The assessment of reproductive potential in Micronesian kingfisher pairs

The Micronesian kingfisher Halcyon cinnamomina cinnamomina is now extinct in the wild and survives only in U.S. zoos. Although pairs have reproduced in captivity, the captive breeding program has been plagued with inconsistencies in reproductive success. One problem has been determining whether birds housed as reproductive pairs have really established pairbonds. The behavior of newly paired birds may provide information that could be used to predict future reproductive success. Observations conducted for 90 min immediately after introduction of five new pairs at three institutions suggest that the specific behavioral combination of high nest activity and low aggression may indicate reproductive compatibility. Pairs that ultimately produced surviving offspring were less aggressive and engaged in more nest activity than pairs that were not productive. Observations conducted on four of these pairs for an additional month after introduction failed to provide additional information relevant to the assessment of pair status. Although long-term behavioral observations are also desirable, quick assessments such as these may be useful for determining the reproductive potential of more pairs than would be possible using traditional methods. The identification of sexually compatible pairs is a critical step toward the ultimate goal of re-establishing this species in the wild. Zoo Biol 17:425–432, 1998. © 1998 Wiley-Liss, Inc.     

Multiscale Habitat Use and Selection in Cooperatively Breeding Micronesian Kingfishers

Abstract: Information about the interaction between behavior and landscape resources is key to directing conservation management for endangered species. We studied multi-scale occurrence, habitat use, and selection in a cooperatively breeding population of Micronesian kingfishers (Todiramphus cinnamominus) on the island of Pohnpei, Federated States of Micronesia. At the landscape level, point-transect surveys resulted in kingfisher detection frequencies that were higher than those reported in 1994, although they remained 15-40% lower than 1983 indices. Integration of spatially explicit vegetation information with survey results indicated that kingfisher detections were positively associated with the amount of wet forest and grass-urban vegetative cover, and they were negatively associated with agricultural forest, secondary vegetation, and upland forest cover types. We used radiotelemetry and remote sensing to evaluate habitat use by individual kingfishers at the home-range scale. A comparison of habitats in Micronesian kingfisher home ranges with those in randomly placed polygons illustrated that birds used more forested areas than were randomly available in the immediate surrounding area. Further, members of cooperatively breeding groups included more forest in their home ranges than birds in pair-breeding territories, and forested portions of study areas appeared to be saturated with territories. Together, these results suggested that forest habitats were limited for Micronesian kingfishers. Thus, protecting and managing forests is important for the restoration of Micronesian kingfishers to the island of Guam (United States Territory), where they are currently extirpated, as well as to maintaining kingfisher populations on the islands of Pohnpei and Palau. Results further indicated that limited forest resources may restrict dispersal opportunities and, therefore, play a role in delayed dispersal and cooperative behaviors in Micronesian kingfishers.     

Sex determination of Pohnpei Micronesian Kingfishers using morphological and molecular genetic techniques

ABSTRACT.   Conservation-oriented studies of Micronesian Kingfishers ( Todiramphus cinnamominus ) have been hindered by a lack of basic natural history information, despite the status of the Guam subspecies ( T. c. cinnamominus ) as one of the most endangered species in the world. We used tissue samples and morphometric measures from museum specimens and wild-captured Pohnpei Micronesian Kingfishers ( T. c. reichenbachii ) to develop methods for sex determination. We present a modified molecular protocol and a discriminant function that yields the probability that a particular individual is male or female. Our results revealed that females were significantly larger than males, and the discriminant function correctly predicted sex in 73% (30/41) of the individuals. The sex of 86% (18/21) of individuals was correctly assigned when a moderate reliability threshold was set. Sex determination using molecular genetic techniques was more reliable than methods based on morphology. Our results will facilitate recovery efforts for the critically endangered Guam Micronesian Kingfisher and provide a basis for sex determination in the 11 other endangered congeners in the Pacific Basin.     

Early maternal behavior of wild cheetahs: Implications for captive husbandry

Against a background of poor breeding success and cub survival in captive cheetahs, a knowledge of the early maternal behavior in the wild may yield useful information for comparison with the captive situation. This paper documents the types of lair sites used by mothers to conceal their newborn cubs in the wild situation, and details patterns of maternal behavior observed during this period. Four kinds of lairs were used by cheetah mothers, and the amount of protection from the elements and predators was assessed for each. Lair type appeared to have little effect on cub survival. Cubs were concealed in lairs for 8.2 weeks on average, although larger litters tended to leave lairs earlier. During this period, cubs were moved to new lairs approximately every 5.6 days. Cubs were left for an average of 9.6 hours while their mothers went hunting, but mothers virtually always returned to them around nightfall, even if they failed to catch any prey. Maternal neglect and cub abandonment, which account for many cub deaths in captivity, are abnormal in the wild, except when prey is very scarce. Improved husbandry techniques, such as the provision of multiple, secluded nest boxes, and remote monitoring conditions should promote breeding success in captivity. In addition, noise and human disturbance should be minimized.     

Assortative mating among animals of captive and wild origin following experimental conservation releases

Captive breeding is a high profile management tool used for conserving threatened species. However, the inevitable consequence of generations in captivity is broad scale and often-rapid phenotypic divergence between captive and wild individuals, through environmental differences and genetic processes. Although poorly understood, mate choice preference is one of the changes that may occur in captivity that could have important implications for the reintroduction success of captive-bred animals. We bred wild-caught house mice for three generations to examine mating patterns and reproductive outcomes when these animals were simultaneously released into multiple outdoor enclosures with wild conspecifics. At release, there were significant differences in phenotypic (e.g. body mass) and genetic measures (e.g. G_st and F) between captive-bred and wild adult mice. Furthermore, 83% of offspring produced post-release were of same source parentage, inferring pronounced assortative mating. Our findings suggest that captive breeding may affect mating preferences, with potentially adverse implications for the success of threatened species reintroduction programmes.     

Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild

Supplementation of wild populations with captive-bred organisms is a common practice for conservation of threatened wild populations. Yet it is largely unknown whether such programmes actually help population size recovery. While a negative genetic effect of captive breeding that decreases fitness of captive-bred organisms has been detected, there is no direct evidence for a carry-over effect of captive breeding in their wild-born descendants, which would drag down the fitness of the wild population in subsequent generations. In this study, we use genetic parentage assignments to reconstruct a pedigree and estimate reproductive fitness of the wild-born descendants of captive-bred parents in a supplemented population of steelhead trout (Oncorhynchus mykiss). The estimated fitness varied among years, but overall relative reproductive fitness was only 37 per cent in wild-born fish from two captive-bred parents and 87 per cent in those from one captive-bred and one wild parent (relative to those from two wild parents). Our results suggest a significant carry-over effect of captive breeding, which has negative influence on the size of the wild population in the generation after supplementation. In this population, the population fitness could have been 8 per cent higher if there was no carry-over effect during the study period.     

Sex identification of parrots,toucans, and curassows by PCR: Perspectives for wild and captive population studies

Methods for the identification of the sex of bird species without external sexual dimorphism are specially important in field studies and for captive breeding of endangered taxa. We confirmed the accuracy of a polymerase chain reaction (PCR)-based method to identify the sex in three disparate avian orders that included 31 species of parrot, two species of toucan, and eight species of curassow, for which many individuals were previously sexed. In each case, two DNA fragments were amplified in females and one in males with the use of a single set of primers. This method was also tested on unsexed birds of 13 other species of parrot and five species of toucan. The same kind of polymorphism was detected in each. The PCR products of parrots and toucans could be separated in simple agarose gels, while the curassows' products could only be distinguished in acrylamide gels. An advantage of this DNA test is that samples of blood or feathers can be easily collected and stored at room temperature, which is of particular importance for studies of wild birds. Zoo Biol 17:415–423, 1998. © 1998 Wiley-Liss, Inc.     

Body weights of wild and captive lemurs

The mean body weight of a species is often used as a summary measure of size in evolutionary and functional studies. Additionally, body weight is often used to assess the health of captive animals. Contrasts of the captive and wild body weights of a species can be used to examine the effects of captivity on the species. We provide an analysis of adult body weight in nine taxa of Malagasy lemurs. We compare weights of wild and captive lemurs and provide analyses of relationships between captive weight variation and management actions. Body weights are derived from a number of sources, the majority from the Duke University Primate Center (DUPC) capture and husbandry records. Captive animals are, on average, heavier than wild conspecifics. However, the difference is significant in only three taxa (Hapalemur griseus griseus, Eulemur coronatus, E. macaco flavifrons). Based on a retrospective analysis of DUPC records, we assess patterns of adult weight relative to caging conditions and evaluate changes in mean weight over a period of approximately 20 years. Cage type appears to have no effect on body weight. Mean weight has decreased for some taxa housed at the DUPC over time. We calculate a weight-based criterion for identifying obese animals and demonstrate that obesity is not currently a prevalent condition in DUPC lemurs. Examinations of the physiological correlates of excessive weight, and especially relationships between weight and reproductive success, await further analysis. These analyses need to be based, in part, on reliable measures of body weight. We suggest that systematic weighing of wild and captive animals is important for further examinations of the overall health of captive animals as well as for studies ranging in scope from evolutionary to clinical. Zoo Biol 16:17–30, 1997. © 1997 Wiley-Liss, Inc.     

Retrospective investigation of captive red wolf reproductive success in relation to age and inbreeding

The critically endangered red wolf (Canis rufus) has been subject to a strictly managed captive breeding program for three decades. A retrospective demographic analysis of the captive population was performed based on data from the red wolf studbook. Data analyses revealed a decrease in the effective population size relative to the total population size, and changes in age structure and inbreeding coefficients over time. To varying degrees, the probability of successful breeding and litter sizes declined in association with increasing dam age and sire inbreeding coefficients. Neonate survival also declined with increasing dam age. Recent changes in strategies regarding breed-pair recommendations have resulted in moderate increases in reproductive success. Zoo Biol 28:214–229, 2009. © 2009 Wiley-Liss, Inc.     

Effects of early rearing experience on adult behavior and nesting in captive Hawaiian crows (Corvus hawaiiensis)

Behavioral data were collected during the breeding season on eight pairs of Hawaiian crows (Corvus hawaiiensis) housed at two facilities on different islands. All data were collected from videocamera time‐lapse recordings of the nesting platforms. Behaviors included frequency of nest cup manipulation, percent of time spent on nest, allopreening, play, and stereotypy. The number of breeding pairs increased from four in 1996 to six in 1997, to seven in 1998, and to eight in 1999. Five of the older birds (three males and two females) were solitary‐reared for most if not all of their first year, while the remaining 12 birds were all socially reared. Significant differences were found between isolate‐ and socially‐reared birds, with isolate‐reared birds having higher rates of solo play (P = 0.0041) and stereotypies (P = 0.0090). Pairs that were comprised of at least one isolate‐reared bird engaged in significantly less allopreening (P = <0.0001) than pairs in which both birds were socially reared. From 1996 to 1999, 87 eggs were laid, with a mean of 1.88 ± 0.24 SEM eggs per clutch. Only three females produced clutches every year, and they were responsible for 85.1% of the eggs laid. Although not significant, the mean number of clutches produced per pair decreased from 2.50 ± 0.65 in 1996 to 0.87 ± 0.99 in 1999. Age of females does not appear to be a critical factor in the decrease in clutch production. New pairing combinations are under way in an effort to improve propagation in this highly endangered species. Zoo Biol 21:59–75, 2002. © 2002 Wiley‐Liss, Inc.     

Thermal and trophic habitats of the leatherback turtle during the nesting season in French Guiana

Understanding environmental cues determining behaviour and habitat use of species of conservation concern is crucial if one aims at implementing sustainable management of these natural resources. In this way, here, we investigate the thermal and trophic conditions encountered by the critically endangered leatherback sea turtle Dermochelys coriacea during its nesting season in French Guiana where high bycatch rates have been reported.Mean sea water temperatures obtained in situ by animal-borne recorders were 26.6 ± 0.7 °C in the water column, with all but one turtle remaining in water > 25 °C during the inter-nesting interval. In terms of prey availability, regular jellyfish stranding events were recorded during the nesting season, on a 1.25-km long section of the nesting beach. The occurrence of jellyfish was supported by benthic trawls performed on the continental shelf, with a total of 45.4 kg of jellyfish collected in 3.5 h exclusively in coastal waters 10 to 20 m deep where water transparency was between 0.8 and 3 m. This is consistent with the at sea distribution area of gravid leatherbacks during their inter-nesting intervals, as they spent almost 70% of their time diving in shallow (< 20 m deep) waters in front of the Maroni River estuary. In French Guiana, leatherback's gelatinous prey are thus present in very shallow water close to the nesting site and may be easily exploited by active gravid leatherbacks. This suggests that French Guiana female leatherbacks may be influenced by local trophic conditions and actively prospect productive areas overlapping with local fisheries ground.     

Evaluation of behavioral factors influencing reproductive success and failure in captive giant pandas

The giant panda (Ailuropoda melanoleuca) breeding center in Wolong, China, has experienced a recent dramatic increase in reproduction, with the population nearly tripling in the past 7 years. Much of this success comes from the development of behavioral management strategies, guided by the application of scientific knowledge. Here we present statistics that illuminate where reproductive problems have occurred, and discuss remedial actions taken with individual animals. During each year of this study (1996–2000), 93% of the females experienced estrus, 72% copulated, and 51% gave birth. Two‐thirds of the males mated each year. Most instances of mating failure were attributed to male behavior. In nearly half of mating failures, the male mounted but did not copulate. In about one‐third of mating failures, the male lacked sexual motivation, and showed excessive aggression 20% of the time. The males varied, and some were more likely to show interest in estrous females in neighboring enclosures and/or mate successfully during introductions. Copulation time was unrelated to reproductive success, but more insemination events (matings and artificial inseminations (AIs) combined) may be related to twinning. We suspect that temperament, stress, and husbandry practices play a role in isolated cases of reproductive failure in females, both pre‐ and postcopulation. Pregnancy or conception failure occurred in 35% of females inseminated naturally or through artificial insemination (AI). Behavioral management at Wolong is holistic and emphasizes biological relevance, including enrichment and well‐being, intensive monitoring of signs of estrus, and male–female familiarization and olfactory communication during the mating season. Zoo Biol 23:15–31, 2004. © 2004 Wiley‐Liss, Inc.     

Hereditary defects and conservation genetic management of captive populations

The occurrence of hereditary disorders in conservation breeding programs may severely hamper the overall aim of such programs. The obstacles that arise in this context and the particular management strategies needed to deal with the problems are yet to be adequately addressed. Results from a literature review indicate that hereditary disorders may be fairly common in zoo populations. An example with albinism in a captive brown bear population bred in Nordic zoos is presented. It is demonstrated that the segregation pattern is consistent with an autosomal recessive allele, and carrier probabilities of live animals indicate that the allele occurs in high frequency in the present population. Removing animals with a probability of carrying the allele will result in loss of founder alleles considered particularly valuable. Zoo Biol 18:81–99, 1999. © 1999 Wiley‐Liss, Inc.     

Role of inbreeding depression and purging in captive breeding and restoration programmes

Inbreeding depression is a major force affecting the evolution and viability of small populations in captive breeding and restoration programmes. Populations that experience small sizes may be less susceptible to future inbreeding depression because they have been purged of deleterious recessive alleles. We review issues related to purging, as they apply to the management of small populations, and discuss an experiment we conducted examining purging in populations of mosquitofish (Gambusia affinis). Purging is an important process in many small populations, but the literature contains a diversity of responses to purging both within and among studies. With the exception that slow inbreeding results in more purging and less threat to population viability, there seem to be few consistent trends that aid in prediction of how a purging event will affect a population. In our examination of purging on population viability in mosquitofish, single or multiple bottlenecks do not appear to have resulted in any purging of the influence of genetic load on population growth. Rather, serial bottlenecks resulted in a marked decline in population growth and an increase in extinction. Our results, taken together with those of reviewed studies, suggest that in small populations there is great uncertainty regarding the success of any single purging event in eliminating inbreeding depression, together with the high likelihood that purging will depress population viability through the fixation of deleterious alleles. In management of captive breeding and restoration programmes, the common practice of avoiding inbreeding and small population sizes should be followed whenever possible.     

The effects of captivity on the morphology of captive, domesticated and feral mammals

• 1 The effects of captivity on the behaviour of wild and domestic animals have been relatively well studied, but little has been published on morphological changes in wild animals in captivity. We review the evidence for changes in a wide variety of mammalian taxa, with non-mammalian examples where relevant.
• 2 We consider the morphological effects of the process of domestication, and compare changes in both hard and soft tissues in captive and domestic animals with those in their wild counterparts. These include skull shape differences, brain size reduction, postcranial adaptations and digestive tract changes.
• 3 We also summarize studies that have looked at morphological change in feral animals in comparison with their wild and domestic ancestors, and consider their use as an analogue for morphological change in captive-bred animals that have been released into the wild.
• 4 We then discuss the importance of this work for the wider aims of conservation of endangered species and captive breeding over many generations, and emphasize the importance of studying these changes now, while for many species, the process is just beginning rather than many generations down the line, or immediately prior to release, where survival of captive-bred animals may be severely compromised.

     

Captive breeding for reintroduction: influence of management practices and biological factors on survival of captive kaki (black stilt)

An important component of the restoration strategy for the critically endangered kaki or black stilt (Himantopus novaezelandiae) is captive breeding for release. Since 1981 1,879 eggs were collected from wild and captive pairs, with birds laying up to four clutches. Eggs were incubated artificially and most chicks reared by hand until released as juveniles (about 60 days) or sub‐adults (9–10 months). Because survival in captivity is a significant determinant of the number of birds available for release, we wished to identify sources of variation in mortality to assess potential impacts of management on productivity. Hatchability was 78% for captive‐laid eggs and 91% for wild‐laid eggs. Survival of hatched eggs was 82% by 10 months of age for both wild and captive birds. Most egg mortality occurred early in incubation and around hatching: the timing of mortality was unaffected by whether birds were captive or wild, hybrid or pure kaki, or when eggs were laid. Heavier hatchlings showed higher initial survival, as did chicks from wild parents. Hatchlings from fourth‐laid eggs showed lowest survival, even though hatchling mass tended to increase with hatch order. Survival of chicks subjected to major health interventions was 69% after 4 months. No differences in survival were found between different genders, hybrids and pure kaki, hand‐reared or parent‐reared birds, chicks hatching early or late in the season, different seasons, different‐sized groups of chicks, chicks reared in different brooders, juveniles kept in different aviaries, and chicks from subsequent clutches. Birds subjected to minor health interventions were equally likely to survive as healthy chicks (82%). Survival was high despite aggressive management (quadruple clutching and collecting late in the season). Differences between captive and wild birds suggest further improvements could be made to captive diet. Wide variation in hatchability between parent pairs substantiates the practice of breaking up poorly performing pairs. Zoo Biol 0:1–16, 2005. © 2005 Wiley‐Liss, Inc.     

Ultrasound examination and behavior scoring of captive broadnose sevengill sharks,Notorynchus cepedianus (Peron, 1807)

Serial ultrasound examination of four mature female sevengill sharks (Notorynchus cepedianus) was carried out over 18 months. Monitoring the reproductive cycle and development of follicles and fetuses in sharks in a noninvasive manner using this technique has not been reported previously. Sharks were caught out of the “Oceanarium” tank by divers using a specially made catch‐out bag, and brought to a holding area for examination. A behavior scoring system was used to monitor the impact of regular handling on the well‐being of the animals. Ultrasound showed the growth and regression of follicles in sevengill ovaries, and allowed an approximation of the reproductive stage of these sharks. Monitoring behavior at five time points during the procedure showed that regular handling of sharks for clinical studies could be done with minimal impact on animal welfare. The ability to follow reproductive events in elasmobranches using ultrasonography is an important step in the application of assisted reproductive technology in these species. Assisted reproductive technology, such as monitoring female reproductive cycles and artificial insemination, could potentially be used to maintain genetic diversity and compliment aquaria‐based breeding programs for endangered species such as the gray nurse shark (Carcharias taurus). Zoo Biol 26:383–395, 2007. © 2007 Wiley‐Liss, Inc.     

Development of restoration techniques for Hawaiian thrushes: Collection of wild eggs,artificial incubation,hand‐rearing,captive‐breeding,and re‐introduction to the wild

From 1995 to 1999, two species of endemic Hawaiian thrushes, `Oma`o (Myadestes obscurus) and Puaiohi (M. palmeri), were captive‐reared and re‐introduced into their historic range in Hawai`i by The Peregrine Fund, in collaboration with the U.S. Geological Survey–Biological Resources Division (BRD) and the Hawai`i State Department of Land and Natural Resources. This paper describes the management techniques that were developed (collection of wild eggs, artificial incubation, hand‐rearing, captive propagation, and release) with the non‐endangered surrogate species, the `Oma`o; techniques that are now being used for recovery of the endangered Puaiohi. In 1995 and 1996, 29 viable `Oma`o eggs were collected from the wild. Of 27 chicks hatched, 25 were hand‐reared and released into Pu`u Wa`awa`a Wildlife Reserve. Using the techniques developed for the `Oma`o, a captive propagation and release program was initiated in 1996 to aid the recovery of the endangered Puaiohi. Fifteen viable Puaiohi eggs were collected from the wild (1996–1997) to establish a captive breeding flock to produce birds for re‐introduction. These Puaiohi reproduced for the first time in captivity in 1998 (total Puaiohi chicks reared in captivity 1996–1998 = 41). In 1999, 14 captive‐bred Puaiohi were re‐introduced into the Alaka`i Swamp, Kaua`i. These captive‐bred birds reproduced and fledged seven chicks in the wild after release. This is the first endangered passerine recovery program using this broad spectrum of management techniques (collection of wild eggs, artificial incubation, hand‐rearing, captive‐breeding, and release) in which re‐introduced birds survived and bred in the wild. Long‐term population monitoring will be published separately [BRD, in preparation]. Zoo Biol 19:263–277, 2000. © 2000 Wiley‐Liss, Inc.