Genetic wealth,population health: Major histocompatibility complex variation in captive and wild ring‐tailed lemurs (Lemur catta)

Across species, diversity at the major histocompatibility complex (MHC) is critical to individual disease resistance and, hence, to population health; however, MHC diversity can be reduced in small, fragmented, or isolated populations. Given the need for comparative studies of functional genetic diversity, we investigated whether MHC diversity differs between populations which are open, that is experiencing gene flow, versus populations which are closed, that is isolated from other populations. Using the endangered ring‐tailed lemur (Lemur catta) as a model, we compared two populations under long‐term study: a relatively “open,” wild population (n = 180) derived from Bezà Mahafaly Special Reserve, Madagascar (2003–2013) and a “closed,” captive population (n = 121) derived from the Duke Lemur Center (DLC, 1980–2013) and from the Indianapolis and Cincinnati Zoos (2012). For all animals, we assessed MHC‐DRB diversity and, across populations, we compared the number of unique MHC‐DRB alleles and their distributions. Wild individuals possessed more MHC‐DRB alleles than did captive individuals, and overall, the wild population had more unique MHC‐DRB alleles that were more evenly distributed than did the captive population. Despite management efforts to maintain or increase genetic diversity in the DLC population, MHC diversity remained static from 1980 to 2010. Since 2010, however, captive‐breeding efforts resulted in the MHC diversity of offspring increasing to a level commensurate with that found in wild individuals. Therefore, loss of genetic diversity in lemurs, owing to small founder populations or reduced gene flow, can be mitigated by managed breeding efforts. Quantifying MHC diversity within individuals and between populations is the necessary first step to identifying potential improvements to captive management and conservation plans.     

Characterization of new microsatellite loci for the ring‐tailed lemur (Lemur catta)

In this report we describe the development and characterization of six dinucleotide microsatellite loci for the ring‐tailed lemur (Lemur catta). The new markers were isolated from the genomic DNA of L. catta and all loci were found to be polymorphic when evaluated by genotyping a minimum of 34 individuals. Mendelian inheritance of each locus was verified using four families of captive ring‐tailed lemurs. The loci presented will facilitate the genetic survey of free‐ranging L. catta, enabling study of their social organization and mating patterns.     

Variation in dental wear and tooth loss among known‐aged,older ring‐tailed lemurs (Lemur catta): a comparison between wild and captive individuals

Tooth wear is generally an age‐related phenomenon, often assumed to occur at similar rates within populations of primates and other mammals, and has been suggested as a correlate of reduced offspring survival among wild lemurs. Few long‐term wild studies have combined detailed study of primate behavior and ecology with dental analyses. Here, we present data on dental wear and tooth loss in older (>10 years old) wild and captive ring‐tailed lemurs (Lemur catta). Among older ring‐tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar (n=6), the percentage of severe dental wear and tooth loss ranges from 6 to 50%. Among these six individuals, the oldest (19 years old) exhibits the second lowest frequency of tooth loss (14%). The majority of captive lemurs at the Indianapolis Zoo (n=7) are older than the oldest BMSR lemur, yet display significantly less overall tooth wear for 19 of 36 tooth positions, with only two individuals exhibiting antemortem tooth loss. Among the captive lemurs, only one lemur (a nearly 29 year old male) has lost more than one tooth. This individual is only missing anterior teeth, in contrast to lemurs at BMSR, where the majority of lost teeth are postcanine teeth associated with processing specific fallback foods. Postcanine teeth also show significantly more overall wear at BMSR than in the captive sample. At BMSR, degree of severe wear and tooth loss varies in same aged, older individuals, likely reflecting differences in microhabitat, and thus the availability and use of different foods. This pattern becomes apparent before “old age,” as seen in individuals as young as 7 years. Among the four “older” female lemurs at BMSR, severe wear and/or tooth loss do not predict offspring survival. Am. J. Primatol. 72:1026–1037, 2010. © 2010 Wiley‐Liss, Inc.     

Evaluation of the genetic management of the endangered black‐footed ferret (Mustela nigripes)

Empirical support for the genetic management strategies employed by captive breeding and reintroduction programs is scarce. We evaluated the genetic management plan for the highly endangered black‐footed ferret (Mustela nigripes) developed by the American Zoo and Aquarium Associations (AZA) as a part of the species survival plan (SSP). We contrasted data collected from five microsatellite loci to predictions from a pedigree‐based kinship matrix analysis of the captive black‐footed ferret population. We compared genetic diversity among captive populations managed for continued captive breeding or reintroduction, and among wild‐born individuals from two reintroduced populations. Microsatellite data gave an accurate but only moderately precise estimate of heterozygosity. Genetic diversity was similar in captive populations maintained for breeding and release, and it appears that the recovery program will achieve its goal of maintaining 80% of the genetic diversity of the founder population over 25 years. Wild‐born individuals from reintroduced populations maintained genetic diversity and avoided close inbreeding. We detected small but measurable genetic differentiation between the reintroduced populations. The model of random mating predicted only slightly lower levels of heterozygosity retention compared to the SSP strategy. The random mating strategy may be a viable alternative for managing large, stable, captive populations such as that of the black‐footed ferret. Zoo Biol 22:287–298, 2003. © 2003 Wiley‐Liss, Inc.     

川金丝猴圈养种群现状分析

川金丝猴(Rhinopithecus roxellartae)圈养种群大多饲养在中国的动物园中。根据《川金丝猴国际谱系簿2002》记录,到2002年12月31日种群存活数量185只,包括野外捕获个体和圈养出生个体。近年圈养出生数量一直保持增加,到2000年超过野外捕获个体数量,现在种群的增加更多地依靠圈养出生个体数量的增加。近12年中种群繁殖率不断提高。每年新生幼仔中野外捕获个体组产仔比率逐年减少,圈养出生个体组产仔比率逐年增大,但到2002年前者仍高于后者40％。两组动物的繁殖率都有上升趋势,野外捕获个体组的繁殖率大多高于圈养出生个体组的繁殖率,二者有明显差异。种群遗传状况是基因多样性保存量较高,各小种群的基因多样性却处于较整体低的水平。提高子代的繁殖率,增加各机构之间的合作繁殖以提高小种群的基因多样性保持量,这两者对于种群的健康发展是非常重要的。     

Pedigree analysis for the genetic management of group‐living species

Captive breeding programs are an important tool for the conservation of endangered species. These programs are commonly managed using pedigrees containing information about the history of each individual's family, such as breeding pairs and parentage. However, there are some species that are kept in groups where it is hard to distinguish between particular individuals within the group, making it very difficult to record any information at an individual level. Currently, software and methods commonly used for registering and analyzing pedigrees to help manage populations at an individual level are not adequate for managing these group‐living species. Therefore, there is a need to further develop these tools and methodologies for pedigree analysis to better manage group‐living species. PMx is a program used for the management of ex situ populations in zoos and aquariums. We adapted the pedigree analysis method implemented in PMx to analyze pedigrees (records of descendant lineages) of group‐living species. In addition, we developed a group pedigree data entry sheet and group2PMx, a converter program that enables group datasets to be imported into PMx. We show how pedigree analysis of a group‐living species can be used for population management using the studbook of the endangered Texas blind cave salamander Eurycea rathbuni. Such analyses of the pedigree of groups can improve the management of group‐living species in ex situ breeding programs. Firstly, it enables better management decisions based on more accurate genetic measures between groups, allowing for greater control of inbreeding. Secondly, it can improve the conditions in which group‐living species are held by adapting husbandry practices to better reflect conditions of these species living in the wild. The use of the spreadsheet and group2PMx extends the application of PMx_, allowing conservation managers and other institutions outside the zoo and aquarium community to easily import and analyze their pedigree data.     

Lineage Identification and Genealogical Relationships Among Captive Galápagos Tortoises

Genetic tools have become a critical complement to traditional approaches for meeting short‐ and long‐term goals of ex situ conservation programs. The San Diego Zoo (SDZ) harbors a collection of wild‐born and captive‐born Galápagos giant tortoises (n = 22) of uncertain species designation and unknown genealogical relationships. Here, we used mitochondrial DNA haplotypic data and nuclear microsatellite genotypic data to identify the evolutionary lineage of wild‐born and captive‐born tortoises of unknown ancestry, to infer levels of relatedness among founders and captive‐born tortoises, and assess putative pedigree relationships assigned by the SDZ studbook. Assignment tests revealed that 12 wild‐born and five captive‐born tortoises represent five different species from Isabela Island and one species from Santa Cruz Island, only five of which were consistent with current studbook designations. Three wild‐born and one captive‐born tortoise were of mixed ancestry. In addition, kinship analyses revealed two significant first‐order relationship pairs between wild‐born and captive‐born tortoises, four second‐order relationships (half‐sibling) between wild‐born and captive tortoises (full‐sibs or parent‐offspring), and one second‐order relationship between two captive‐born tortoises. Of particular note, we also reconstructed a first‐order relationship between two wild‐born individuals, violating the founder assumption. Overall, our results contribute to a worldwide effort in identifying genetically important Galápagos tortoises currently in captivity while revealing closely related founders, reconstructing genealogical relationships, and providing detailed management recommendations for the SDZ tortoises. Zoo Biol 31:107;–120, 2012. © 2011 Wiley Periodicals, Inc.     

A Large‐Scale SNP‐Based Genomic Admixture Analysis of the Captive Rhesus Macaque Colony at the California National Primate Research Center

Some breeding facilities in the United States have crossbred Chinese and Indian rhesus macaque (Macaca mulatta) founders either purposefully or inadvertently. Genetic variation that reflects geographic origins among research subjects has the potential to influence experimental outcomes. The use of animals from different geographic regions, their hybrids, and animals of varying degrees of kinship in an experiment can obscure treatment effects under study because high interanimal genetic variance can increase phenotypic variance among the research subjects. The intent of this study, based on a broad genomic analysis of 2,808 single nucleotide polymorphisms (SNPs), is to ensure that only animals estimated to be of pure Indian or Chinese ancestry, based on both demographic and genetic information, are used as sources of infants for derivation and expansion of the California National Primate Research Center's (CNPRC) super‐Specific Pathogen Free (SSPF) rhesus macaque colony. Studies of short tandem repeats (STRs) in Indian and Chinese rhesus macaques have reported that heterozygosity of STRs is higher in Chinese rhesus macaques than in Indian rhesus macaques. The present study shows that heterozygosity of SNPs is actually higher in Indian than in Chinese rhesus macaques and that the Chinese SSPF rhesus macaque colony is far less differentiated from their founders compared to the Indian‐origin animals. The results also reveal no evidence of recent gene flow from long‐tailed and pig‐tailed macaques into the source populations of the SSPF rhesus macaques. This study indicates that many of the long‐tailed macaques held in the CNPRC are closely related individuals. Most polymorphisms shared among the captive rhesus, long‐tailed, and pig‐tailed macaques likely predate the divergence among these groups. Am. J. Primatol. 74:747‐757, 2012. © 2012 Wiley Periodicals, Inc.     

Implementing long‐term baselines into primate tool‐use studies

Studies on primate tool‐use often involve the use of baseline conditions, as they allow for the examination of any differences in the subjects' behavior before and after the introduction of a tool‐use task. While these baseline conditions can be powerful for identifying the relative contributions of individual and social learning for the acquisition of tool‐use behaviors in naïve (usually captive) subjects, many have criticized them for being too short, and not allowing enough time for the behavior to develop spontaneously. Furthermore, some wild tool‐use behaviors such as chimpanzee nut‐cracking require animals to manipulate and familiarize themselves with the materials of the behavior within a “sensitive learning period” before it develops later on in life. One solution to this problem is to implement long‐term baselines, in which, with collaboration with zoological institutions, the materials of the behavior are left in the enclosure for an extended period. The keepers would then be asked not to demonstrate or train the animals in the target behavior, but to report back to the researchers if they observe the behavior emerge during this extended period. Alongside keeper reports, video cameras could be installed in the enclosure to minimize the chance of false negatives and to allow for coding and inter‐rater reliability to be carried out on the videos. These long‐term baselines therefore provide extended enrichment opportunities for the animals, alongside allowing the zoological institution to publicize their involvement with the study and guests to observe animals interacting with different testing apparatuses and tools. Finally, long‐term baselines can provide invaluable insight on the individual and social learning abilities of primates as well as the potential development stages and sensitive learning periods required for specific behaviors.     

The effects of olfactory stimulation on the behavior of captive ring‐tailed lemurs (Lemur catta)

Ring‐tailed lemurs reside in many animal collections worldwide. Lemur welfare may be a cause of concern due to some captive individuals exhibiting stereotypic behavior. Despite these concerns, there has been little exploration of methods of environmental enrichment for ring‐tailed lemurs. Olfactory stimulation can enhance captive animal welfare by encouraging species‐typical behaviors, enhancing behavioral diversity, and decreasing stereotypic behaviors. We aimed to investigate the effects of olfactory stimulation via lavender, peppermint, coconut, and prey odor upon the behavior of eight captive ring‐tailed lemurs. We exposed the lemurs to six individual odor conditions (odor control, novel object control, lavender, peppermint, coconut, and Morio worms) and observed them for 4 hr a day for 3 days with an intervening period of 4 days between conditions. We recorded the lemurs’ behavior under each condition using instantaneous scan sampling. We found significant effects of olfactory stimulation on the ring‐tailed lemurs’ behavior in the initial analysis but these did not survive correction for multiple testing. Overall, while our findings are suggestive of a general effect of olfactory stimulation on the captive ring‐tailed lemurs they did not indicate a marked influence of olfactory condition. However, further investigation with a larger sample size and more biologically relevant odors may be beneficial to fully examine potential effects of olfactory stimulation in captive lemurs.     

A Suite of Microsatellite Markers Optimized for Amplification of DNA From Addax (Addax nasomaculatus) Blood Preserved on FTA Cards

The addax (Addax nasomaculatus) is a critically endangered antelope that is currently maintained in zoos through regional, conservation breeding programs. As for many captive species, incomplete pedigree data currently impedes the ability of addax breeding programs to confidently manage the genetics of captive populations and to select appropriate animals for reintroduction. Molecular markers are often used to improve pedigree resolution, thereby improving the long‐term effectiveness of genetic management. When developing a suite of molecular markers, it is important to consider the source of DNA, as the utility of markers may vary across DNA sources. In this study, we optimized a suite of microsatellite markers for use in genotyping captive addax blood samples collected on FTA cards. We amplified 66 microsatellite loci previously described in other Artiodactyls. Sixteen markers amplified a single product in addax, but only 5 of these were found to be polymorphic in a sample of 37 addax sampled from a captive herd at Fossil Rim Wildlife Center in the US. The suite of microsatellite markers developed in this study provides a new tool for the genetic management of captive addax, and demonstrates that FTA cards can be a useful means of sample storage, provided appropriate loci are used in downstream analyses. Zoo Biol 31:98;–106, 2012. © 2011 Wiley Periodicals, Inc.     

Genetic kinship and social structure in a herd of square‐lipped rhinoceroses (Ceratotherium simum simum) at the zoological center,Tel Aviv/Ramat‐Gan,Israel

Zoos and zoological parks serve as genetic and demographic reserves for strengthening endangered populations and reestablishing extinct populations in the wild. Knowing the genetic ties within captive populations is a very helpful tool for successful reproductive management. In the present study we addressed kinship relationships and behavior among rhinoceroses (Ceratotherium simum simum) raised at the Zoological Center, Tel Aviv/Ramat Gan, Israel, with the hope of identifying reasons for the declining rate of reproduction within the herd. We used the random amplified polymorphic DNA (RAPD) technique to reveal the paternity of the rhinos born at the park. In this way, we identified the paternity of five out of seven young born in the herd, which are currently in Ramat Gan. One male accounted for three (37.5%) births, and two other males accounted for one each. The paternity of the two other animals is unknown and may be of animals that are no longer in the Zoological Center. The genetic determinations were accompanied by behavioral observations, which enabled us to determine the social dynamics in the herd. This study suggests that there are at least three contributing factors to the reproductive decline in the herd: 1) a surplus of males, 2) exclusion of potentially reproductive males from the breeding stock, and 3) specific behavioral and physiological problems in some members of the herd. Zoo Biol 21:561–571, 2002. © 2002 Wiley‐Liss, Inc.     

A comparison of pedigree‐ and DNA‐based measures for identifying inbreeding depression in the critically endangered Attwater's Prairie‐chicken

The primary goal of captive breeding programmes for endangered species is to prevent extinction, a component of which includes the preservation of genetic diversity and avoidance of inbreeding. This is typically accomplished by minimizing mean kinship in the population, thereby maintaining equal representation of the genetic founders used to initiate the captive population. If errors in the pedigree do exist, such an approach becomes less effective for minimizing inbreeding depression. In this study, both pedigree‐ and DNA‐based methods were used to assess whether inbreeding depression existed in the captive population of the critically endangered Attwater's Prairie‐chicken (Tympanuchus cupido attwateri), a subspecies of prairie grouse that has experienced a significant decline in abundance and concurrent reduction in neutral genetic diversity. When examining the captive population for signs of inbreeding, variation in pedigree‐based inbreeding coefficients (f_pedigree) was less than that obtained from DNA‐based methods (f_DNA). Mortality of chicks and adults in captivity were also positively correlated with parental relatedness (r_DNA) and f_DNA, respectively, while no correlation was observed with pedigree‐based measures when controlling for additional variables such as age, breeding facility, gender and captive/release status. Further, individual homozygosity by loci (HL) and parental r_DNA values were positively correlated with adult mortality in captivity and the occurrence of a lethal congenital defect in chicks, respectively, suggesting that inbreeding may be a contributing factor increasing the frequency of this condition among Attwater's Prairie‐chickens. This study highlights the importance of using DNA‐based methods to better inform management decisions when pedigrees are incomplete or errors may exist due to uncertainty in pairings.     

Effects of captivity,diet, and relocation on the gut bacterial communities of white‐footed mice

Microbes can have important impacts on their host's survival. Captive breeding programs for endangered species include periods of captivity that can ultimately have an impact on reintroduction success. No study to date has investigated the impacts of captive diet on the gut microbiota during the relocation process of generalist species. This study simulated a captive breeding program with white‐footed mice (Peromyscus leucopus) to describe the variability in gut microbial community structure and composition during captivity and relocation in their natural habitat, and compared it to wild individuals. Mice born in captivity were fed two different diets, a control with dry standardized pellets and a treatment with nonprocessed components that reflect a version of their wild diet that could be provided in captivity. The mice from the two groups were then relocated to their natural habitat. Relocated mice that had the treatment diet had more phylotypes in common with the wild‐host microbiota than mice under the control diet or mice kept in captivity. These results have broad implications for our understanding of microbial community dynamics and the effects of captivity on reintroduced animals, including the potential impact on the survival of endangered species. This study demonstrates that ex situ conservation actions should consider a more holistic perspective of an animal's biology including its microbes.     

Captive breeding of cheetahs in North American Zoos: 1987–1991

From 1987 to 1991, the North American captive cheetah population increased by 38% (to 266 animals), due to importation and captive breeding. This population constitutes 26% of the world's captive cheetahs and 36% of all reproductively successful animals. Since 1956, 33% of all cubs born in North America occurred during this 5-year period. Because of importation of animals from breeding programs abroad, East African (A. jubatus raineyi) genes have been introduced into the North American cheetah population, and 39% of all cubs born during 1987--1991 were South African/East African hybrids. Also during this time, the breeding population and effective breeding population increased by 86% and 72.6%, respectively. The incidence of infant mortality decreased from 37% (last recorded for the years 1956 to 1986) to 28% (averaged over 5 years), although infant mortality during the latter period ranged from 15% (for unrelated parents) to 41% (for related parents). Management recommendations implemented to increase fecundity and population size appear to be successful, although the founder base of the population still has only been increased from 52 cheetahs in 1986 to 72 animals in 1991. © 1993 Wiley-Liss, Inc.     

Relationship between arrival timing and breeding success of intra‐tropical migratory Fork‐tailed Flycatchers (Tyrannus savana)

For migratory birds, early arrival at breeding areas has many benefits, such as acquisition of better territories and mates. This strategy has been found in numerous species breeding at north‐temperate latitudes, but has not been yet reported for intra‐tropical migratory species. We evaluated the relationship between arrival date, initiation of breeding, and breeding success of Fork‐tailed Flycatchers (Tyrannus savana) breeding in southeastern Brazil and overwintering in northern South America. We color‐banded adult flycatchers during three breeding seasons and searched for them during the following breeding seasons. We also monitored nests from construction until either failure or fledging of young. We found that: (1) male Fork‐tailed Flycatchers arrived at the breeding site earlier than females, (2) males that arrived earlier had greater breeding success, and (3) nests where eggs were laid earlier in the breeding season were more likely to be successful than those where eggs were laid later. Male Fork‐tailed Flycatchers appeared to benefit from early arrival at a tropical breeding site, potentially mediated by their ability to acquire a high‐quality territory and mate as early as possible, and by the ability of their mate to begin breeding as early as possible. Breeding success for female Fork‐tailed Flycatchers may be determined primarily by a combination of the arrival date of their mate and how quickly they can begin breeding. Our results suggest that protandry occurs in an intra‐tropical migratory bird and that early arrival of males and early initiation of reproduction by females results in greater reproductive success. A better understanding of the underlying mechanisms that control the timing of migration and reproduction of this and other intra‐tropical migratory species is important for evaluating the challenges they face in light of current and future rapid environmental changes.     

Conservation genetics of Boelen’s python (Morelia boeleni) from New Guinea: reduced genetic diversity and divergence of captive and wild animals

Boelen’s python (Morelia boeleni) is a montane New Guinea endemic found in highlands above 1000 m and below the tree line. The ecology, natural history, distribution, population size, and conservation status of this species are largely unknown. It has a protected status in Papua New Guinea but not in Indonesian Papua and several US and European zoos have active captive breeding programs that have been largely unsuccessful. To understand the degree of genetic diversity in wild and captive animals we undertook a genetic analysis of 90 M. boeleni for which we sequenced two mtDNA loci and one nuclear locus for a total of 1,418 bp of sequence data per individual. All 16 wild-caught M. boeleni from Indonesia and all captive M. boeleni are genetically uniform for all three loci. The single wild-caught animal from Papua New Guinea showed extremely low levels of genetic divergence and diversity from the Indonesian and captive samples. Data from two congeners, M. amethistina and M. viridis, suggests that M. boeleni have reduced genetic variation with a small effective population size possibly due to historical bottlenecks. These data demonstrate the need for further studies of genetic diversity of M. boeleni from across its range and raise particular concern for the limited genetic diversity of M. boeleni used captive breeding programs in zoological parks.     

Breeding program for the lesser kudu (Tragelaphus imberbis) in North America

The lesser kudu (Tragelaphus imberbis) has been kept in North American zoological parks since 1930 but has never been a common species in collections. In 1987 this population totaled 28 animals: 15 males and 13 females. A pedigree evaluation in 1987 of the existing population indicated that eight effective founders and one potential founder were represented in the North American herd. Three new potential founders from European captive populations were added to the population in 1987 to increase the number of existing founder lines to 12 animals. As this species is not endangered or threatened in its native habitat, it is not a high priority to qualify for designation as an SSP species. Because of this, the institutions holding lesser kudu in North America decided to join informally and draft a breeding program to better manage this small captive population. This program was designed to minimize inbreeding and equalize genetic representation of founder animals to maximize genetic diversity. It requires a shift in management philosophy to establish stable groups of breeding females at participating institutions while rotating appropriate breeder males through these herds in a controlled manner to ensure minimization of inbreeding and maximization of genetic diversity. It is hoped that this program can serve as a model for the management of other small captive populations of non-SSP species.     

Management and husbandry of ruffed lemurs,Varecia variegata,at the San Diego Zoo. I. Captive population,San Diego Zoo housing and diet

The captive history of the ruffed lemur is presented with concentration on taxonomy, captive population and husbandry of the San Diego Zoo population. At the conclusion of 1985, the living population of black and white ruffed lemurs numbered 358; red ruffed lemurs totaled 125. The San Diego Zoo population, established between 1965 and 1970, began with two pairs of each subspecies. Intensive breeding at the Primate Propagation Center resulted in the birth of 135 black and white ruffed lemur infants and 95 red ruffed lemur infants as of January 7, 1986. Housing specifications are presented for the off-exhibit 96-unit breeding facility, describing enclosure size, material, nest box composition, and enclosure furniture. The diet is described, which emphasizes high-protein, high-fiber foods and leaves.     

Cotton-top tamarins (Saguinus (o.) oedipus) in a semi-naturalistic captive colony

To test the prediction that the breeding success of captive cotton-top tamarins (Saguinus (o.) oedipus) could be improved by maintaining them in groups whose size and age-sex composition resembled those of wild groups, data were collated from 6.5 years of records from a breeding colony that otherwise had housing and husbandry procedures similar to those of other successful colonies. Group size and composition in the colony closely resembled those of wild groups, and infant survival was the highest yet reported for the species, with 69% of the 124 infants born reared by their parents to adulthood, and a mean surviving litter size of 1.5 infants. Abortion, stillbirth, and parental neglect of infants were rare. Parity had several effects on reproduction: mean litter size decreased, but percentage infant survival increased; interbirth intervals decreased in length; and seasonality in reproduction was more pronounced for the first four litters born to breeding females than for their subsequent litters, with a birth peak in the spring. Although a spacious and complex physical environment, retention of offspring in their natal families until experience of several sets of infant siblings had been obtained, and non-invasive husbandry and research techniques may all have contributed to the colony's success, it seems possible that the improvement over other colonies is due to the resemblance of group composition to those of wild tamarins.