FACTORS AFFECTING INFANT SURVIVAL OF COTTON-TOP TAMARINS. (Saguinus oedipus) IN ZOOS. A Professional Paper HOLLIE J. COLAHAN

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1 FACTORS AFFECTING INFANT SURVIVAL OF COTTON-TOP TAMARINS (Saguinus oedipus) IN ZOOS A Professional Paper by HOLLIE J. COLAHAN Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of MASTER OF WILDLIFE SCIENCE August 2009

2 FACTORS AFFECTING INFANT SURVIVAL OF COTTON-TOP TAMARINS (Saguinus oedipus) IN ZOOS A Professional Paper by HOLLIE J. COLAHAN Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of MASTER OF WILDLIFE SCIENCE Approved by: Chair of Committee, Jane Packard Committee Members, Sharon Gursky Amanda Stronza Anne Savage Head of Department, Thomas Lacher

3 iii ABSTRACT Factors Affecting Infant Survival of Cotton-Top Tamarins (Saguinus oedipus) in Zoos. (August 2009) Hollie J. Colahan, B.S., Kansas State University Chair of Advisory Committee: Dr. Jane Packard Factors affecting the survival of infant cotton-top tamarins (Saguinus oedipus) in zoos have not been as widely studied as in the laboratory. Laboratory results on the effect of sibling experience are conflicting and no multi-institutional studies have been done in zoos. This paper analyzes information on 117 animals living in North American zoos from and compares the effect of sibling experience on first and second litter survival with both females and males. Females with sibling experience are more likely to have surviving offspring from their first litter (71%) than those without sibling experience (48%), although results were not statistically significant using log likelihood ratios (G 2 =3.14, df=1, P>0.05). However, survival rates for the subsequent litter are virtually equal at 80% for those with sibling experience and 81% for females without it. No significant difference in litter survival was found for males but litter survival did improve for both groups by the second litter (G 2 =0.31, df=1, P>0.05). The management of small populations of critically endangered species requires that erring on the side of caution when making management decisions and these results do support previous

4 iv management practices that recommended breeding of animals with sibling experience over those without it and the information about the success rate of second litters should be considered if there is a need to breed tamarins that lack sibling experience.

5 v ACKNOWLEDGEMENTS I would like to thank Dr. Anne Savage for inviting me into the world of Neotropical Primates and her input on this paper. Rebecca Phillips also provided invaluable advice on this project. I am grateful to the Houston Zoo, Inc for financial assistance and support in pursuing this degree. Finally, thanks to Dr. Jane Packard for all her guidance and support, as well as to Drs. Sharon Gursky and Amanda Stronza for their time and feedback on this paper.

6 vi TABLE OF CONTENTS ABSTRACT... iii ACKNOWLEDGEMENTS... v LIST OF FIGURES... vii LIST OF TABLES... viii INTRODUCTION... 1 METHODS... 5 RESULTS... 9 DISCUSSION CONCLUSION REFERENCES VITA... 20

7 vii LIST OF FIGURES 1. Studbook Data Filtering Process Litter survival results for females by percentage Litter survival results for males by percentage... 11

8 viii LIST OF TABLES 1. Definitions of terms Subjects... 8

9 1 INTRODUCTION Cotton-top tamarins (Saguinus oedipus) are small primates of the family Callitrichidae endemic to Colombia. They have been a popular model for biomedical research (particularly colitis and colorectal cancer) and have been maintained in research colonies in the United States, Germany, and the United Kingdom since the 1960s (Colahan, 2009; Defler, 2004). Over 20,000 cotton-top tamarins were imported from Colombia until they were placed on the Endangered Species List (CITES, Appendix I) in the 1970s and importation was prohibited (Leong et al., 2004). Efforts to breed callitrichids in captivity began in earnest in the 1970s after these restrictions on the importation of wild-caught primates made acquisition of animals for research more difficult. Wild cotton-top tamarins typically give birth to 1-2 offspring once each year (Savage et al., 1996). In captivity tamarins frequently give birth to triplets though all three rarely survive (Leong et al., 2004). In the first days of life, mothers are the primary caregivers and older siblings and the father assist in care beginning in the first few days or weeks. Cotton-top tamarin infants are transported on the backs of the parents and helpers and the carrier does not offer assistance, except during transfers, so the infant must be able to cling in order to survive (Tardif, 1997). Each offspring may weigh up to 20% of the dam s body weight and she will not be able to raise them without assistance from others in the group (Tardif et al., 1993). This paper follows the style of Zoo Biology

10 2 Early laboratory studies indicated that captive born animals had lower infant survival rates than their wild-born counterparts (Gengozian et al., 1978). Kirkwood (1983) proposed that this parental incompetence stemmed from animals being removed from their family at a young age and missing developmentally important experience assisting in the care of younger siblings. Evidence supporting the "parental incompetence" hypothesis in laboratory colonies has been ambiguous. Tardif et al. (1984) found that sibling experience, being present in the family group when younger siblings are born, may be more important for cotton-top tamarins than in other callitrichid species. However, this hypothesis was supported by a small sample size (N=9 females and 11 males). In a laboratory colony at the University of Wisconsin- Madison, Snowdon et al. (1985) found lower infant mortality for females (N=11) with sibling experience but also attributed the improved success of the research colony to changes in husbandry factors such as cage complexity, nutrition, and handling practices. Johnson et al. (1991) found no significant difference between cotton-top tamarins with and without sibling experience (the number of dams in the study was not noted). In addition to simply being present in the family group when siblings are born, Cleveland and Snowdon (1984) found that the age of the older sibling influenced the type of interactions. Juveniles (7-14 months) play with infants but do not carry them, potentially learning to be more tolerant of infants clinging to their backs. Subadults (over 14 months) rarely played with infants but did frequently carry them, which assists the parents in the care of offspring and provides the older siblings with carrying skills that will need to possess as parents. More helpers in the group reduces the dam s carrying

11 3 time (Cleveland and Snowdon, 1984). Juveniles are more inept at carrying infants, often positioning them incorrectly or not retrieving them when they fall but this ability improves as they get older, indicating a benefit of this experience (Tardif, 1997). However, Tardif (1997) cautions that it is difficult to determine if this benefit comes simply from being present when younger siblings are born into the group or if actual participation in care is required. Finally, another recent area of study has been the role of hormones in parental care behavior, particularly in males. Males show increased levels of prolactin before and after the birth of infants, regardless of infant survival. This is different from females, whose prolactin levels elevate later in the pregnancy and will drop if infants do not survive (Ziegler and Snowdon, 1997). Prolactin levels are correlated to the number of previous births the males have experienced and prolactin has been shown to increase parental care behaviors in other species (Ziegler and Snowdon, 2000). Ziegler et al. (2004) also found changes in males estrogen and glucocorticoid levels but the effect is unknown. While such data are not available in a retrospective study such as this one, the hormonal changes in the parents most certainly plays a role in their parental care behavior and likely interacts with previous experience with infants (Ziegler et al., 2004). Management decisions for cotton-top tamarins in zoos have been based historically on the results of research at the University of Wisconsin-Madison laboratory colony and there has not been a large-scale study of the of effect sibling experience in a zoo environment to date. The Cotton-Top Tamarin Species Survival Plan (SSP ) was

12 4 formed by the Association of Zoos and Aquariums (AZA) in 1992 (Hutchins and Wiese, 1991). Efforts were made to preferentially breed animals with sibling experience to reduce the effects of the parental incompetence seen in laboratory colonies (Savage, 1995). The program has been a success, resulting in over 300 animals in 80 institutions. The goal of this study was to examine the effect of sibling experience on litter survival for both female and male cotton-top tamarins since the inception of the SSP.

13 5 METHODS Subjects The data used by the SSP is kept in the Cotton-Top Tamarin International Studbook, currently maintained by the author (Colahan, 2009). The studbook is the official record of the species history in captivity, which includes pedigrees and major life events such as births, deaths, and transfers. The studbook keeper collects historic data from each institution and annual updates are requested thereafter. The studbook contains over 11,000 historic specimens, making it the primary source of data on infant survival in zoos and aquariums. This large number of specimens includes many early and incomplete records so the dataset used in this study is a subset of the total studbook Figure 1). The most accurate and detailed records of infant survival rates and rearing history are from AZA zoos since the inception of the SSP. Therefore, animals included in this study are those in the SSP that gave birth to their first litter between 1 January December 2007, which provides a sample size of 55 males and 62 females (Figure 1).

14 6 Figure 1. Studbook Data Filtering Process Complete Historic = 11,603 AZA Historic = 2,732 SSP Living = 1,038 Known Rearing = 981 Reproduced = 160 Known Sibling Experience = 117 After the above filtering, a reproductive history report was run on each individual specimen, which listed all offspring born along with birth dates, death dates, and the other parent of the litter. In most cases, data on the first two litters were recorded, except when one or both of those litters was stillborn. In those instances, the subsequent litter

15 7 was used. In a few cases, animals only had one litter during the study period, which is also indicated in Table 1. Data on sibling experience were obtained via the reproductive history report and SSP records where possible and supplemented with further communication with the zoo where that animal was born. Table 1. Definitions of terms Parent Reared Litter Survival Sibling Experience Definition Animals raised by their parents in a family group, which may or may not include siblings At least one animal in the litter survived at least 30 days without human intervention such as hand rearing. Animals were present in their family group for the birth of at least one subsequent litter (Baker and Woods, 1992; Tardif et al., 1984) Data Analysis and Statistics Males and females were analyzed separately since they often share the same litter and are therefore not independent of each other; grouping them together would count the same litter twice is some instances. Both males and females were divided into one of four groups: sibling experience and litter survived, sibling experience and litter did not survive, no sibling experience and litter survived and no sibling experience and litter did not survive (Table 1). This grouping was repeated for the survival of the second litter (Table 2). To test for the effect of sibling experience on reproductive success, data were

16 8 tallied in a contingency table. Log-likelihood ratios (G 2 statistics) were used to determine differences in the results from chance at p=0.05 (Bishop et al., 1975; Gottman and Roy, 1990). Table 2. Subjects Sibling Experience Infant Survival 1 st Litter 2 nd Litter Females Yes No Yes No Yes No Total 62 Males Yes No Total 55

17 9 RESULTS Females Of the 62 females in the study, 41 (66%) had sibling experience and 21 (34%) did not (Table 1). Females with sibling experience had surviving litters 70% of the time while those without sibling experience only raised surviving infants in 48% of first litters, which was not significant (G 2 =3.14, df=1, P>0.05, Figure 2). However, by the second litter both groups are virtually equal with litters surviving 80% of the time for those with sibling experience and 81% for those without it (Figure 2). Figure 2. Litter survival results for females by percentage

18 10 Males Of the 55 males in the study, 34 (62%) had sibling experience and 21 (38%) did not (Table 1). The males with sibling experience had a 65% survival rate for their first litter and those without sibling experience had a 57% survival rate, which was also not significant (G 2 =0.31, df=1, P>0.05, Figure 3). For their second litter, both groups were also much closer together; males with sibling experience had surviving litters 79% of the time and those without had second litters survive 76% of the time (Figure 3)

19 Figure 3. Litter survival results for males by percentage 11

20 12 DISCUSSION Females with sibling experience had an advantage in litter survival over those without it for their first litter. However, by their second litter, success rates were higher for both groups and females with sibling experience and those without it had virtually equal success rates. This suggests that the necessary skills for raising offspring may be acquired either with siblings or with the first litter. The lack of significant differences for male parents with and without sibling experience is not surprising, since the success of a male is more dependent on the female s skills then vice versa in the first few days of life. If the female does not allow the infant to nurse, it will die regardless of parental care efforts (Tardif et al., 1984). One study did find that sibling experience was more important for males than females and another found that it was equally important (Johnson et al., 1991; Snowdon et al., 1985; Tardif and Bales, 1997). A male s lack of participation or skill may also be offset by other alloparents in the group (Price, 1992; Tardif et al., 1993). Further examination of the male s partner and group size may provide additional insight into the effect of these factors. Baker and Woods (1992) proposed that age at removal from the family group, first pairing, and at first reproduction could all be additional variables that affect litter survival. While the first two of these variables were not available in the studbook database, the minimum age at first reproduction was 2 years, similar to wild tamarins (Savage, personal communication). However, the age when the animals were first paired

21 13 is not available in the studbook database and this could be another confounding factor. Another factor mentioned above but not analyzed in this study (and not recorded in the studbook database) was group size, which has been shown to affect infant survival (Johnson et al., 1991; Price, 1992; Washabaugh et al., 2002). In laboratory studies cage size and complexity, as well as changes in husbandry practices have also been shown to improve infant survival (Price, 1992; Washabaugh et al., 2002). Laboratory colonies provide a large sample size of animals that are all held in similar and controlled conditions and this data would be difficult to collect and quantify across the 80 zoos and aquariums that hold cotton-top tamarins, though it does likely play a role. Litter size is another factor that may influence survival but in this study, it was not recorded and litters in which one of one offspring survived were counted the same as one of two, three of three, etc. This information exists in the studbook database and could be examined in the future. When working with a relatively small captive population of a critically endangered primate a Type II error could result in irreversible damage to the population. Using the laboratory experiences as a guide and favoring the possibility of a Type I error, the Cotton-Top Tamarin SSP began to track the sibling experience of all individuals in the population. Animals that lacked sibling experience were not recommended to breed and animals that failed to raise their offspring or had been hand reared were also excluded from breeding. By the late 1990s the population had exceeded its target of 250 animals so the SSP began to recommend less breeding than in the past, but still sought to maximize genetic diversity and infant survival. Today, the SSP

22 14 population remains stable at about 300 animals and is genetically healthy and selfsustaining (Phillips, 2008). However, due to the planned decrease in breeding recommendations in recent years in order to maintain this population size, there are many animals in the SSP population that do not have sibling experience that may be needed for breeding in the future. Based on the results of this study, those animals may require two or more attempts at raising offspring to be successful, which is valuable information for both collection managers and the Cotton-Top Tamarin SSP. Over the last 40 years, cotton-top tamarins have gone from being a species that was difficult to breed and whose husbandry was not well understood to one of the most numerous and well-studied primates in captivity. Years of research in laboratories, zoos and the in the field, have produced an impressive body of work and have guided captive management techniques. The results of this study support the past strategies for successful infant rearing but also open up consideration of other possibilities and future research.

23 15 CONCLUSION 1. Similar to the results of laboratory studies, this analysis of the zoo population provides ambiguous results due to the number of factors that likely influence litter survival. However these results do support the SSP s strategy of preferentially breeding tamarins with sibling experience because they will likely be more successful. 2. Females without sibling experience have success rates of 80% with their second litter, virtually equal to the success rates of those with sibling experience with their second litters. As breeding recommendations decrease to maintain zero population growth, more animals without sibling experience will be needed to breed and these inexperienced females that were excluded from breeding in the past could still be successful parents after one failed litter. 3. The limitations of a retrospective multi-institutional study using a studbook database prevented the analysis of several additional factors that likely contribute to litter survival. Variations in enclosures and husbandry practices, such as diets and social housing, are not recorded in the studbook. Variations in institutional record keeping and the lack of behavioral data prevent the analysis of group size and carrying time.

24 16 REFERENCES Baker AJ, Woods F Reproduction of the emperor tamarin (Saguinus imperator) in captivity, with comparisons to cotton-top and golden lion tamarins. American Journal of Primatology 26:1-10. Bishop Y, Fienberg S, Holland P Discrete Multivariate Analysis. Cambridge: The MIT Press. Cleveland J, Snowdon CT Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus). Animal Behavior 32(2): Colahan H Cotton-Top Tamarin International Studbook. 5th ed. Houston: Houston Zoo. Inc. Defler TR Primates of Colombia. Rodriguez-Mahecha JV, Rylands A, Mittermeier RA, editors. Bogota: Conservation International. 550 p. Gengozian N, Batson J, Smith T Breeding of tamarins (Saguinus spp.) in the laboratory. In: Kleiman DG, editor. The Biology and Conservation of the Callitrichidae. Washington DC: Smithsonian Institution Press. p Gottman J, Roy A Sequential Analysis: A Guide for Behavioral Researchers. Cambridge: Cambridge Universtiy Press. Hutchins M, Wiese R Beyond genetic and demographic management: The future of the Species Survival Plan and related AAZPA conservation efforts. Zoo Biology 10:

25 17 Johnson LD, Petto AJ, Sehgal PK Factors in the rejection and survival of captive cotton top tamarins (Saguinus oedipus). American Journal of Primatology 25: Kirkwood J, Epstein M, Terlecki A Factors influencing population growth of a colony of cotton-top tamarins. Laboratory Animals 17: Leong KM, Terrell SP, Savage A Causes of mortality in captive cotton-top tamarins (Saguinus oedipus). Zoo Biology 23: Phillips R Cotton-top Tamarin SSP Masterplan Report. Lake Buena Vista, FL: Disney's Animal Kingdom. Price EC The benefits of helpers: Effects of group and litter size on infant care in tamarins (Saguinus oedipus). American Journal of Primatology 26: Savage A, editor The Cotton-top Tamarin Husbandry Manual. Providence, RI: Roger Williams Park Zoo. Savage A, Giraldo LH, Soto LH, Snowdon CT Demography, group composition and dispersal in wild cotton-top tamarin (Saguinus oedipus) groups. American Journal of Primatology 38: Snowdon CT, Savage A, McConnell PB A breeding colony of cotton-top tamarins (Saguinus oedipus). Laboratory Animal Science 35(5): Tardif SD The bioenergetics of parental behavior and the evoluation of alloparental care in marmosets and tamarins. In: Solomon NG, French JA, editors. Cooperative Breeding in Mammals. Cambridge: Cambridge University Press. p

26 18 Tardif SD, Bales K Is infant-carrying a courtship strategy in callitrichid primates? Animal Behaviour 53: Tardif SD, Harrison ML, Simek MA Communal care in marmosets and tamarins: Relation to energetics, ecology, and social organization. In: Rylands A, editor. Marmosets and Tamarins: Systematics, Behaviour, and Ecology. Oxford: Oxford University Press. Tardif SD, Richter CB, Carlson RB Effects of sibling-rearing experience on future reproductive success in two species of Callitrichidae. American Journal of Primatology 6: Washabaugh KF, Snowdon CT, Ziegler TE Variations in care for cotton-top tamarin, Saguinus oedipus, infants as a function of parental experience and group size. Animal Behaviour 63(6): Ziegler T, Washabaugh KF, Snowdon C Responsiveness of expectant male cotton-top tamarins, Saguinus oedipus, to mate's pregnancy. Hormones and Behavior 45: Ziegler TE, Snowdon CT Role of prolactin in paternal care in a monogamous New World primate, Saguinus oedipus. Integrative Neurobiology of Affiliation 807: Ziegler TE, Snowdon CT Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus. Hormones and Behavior 38(3):

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28 20 VITA Name: Address: Address: Hollie Colahan 1513 N MacGregor Houston, TX hjcola@tamu.edu Education: B.S., Biology, Kansas State University, 1995