While many recent advances have been made in the breeding of giant pandas ex situ, historically this species has never reproduced well in captivity. Sexual incompatibility, health problems, low fecundity and a juvenile mortality rate in excess of 70% have contributed to low reproductive success (O'Brien & Knight, 1987; O'Brien et al., 1994; Peng et al, 2001a,b). Wild- and captive-born giant pandas, particularly those captured at a young age, traditionally had difficulty producing offspring in captivity upon becoming adults (Lu & Kemf, 2001). As a result, the ex-situ giant panda population has not been self-sustaining and, until recently, its growth has relied on introducing animals captured from nature. In some cases, this included individuals that appeared ill (rescues) or cubs that were believed to be neglected or abandoned by their mothers. Later field studies, however, revealed that females often leave cubs alone for four to eight hours while foraging, and in one documented case for 52 hours (Lu et al, 1994). Recently, China has
* These authors contributed equivalently to this work.
The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products or organisations imply endorsement by the US Government. Giant Pandas: Biology, Veterinary Medicine and Management, ed. David E. Wildt, Anju Zhang, Hemin Zhang, Donald L. Janssen and Susie Ellis. Published by Cambridge University Press. # Cambridge University Press 2006.
placed a general moratorium on capturing wild giant pandas for captive breeding (Lu & Kemf, 2001), a move that forces the breeding community to develop a self-sustaining population.
The goal, however, is not only ensuring demographic self-sustain-ability but also the maintenance of genetic diversity. The deleterious effects of inbreeding are well recognised (O'Brien, 1994a; Frankham, 1995; Hedrick & Kalinowski, 2001; Frankham et al., 2002). For an outstanding example, one need look no further than the Florida panther, perhaps the flagship species for illustrating the dramatic biological consequences of severe inbreeding (Roelke et al., 1993; O'Brien, 1994b). In the case of this felid subspecies, a small remnant population of pumas underwent a population crash followed by incestuous matings that resulted in a high incidence of malformed sperm, missing or undescended testicles, congenital cardiac abnormalities and high microbial parasite disease loads. There is no doubt that inbreeding depression occurs in poorly managed wildlife populations and must be avoided.
For the giant panda, there are multiple challenges to genetic management (see Chapter 21). For example, there are bureaucratic obstacles to transferring animals between institutions to allow the easier mixing of diverse genes. Additionally, the breeding process itself presents some unusual complications because sexual incompatibility among designated pairs can be high. Historically, a given Chinese giant panda breeding facility has been likely to maintain only one to three unrelated males that are capable of naturally mating. Other males in these collections fail to mate, but generally are available as semen donors for artificial insemination (AI). To maximise both reproductive success and genetic representation, a common management practice is to arrange copulation with one or more competent males during the short two- to three-day oestrus. This then is followed immediately by AI with semen from a male (or males) incapable of natural mating. The result has been that some females have been naturally mated with up to three different males and artificially inseminated with semen from up to another three different males. Thus, paternity has been unknown for the majority of giant panda cubs born in captivity. To allow accurate genetic management and to avoid future inbreeding, it is imperative to verify the paternity of all animals born in captivity.
The first case of giant panda paternity was resolved 20 years ago. At that time, Ling Ling, Studbook 112 (SB 112), the female panda at the Smithsonian's National Zoo in Washington, was the subject of much media attention. For years, Ling Ling had been sexually incompatible with her resident mate Hsing Hsing (SB 121), much to the dismay of the American public. After years of futile courtship, there was a successful mating in 1983. Nonetheless, to maximise the chances of a pregnancy, Ling Ling was also artificially inseminated with semen from Chia Chia (SB 141), the male panda living at London Zoo. A cub was produced which unfortunately died soon after birth. By typing electrophoretic protein polymorphisms, O'Brien and colleagues (1984) determined that Hsing Hsing (and not Chia Chia) indeed sired the cub.
More recently, paternity issues have been addressed using DNA fingerprinting probes (Fang et al., 1997b) and a panel of seven panda-specific microsatellites (Zhang et al., 1994; Ding et al, 2000). Microsatellites represent a class of abundant and highly polymorphic genetic markers, randomly dispersed among the genomes of vertebrate species that are easily isolated and assayed. They are incorporated in genetic maps as tools for locating genes associated with heritable genetic disorders, for human forensic analysis, for paternity assessment and for conservation genetics (Bruford & Wayne, 1993; Goldstein & Schlotterer, 1999; Lu et al., 2001; Driscoll et al., 2002). In this report, we apply mul-tilocus microsatellite assessment to 50 captive giant pandas in the two largest giant panda breeding centres: the Chengdu Research Base of Giant Panda Breeding and the China Conservation and Research Centre for the Giant Panda, Wolong Nature Reserve. We demonstrate parentage of 50 cubs and present a validated pedigree of giant pandas produced in these facilities from 1990 to 2000.
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