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«A Thesis Presented to The Academic Faculty by Pei Sun In Partial Fulfillment of the Requirements for the Degree Master of Science in Psychology ...»

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The Effect of Early Rearing Experience on Adult Reproductive Behavior in Captive

Giant Pandas (Ailuropoda melanoleuca) and Spectacled Bears (Tremarctos ornatus)

A Thesis

Presented to

The Academic Faculty

by

Pei Sun

In Partial Fulfillment

of the Requirements for the Degree

Master of Science in Psychology

Georgia Institute of Technology

November 2004

The Effect of Early Rearing Experience on Adult Reproductive Behavior in Captive

Giant Pandas (Ailuropoda melanoleuca) and Spectacled Bears (Tremarctos ornatus)

Approved by:

Dr. Terry L. Maple, Advisor Dr. Mollie A Bloomsmith Dr. M. Jackson Marr November 19, 2004

ACKNOWLEDGEMENTS

I would very much like to thank Dr. Yanjie Su at Peking University for her training and guidance in animal behavior research during my undergraduate education. I would also like to thank Dr. Terry Maple for his support and encouragement throughout the duration of this project. I also express gratitude to Dr. Mollie Bloomsmith and Dr. M.

Jackson Marr for their feedback and comments to better improve my understanding of research. I would like to thank Dr. Rebecca Snyder for her help in designing this study.

Special thanks to Li Chunlin, Zhong Shunlong, Megan Wilson, and Laurie McGivern, who provided invaluable assistance in data collection.

Finally, I would like to thank the following zoological institutions in China and the United States for providing data for this study. They are, Brookfield Zoo, Chengdu Research Base of Giant Panda Breeding (China), Chengdu Zoo (China), Chongqing Zoo (China), Cincinnati Zoo, Connecticut’s Beardsley Zoo, Erie Zoo, Fuzhou Giant Panda Breeding Center (China), Jackson Zoo, Lincoln Park Zoo, Los Angeles Zoo, Montgomery Zoo, National Zoo, Philadelphia Zoo, Pittsburgh Zoo, Reid Park Zoo, Salisbury Zoo, San Antonio Zoo, San Francisco Zoo, Sedgwick County Zoo, Shanxi Rare Wildlife Rescue & Research Center (China), Silver Spring Park, Tulsa Zoo, and Zoo Atlanta.

iii

TABLE OF CONTENTS

ACKNOWLEDGEMENTS iii

LIST OF TABLES v

LIST OF FIGURES vi SUMMARY vii

INTRODUCTION 1

METHOD 14

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Table 1 Comparison of the Biological Background and Behaviors of 12 Giant Pandas and Spectacled Bears Table 2 Percentage and Number of Giant Pandas and Spectacled 15 Bears that Copulated as Adults Table 3 Number of Giant Panda Subjects within each Duration of 21 Mother Rearing Condition and Their Copulation Status Table 4 Spearman Correlations between Various Independent 24 Variables and Reproductive Success in Giant Pandas Table 5 Chi-square Test for Relationship between Various 27 Independent Variables and the Occurrence of Successful Copulation in Giant Pandas Table 6 Number of Spectacled Bear Subjects within each Duration 28 of Mother Rearing Condition and Their Copulation Status Table 7 Spearman Correlations between Various Independent 30 Variables and Reproductive Success in Spectacled Bears Table 8 Chi-square Test for Relationship between Various 34 Independent Variables and the Occurrence of Successful Copulation in Spectacled Bears

–  –  –

Figure 3 Percentage of Giant Panda Subjects Copulated in each 26 Duration of Mother Rearing Category Figure 4 Percentage of Spectacled Bear Subjects Copulated in each 29 Duration of Mother Rearing Condition Figure 5 Relationship between Duration of Mother Rearing and 30 Reproduction Rate of the Spectacled Bears Figure 6 Percentage of Wild-born vs. Captive-born Subjects that had 31 Copulated as Adults

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The present study examined the relationship between early rearing experience and reproductive competence in captive adult giant pandas (Ailuropoda melanoleuca) and spectacled bears (Tremarctos ornatus). Life history information of 52 giant pandas and 34 spectacled bears were obtained from the International Studbook and by interviewing staff at institutions housing the subjects. The early rearing experience variables included duration of mother rearing, social access within 1-yr period following maternal separation, and birth origin. Correlation, Chi-square, and logistic regression analyses were used to analyze the data. Contrary to findings from studies with other animals, the results generally suggest that early rearing experience is not related to adult reproductive success in giant pandas and spectacled bears. Alternative explanation and limitation of the study were discussed; suggestions were made for future study.

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According to the IUCN (World Conservation Union) Red List categories, the giant panda and the spectacled bear are considered endangered and vulnerable to extinction, respectively (IUCN, 2001). For the giant pandas, only about 1,600 individuals remain in the wild; moreover, the captive population is not self-sustaining (Huang, 1994;

Tang & Zhang, 2001). Both captive giant panda males and females exhibit behavioral problems that lead to reproductive failures (Snyder, 2001; Snyder, Bloomsmith, Zhang, Zhang, & Maple, in press). However, factors that influence adult sexual behaviors are not yet clear (Zhu, Lindburg, Pan, Forney & Wang, 2001). For the spectacled bears, little research has been done and little is known about their reproductive behaviors, even though the captive birth rate is considered not optimal (Rosenthal, 1999). Therefore, factors that contribute to a self-sustaining captive population for both giant pandas and spectacled bears need to be identified.





One determinant of reproductive success is early rearing experience (Beach & Jaynes, 1954; King, 1958; Lindburg & Fitch-Snyder, 1994). Lack of early social experience with conspecifics has been found to affect later reproductive behavior in a variety of species, such as non-human primates (Arling & Harlow, 1967; Beck & Power, 1988; Bloomsmith, Pazol, & Alford, 1994; King & Mellen, 1994; Mason, 1963; Mitchell & Clark, 1968; Simpson, 1978), domestic cats (Mellen, 1992; Rosenblatt, 1965), rodents (Cooke, Chowanadisai, & Breedlove, 2000; Gerall, Ward, & Gerall, 1967; Hole, Einon, & Plotkin, 1986), and birds (Bambaridge, 1962; Myers, Millam, Roudybush, & Grau, 1988). Offspring reared under circumstances with sufficient social input are more likely

–  –  –

abnormal behaviors and are more likely to demonstrate appropriate social, sexual, and maternal behavior as adults (Zhang et al., 2000). In addition, the visual, auditory, and olfactory exchanges between the dam and offspring also have profound and lasting effects on the young animal’s later behavior. This study will extend the findings from past research on various species to the literature on giant pandas and spectacled bears.

Early Rearing Experience Research on Nonhuman Primates Prior research on nonhuman primates has found relationships between early rearing experience and adult sexual behavior. For example, King and Mellen (1994) examined the effect of early rearing experience on adult copulatory behavior of zoo-born chimpanzees (Pan trogologytes). The results showed that 93% of the chimpanzees that were raised by their mother for at least one year copulated as adults, whereas only 44% of chimpanzees that were removed from their mothers at an early age (prior to one month of age) copulated as adults. In addition, significantly higher percentage of chimpanzees that were raised with siblings or peers (53.8%) than chimpanzees that were hand reared alone (30%) copulated as adults. These results supported the contention that certain components of early rearing experience greatly influence the sexual competence of adult chimpanzees.

Beck and Power (1988) conducted an exhaustive survey and obtained the standardized biographies of every gorilla (Gorilla gorilla gorilla) held in North America in order to determine the factors associated with reproductive success. The data demonstrated that when defining reproductive success as number of infants per year of

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However, although there was no difference between the reproductive success of motherreared and hand-reared males, mother-reared females were reproductively more successful than hand-reared females. In addition, first-year social access to conspecifics appeared to be associated with higher reproductive success among captive-born females.

Given the equal mating opportunities, reproductively unsuccessful animals were less likely to exhibit normal sexual behavior than successful ones. The investigators concluded that many cases of reproductive failure were due to lack of early social experience with conspecifics.

Similarly, early rearing experience has been found to be critical for exhibiting appropriate reproductive behavior as adults in rhesus monkeys (Macaca mulatta) (Arling & Harlow, 1967; Harlow, 1965; Mason, 1963; Mitchell & Clark, 1968; Simpson, 1978).

Male and female captive-born rhesus monkeys that were raised in isolation from other monkeys showed deficiencies in sexual behavior (Mason, 1963, Mitchell & Clark, 1968).

Inadequate early experience made it difficult or impossible for the young animals to pass from the stage of infantile sexuality into the normally subsequent stages of differential sexuality and adult heterosexuality (Harlow, 1965; Simpson, 1978). Female rhesus monkeys separated from mothers at birth and raised isolated from peers were distinctly deficient in providing maternal care compared to feral-raised females (Arling & Harlow, 1967). Furthermore, it has been demonstrated that early social deprivation influences male sexual behavior more strongly than it does female sexual behavior (Goldfoot, 1977;

Sackett, 1974). It was found that all of the isolate-reared male rhesus monkeys in an

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20% of the isolate-reared females in the experimental group (Sackett, 1974).

Early Rearing Experience Research on Cats Mellen (1992) studied the effects of human rearing on adult sexual behavior of domestic cats (Felis catus). Female cats were randomly assigned to three different conditions: human-raised alone, human-raised with a sibling, and mother-raised with a sibling. When the subjects reached their sexual maturity, which was defined by the first estrous period, each of them was paired with a sexually experienced male, and copulatory behavior was observed. Data showed that the human-raised alone females displayed extreme aggression toward their male partners. Human-raised female cats were less likely to reproduce than mother-raised females. The researcher suggested that whenever possible, human-raising of felids should be avoided.

Early Rearing Experience Research on Birds Myers et al. (1988) studied the influence of early rearing experience on the reproductive success of cockatiels (Nymphicus hollandicus). It was found that handreared females were more likely to lay eggs and laid more eggs than parent-reared females, but often laid them on the cage floor rather than in nest-boxes, which reduced hatching success. Pairs containing hand-reared males were less likely than pairs containing parent-reared males to produce fertile eggs, and fledging occurred only in pairs containing parent-reared males. Researchers pointed out that early rearing experience is important for males to learn characteristics of the opposite sex, and for both males and females to learn characteristics of nest-sites.

–  –  –

In general, giant pandas are inefficient at reproducing offspring, which may contribute to their status as endangered species (Wang, Kai, & Tan, 1993). The reproductive inefficiency observed in giant pandas may be partially attributed to the following ontogenetic characteristics. Giant panda females only come into estrus once a year, during the spring. The entire estrous period may last from 12-25 days, but the receptive period (also called peak estrus) only lasts for about 2-7 days (Domico, 1988;

Schaller, Hu, 2001; Hu, Pan, & Zhu, 1985; Wang et al., 1993). Moreover, giant pandas are very particular about their sexual partners, which makes mating difficult even if a panda is in heat (Wang et al., 1993). Further, quite a few females do not let out any fertile ovum when in heat (Wang et al., 1993). They have a delayed embryo implantation for several months. That is, the fertilized ovum only develops to the blastocyst stage and then floats free in the uterus for one to three-and-a-half months before implanting (Domico, 1988; Schaller, Hu, Pan, & Zhu, 1985). In addition, the giant panda newborn is extremely tiny and weak, requiring profound maternal cares from the mother. It typically weighs about 2.6-5.3 ounces (75-150 grams), which is only one thousand percent of its mother’s weight. The cub is blind at birth and is almost naked. It opens its eyes at around six weeks of age, and it cannot see until 120 days after birth. The cub is fully furred at about 25 days of age, and it starts to walk at 4 months of age (Hu, 2001; Wang et al., 1993;

Zhu, Lindburg, Pan, Forney, & Wang, 2001). The mother holds the cub to her breast with her forepaws almost continuously for the first three weeks of the cub’s life and provides an amazing amount of care and attention (Domico, 1988; Schaller et al., 1985). Above 50% of the time, the female will give birth to twins. However, due to the extremely high

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care of two cubs at the same time. Typically, only one of them survives, while the other is usually abandoned and starves to death or becomes accidentally crushed beneath the weight of the mother’s body (Domico, 1988; Schaller et al., 1985; Wang et al., 1993;

Zhang et al., 2000). Finally, male giant pandas have a very short penis (Domico, 1988;

Wang et al., 1993), and they seldom reach sexual climax. The amount of their seminal fluids is small, and the sperm malformation rate is high (Wang et al., 1993). Due to the above facts, giant pandas face dramatic reproductive difficulties in general. As such, a long-term goal of developing a self-sustaining captive population of giant pandas has been established in order to support a long-term, viable population in the wild (Zheng, Zhao, Xie, Wildt, & Seal, 1997). However, both female and male captive giant pandas exhibit behavioral problems that reduce the likelihood of reproduction success (Snyder, 2001, Zheng et al, 1997).



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