our closest living relatives, great apes likely experience physiological patterns associated with reproductive aging that are similar to humans. We present results from a nationwide zoo-based study on female western lowland gorillas during which we evaluated concentrations of progestogens via daily fecal sampling in 30 gorillas, 22 of whom were geriatric (>or=30). Whereas control females cycled regularly, ca. 23% of geriatric females were acyclic (menopausal), and approximately 1/3 showed variable hormonal patterns suggestive of perimenopause. Patterns included increased cycle variability, low luteal phase rises of progestogens - possibly indicative of anovulatory cycling - and peak height variability of progestogens in the luteal phase of the cycle. We discovered a progressive trend toward increased variability in estrous cycle length and toward decreased concentrations of fecal progestogens when we compared control to geriatric cycling and to geriatric noncycling females. Noncycling females had significantly lower overall progestogen concentrations than the cycling females, though differences were not significant when cycle phase was incorporated. Preliminary analyses of follow-up data on 10 perimenopausal females indicated that subjects experienced age-related changes in reproductive function that mirrored those observed in aging human females including a female who transitioned from perimenopause to menopause. To date, maximum longevity in captive female gorillas is 52 years, with poor reproductive prognosis beginning from the age of 37 suggesting a postreproductive lifespan of >25%. Continued study of aging apes is warranted, with emphasis on longitudinal monitoring of aged subjects.

Behavioral effects of introducing pied tamarin (Saguinus bicolor) to black howler monkey (Alouatta caraya) and white-faced saki (Pithecia pithecia) in a zoological park.

Mixed-species primate exhibits are becoming more common in zoological parks as a means to display a diverse array of animals both more naturalistically and with more economy of space. Here, we describe behavioral changes during the introduction process of a pair of pied tamarins (Saguinus bicolor) to an established group of black howler monkeys (Allouatta caraya) and white-faced saki monkeys (Pithecia pithecia). Data were collected during six phases, representing introductions among the various species and to exhibit space and off-exhibit holding. The pied tamarins were consistently the most active of the three species. Although activity levels of the howler and saki monkeys remained constant throughout, that of the tamarins declined as the introduction progressed. Several episodes of aggression between the tamarins and the sakis were observed, but did not coincide with patterns predicted by previous intra-specific introductions. The three-species mix remained stable for several months; however, escalating aggression ultimately led to the removal of the sakis from the mixed-species exhibit. Despite our mixed results, we contend that only through continued trials, coupled with careful and systematic monitoring, can we ultimately identify stable mixes of species.

Assessment of reproductive behavior and hormonal cycles in geriatric western Lowland gorillas.

The population of western lowland gorillas in North American zoos is aging and, as is the case with the aging human population, may have unique physical and social needs. We have documented previously that 25% of aging females (5/22) ceased to show reproductive cycles entirely, and could be defined as menopausal. Approximately 32% of females showed somewhat irregular cycling patterns. We review our hormonal and behavioral findings on reproductive aging in gorillas; describe the range of cycling patterns that we see and how we interpret these; and discuss the implications of these findings for captive management and husbandry of aging gorillas. We monitored fecal hormone metabolites (progestogens) in 30 gorillas and collected simultaneous behavioral data to evaluate the relationship between cyclicity and sexual behavior. We identified and described several discrete patterns of irregular cycling. These included extreme variability of cycle length, cyclic patterns with unusually low progestogen peak concentrations that possibly may not support luteal activity, and large variability in maximum progestogen peak height among cycles. All of these changes are consistent with age-related hormonal changes observed in humans and may be signs of changes in fertility as well. Behaviorally, nearly all cycling females exhibited signs of estrus. Affiliative behavior between male silverbacks and estrous females was observed in the control females, but not the geriatric females. These findings suggest that pre-menopausal females are exhibiting signs of perimenopause. As is the case in humans, such changes in hormone patterns may occur years before the onset of menopause. As enhancements in nutrition, husbandry, and veterinary medicine have led to increased longevity in our zoo populations of apes, it has become imperative that we investigate and better understand associated physiological and behavioral changes in geriatric animals to ensure appropriate management of this increasing demographic sub-population. Zoo Biol 0:1-23, 2007. (c) 2007 Wiley-Liss, Inc.