Captive Breeding and Reintroduction Evaluation Criteria: a Case Study of Peninsular Bighorn Sheep

Abstract: Captive breeding and reintroduction programs are rarely evaluated, and assessment criteria vary widely. We used the following criteria to evaluate a bighorn sheep ( Ovis canadensis ) augmentation program: (1) survival and recruitment rates in the captive population, (2) survival of released animals, (3) recruitment of released animals, (4) growth rate of the reintroduced or augmented population, and (5) establishment of a viable wild population. Captive bighorn survival and recruitment was high, averaging 0.98 (SD = 0.05) and 71.0% (SD = 19.4), respectively. Annual survival of free-ranging captive-reared bighorn ( n = 73, x = 0.80, SD = 0.11) did not differ (   Z = −0.85, p = 0.40; n = 14) from survival of wild-reared bighorn ( n = 43, x = 0.81, SD = 0.12). Recruitment was unusually low for both captive-reared (  x = 13.7%, SD = 0.24) and wild-reared ewes (  x = 13.7%, SD = 0.20). Although reintroduction did not result in population growth or establishment of a viable population, it helped prevent extirpation of the reinforced deme, preserved metapopulation linkage, and aided habitat preservation. Chronic low recruitment and low adult survivorship precluded achievement of criteria 3–5. Environmental conditions in the release area also appeared to hinder program success. Standard evaluation criteria for ongoing reintroductions allow for informative assessments and facilitate comparisons needed to refine reintroduction science as a recovery tool for threatened or endangered populations.     

Demographic Models and Reality in Reintroductions: Persian Fallow Deer in Israel

Abstract:  Because most reintroduced species are rare, data on their dynamics are scarce. Consequently, reintroduction programs often rely on data from other species or captive populations to project the performance of the reintroduced population in the wild. We compared the reproductive success and survival of a Persian fallow deer ( Dama mesopotamica ) population reintroduced in Israel over the first 5 years of the project with the survival and reproduction parameters estimated while planning the reintroduction. In addition, we compared the actual growth of the wild population with the growth originally projected by a computer model in the original reintroduction program. We monitored 74 radio-collared individuals (57 females and 17 males) released semiannually 1996–2001. Survival during the first year after release was lower than later years (0.90 and 0.82 versus 0.95 and 0.88, for females and males, respectively). Such an impact was not anticipated in the original plan, but overall survival was higher than originally projected. As assumed in the reintroduction program, reproductive success improved significantly with time since release and overall, was higher than expected. The mean number of animals released annually was lower than planned. Overall, the growth of the reintroduced population was slower than projected, but the deviation was close to confidence limits and the pattern similar. After 5 years it appears that the original time frame of 8–10 years for project completion can be met or at worst will cause a 1-year delay. Over the short term of 5 years, projection models in reintroduction programs are useful tools for assessing the sustained use of the breeding core, depicting the dynamics of the population in the wild, providing a relatively accurate time frame for the successful completion of the project, and assessing project success.     

Estimates of Natural Selection in a Salmon Population in Captive and Natural Environments

Abstract:  Captive breeding is a commonly used strategy for species conservation. One risk of captive breeding is domestication selection—selection for traits that are advantageous in captivity but deleterious in the wild. Domestication selection is of particular concern for species that are bred in captivity for many generations and that have a high potential to interbreed with wild populations. Domestication is understood conceptually at a broad level, but relatively little is known about how natural selection differs empirically between wild and captive environments. We used genetic parentage analysis to measure natural selection on time of migration, weight, and morphology for a coho salmon ( Oncorhynchus kisutch ) population that was subdivided into captive and natural components. Our goal was to determine whether natural selection acting on the traits we measured differed significantly between the captive and natural environments. For males, larger individuals were favored in both the captive and natural environments in all years of the study, indicating that selection on these traits in captivity was similar to that in the wild. For females, selection on weight was significantly stronger in the natural environment than in the captive environment in 1 year and similar in the 2 environments in 2 other years. In both environments, there was evidence of selection for later time of return for both males and females. Selection on measured traits other than weight and run timing was relatively weak. Our results are a concrete example of how estimates of natural selection during captivity can be used to evaluate this common risk of captive breeding programs.     

Using a common commensal bacterium in endangered Takahe as a model to explore pathogen dynamics in isolated wildlife populations

Predicting and preventing outbreaks of infectious disease in endangered wildlife is problematic without an understanding of the biotic and abiotic factors that influence pathogen transmission and the genetic variation of microorganisms within and between these highly modified host communities. We used a common commensal bacterium, Campylobacter spp., in endangered Takahe (Porphyrio hochstetteri) populations to develop a model with which to study pathogen dynamics in isolated wildlife populations connected through ongoing translocations. Takahe are endemic to New Zealand, where their total population is approximately 230 individuals. Takahe were translocated from a single remnant wild population to multiple offshore and mainland reserves. Several fragmented subpopulations are maintained and connected through regular translocations. We tested 118 Takahe from 8 locations for fecal Campylobacter spp. via culture and DNA extraction and used PCR for species assignment. Factors relating to population connectivity and host life history were explored using multivariate analytical methods to determine associations between host variables and bacterial prevalence. The apparent prevalence of Campylobacter spp. in Takahe was 99%, one of the highest reported in avian populations. Variation in prevalence was evident among Campylobacter species identified. C. sp. nova 1 (90%) colonized the majority of Takahe tested. Prevalence of C. jejuni (38%) and C. coli (24%) was different between Takahe subpopulations, and this difference was associated with factors related to population management, captivity, rearing environment, and the presence of agricultural practices in the location in which birds were sampled. Modeling results of Campylobacter spp. in Takahe metapopulations suggest that anthropogenic management of endangered species within altered environments may have unforeseen effects on microbial exposure, carriage, and disease risk. Translocation of wildlife between locations could have unpredictable consequences including the spread of novel microbes between isolated populations.     

Linking Wild and Captive Populations to Maximize Species Persistence: Optimal Translocation Strategies

Abstract:  Captive breeding of animals is widely used to manage endangered species, frequently with the ambition of future reintroduction into the wild. Because this conservation measure is very expensive, we need to optimize decisions, such as when to capture wild animals or release captive-bred individuals into the wild. It is unlikely that one particular strategy will always work best; instead, we expect the best decision to depend on the number of individuals in the wild and in captivity. We constructed a first-order Markov-chain population model for two populations, one captive and one wild, and we used stochastic dynamic programming to identify optimal state-dependent strategies. The model recommends unique sequences of optimal management actions over several years. A robust rule of thumb for species that can increase faster in captivity than in the wild is to capture the entire wild population whenever the wild population is below a threshold size of 20 females. This rule applies even if the wild population is growing and under a broad range of different parameter values. Once a captive population is established, it should be maintained as a safety net and animals should be released only if the captive population is close to its carrying capacity. We illustrate the utility of this model by applying it to the Arabian oryx ( Oryx leucoryx ). The threshold for capturing the entire Arabian oryx population in the wild is 36 females, and captive-bred individuals should not be released before the captive facilities are at least 85% full.     

New Approaches Toward a Better Understanding of the Decline of Takahe (Porphyrio mantelli) in New Zealand

Island populations of endemic birds are known to be particularly susceptible to extinction. This paper focuses on factors behind past and present declines of the highly endangered Takahe ( Porphyrio mantelli ), a flightless rail endemic to New Zealand. Subfossil evidence indicates that Takahe were once found throughout this island nation, being most abundant along forest margins and streams in lowland regions. Their numbers have declined dramatically since human colonization about 800–1000 years ago, probably due to a combination of habitat destruction and hunting by early Polynesian settlers. Today, the wild Takahe population consists of about 100 adult birds in an isolated alpine habitat and approximately 30 individuals recently released on several small offshore islands. Despite protection and intensive management, including removal of an introduced competitor (red deer, Cervus elaphus ), the alpine population has continued to decline. In contrast, the Takahe's nearest relative, the Pukeko ( Porphyrio porphyrio ) has expanded its range across New Zealand despite heavy hunting pressure since its colonization from Australia less than 1000 years ago. We suggest that, unlike Pukeko, Takahe lack appropriate behavioral responses to cope with mammalian predators such as stoats ( Mustela erminea ), which have been introduced relatively recently by European colonists. A study comparing predator defense behavior between these two closely related species is currently underway.     

Sex-specific differences in site fidelity and the cost of dispersal in yellow-headed blackbirds

Male migratory birds tend to be more faithful than females to previous breeding sites, suggesting sex differences in costs or benefits of dispersal. In Illinois, greater site fidelity by male yellow-headed blackbirds (Xanthocephalus xanthocephalus) was associated with reduced reproductive success the following year for dispersers relative to non-dispersers. Dispersing females suffered no reduction in reproductive success the following year. Males that attracted few social mates, and thus had low reproductive success, were more likely to disperse, whereas females dispersed in response to low-patch reproductive success, regardless of their individual performance. Males that dispersed appeared to be successful acquiring territories because none was observed as a floater. The rate of dispersal by males in this low-density population was greater than in more dense populations where dispersing males may be less successful at acquiring territories. Despite success at obtaining territories, males that dispersed acquired territories on the periphery of wetlands where fewer females nested, resulting in lower reproductive success. In the second year after dispersing, however, males moved onto more central territories where they acquired larger harems. Thus, dispersal by males may be a long-term strategy requiring at least 2 years for benefits to be realized. Long-term success was enhanced because dispersing males moved to wetlands on which reproductive success was higher than on the wetlands they left. In addition to demonstrating that both individual and patch reproductive success affect dispersal decisions, these data indicate that when evaluating costs and benefits of dispersal, researchers should use a time frame beyond 1 year.     

Asymmetric costs favor female desertion in the facultatively polyandrous northern flicker (Colaptes auratus): a removal experiment

Previous studies of biparental care in birds have focused on the males contribution and experimental removal of males. Woodpeckers, with a high level of paternal care including nocturnal incubation and brooding by males, offer a meaningful system in which to examine the importance of care by females. I studied the reproductive performance of 17 widowed male and 8 widowed female northern flickers (Colaptes auratus) relative to biparental (control) pairs. Of these single parents all widowed shortly after hatching, only one female abandoned its nest. Single parents boosted their provisioning rates to achieve 83% the provisioning rate of control broods, but reared significantly fewer young and young of poorer quality. However, single males, with 85% of the reproductive success of controls, were more successful than females with 43% the success of controls. Among widowed birds, a not significant lower survival was observed, but the chance of re-pairing with the same partner in a subsequent year was only 16% in the natural population, so long-term costs of desertion may be small. Although females seem to have the incentive and ability to desert, a lack of available males may constrain opportunities. This study demonstrates that when parental care roles are reversed in altricial birds, asymmetric benefits can favor female and not male desertion.     

Population Viability Analysis of Captive and Released Bearded Vulture Populations

With the computer program VORTEX I ran a series of simulations of the Bearded Vulture ( Gypaetus barbatus ) population held in captivity in European zoos and of the population released in the Alps. The simulations showed that the risk of extinction of the captive population with the extraction rates currently in use is low. It seems possible to maintain the current release rate of two fledglings per year at each of the four release sites in the Alps, but it does not seem possible to increase the release rate by expanding the project to other European mountains without dangerously depleting the captive population. The models showed that the most effective way to increase the release rate without increasing the captive population size is by improving hatching success in captivity. The information on the demographic parameters of the Bearded Vulture population released in the Alps was not good enough to predict the ultimate fate of the present population or to allow for recommendations on how long the population should continue to be supplemented. Although it will be necessary to wait some years to see if Bearded Vultures are able to breed in the wild in the Alps and to estimate fecundity rates, it should be possible to improve the monitoring of the individuals released to obtain more-precise survival estimates. The models of the captive and released population also showed that it should at least be possible to have an artificially supplemented Bearded Vulture population in the Alps, but because this is not the goal of the present reintroduction project, the organizations involved should decide whether this is a politically or economically desirable goal.     

Costs of overlapping reproduction and moult in passerine birds: an experiment with the pied flycatcher

The process of moult in birds requires the investment of substantial amounts of energy and nutrients in feather production and attendant processes. Flight performance may be reduced during the moult of the wing feathers, and moulting birds may suffer from an increased predation risk. These factors may explain why the moult is usually separated in time from other energetically demanding processes, such as reproduction. In this study, we investigated the importance of the temporal separation of moult from breeding activities in the pied flycatcher Ficedula hypoleuca. We induced a moult-breeding overlap by removing the two innermost primaries on both wings, thus imitating the natural loss of these feathers during the initial stage of the moult. The experiment probably did not stimulate feather regrowth, but may have reduced flight performance. Just before fledging of the young, manipulated males and females, as well as the fledglings, had a lower body condition than control birds. The return rate of adult males in the year following the manipulation was significantly lower for males in the manipulated group than for control males. The return rate of females was lower than that of males, but there was no difference between the two female groups. The number of nestlings recruited in the year after the manipulation was significantly lower for the group with an induced moult-breeding overlap than for the control group. The reproductive performance in recruited and returning old females was independent of the manipulation, and in returning adults and recruits the feather quality in terms of number of barbs/mm was independent of the manipulation. These results suggest that a moult-breeding overlap induces fitness costs in terms of reduced recruitment rate and adult survival in a long-distance migrant. Received: 17 September 1997 / Accepted after revision: 23 February 1998     

Dominance and survival of dippers Cinclus cinclus

Survival of dippers Cinclus cinclus in the wild was studied in relation to their dominance. Dominance was assessed amongst groups of temporary captives in a laboratory arena. Adults tended to be more dominant than juveniles, and within age classes males generally dominated females. Dominant individuals also sang more. Logistic regression was used to examine survival in the wild in relation to dominance and other factors. Annual survival of juvenile males was negatively related to dominance during the previous autumn. No significant effects of dominance on winter or annual survival were found amongst females or adult males. Dominance effects on overwinter survival approached significance for adult females, however, and were significant for both winter and annual survival when the data from adult females and juvenile males were combined. None of the other factors considered, which included body size, song frequency and year, had a significant effect on overwinter or annual survival. We concluded that dominance either had no influence on survival, or had a negative effect particularly on dippers of intermediate status. We were unable to show if dominance had a direct effect, however, or acted indirectly on survival via an unidentified factor we did not examine. Received: 23 June 1994/Accepted after revision: 28 October 1995     

Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata)

Developmental stress has recently been shown to have adverse effects upon adult male song structure in birds, which may well act as an honest signal of male quality to discriminating females. However, it still remains to be shown if females can discriminate between the songs of stressed and non-stressed males. Here we use a novel experimental design using an active choice paradigm to investigate preferences in captive female zebra finches (Taeniopygia guttata). Nine females were exposed to ten pairs of songs by previously stressed and non-stressed birds that had learned their song from the same tutor. Song pairs differed significantly in terms of song complexity, with songs of stressed males exhibiting lower numbers of syllables and fewer different syllables in a phrase. Song rate and peak frequency did not differ between stressed and non-stressed males. Females showed a significant preference for non-stressed songs in terms of directed perching activity and time spent on perches. Our results therefore indicate that developmental stress affects not only the structure of male song, but that such structural differences are biologically relevant to female mate choice decisions.     

Conservation Biology Framework for the Release of Wild-Born Orphaned Chimpanzees into the Conkouati Reserve, Congo

Abstract: Returning confiscated animals to their native habitats is desirable when it makes a positive contribution to the conservation of the species. Release of captive individuals is complex and controversial, however, particularly when risks are potentially high, as in the case of orphaned apes. We describe the decision-making process that led to the successive release of 20 wild-born orphan chimpanzees (    Pan troglodytes troglodytes ) into the Conkouati Reserve in the Republic of Congo. Recommendations of the Reintroduction Specialist Group of the World Conservation Union's Species Survival Commission were followed closely. The conservation status, ecology, and behavior of wild chimpanzees; the biological, social, economic and political context of the release site; and the health and genetic status of the candidates for release were all taken into account in the planning and execution of the project. Rigorous post-release monitoring of behavior and health allowed documentation of the outcome. The project was of benefit to the chimpanzees that were released but also brought broad benefits to the site through effective protection from poaching and deforestation, and direct and indirect benefits to local people. The genetic and behavioral diversity of chimpanzees require a variety of conservation strategies to reduce threats and maintain as many viable wild populations as possible.     

Phylogenetic Reanalysis of the Saudi Gazelle and Its Implications for Conservation

Abstract: The identification of taxonomically appropriate populations of endangered species for captive breeding and reintroduction programs is fundamental to the success of those programs. The Saudi gazelle (   Gazella saudiya ) was endemic to the Arabian peninsula but is now considered extinct in the wild and is potentially a candidate for captive breeding and reintroduction. Using 375 base pairs of mitochondrial DNA (mtDNA) cytochrome b gene derived from museum samples collected from the wild prior to the presumed extinction of this species, we show that G. saudiya is the sister taxon of the African dorcas gazelle (  G. dorcas ). Reciprocal monophyly of G. saudiya mtDNA haplotypes with G. dorcas , coupled with morphological distinctiveness, suggests that it is an evolutionarily significant unit. These data indicate that captive populations identified previously as potential sources of G. saudiya for captive breeding appear incorrectly designated and are irrelevant to the conservation of G. saudiya. The polymerase chain reaction–restriction fragment length polymorphism ( PCR-RFLP) analysis of several private collections of living gazelles in Saudi Arabia provides no evidence for the survival of G. saudiya. We recommend that field surveys be undertaken to establish whether G. saudiya is indeed extinct in the wild and that other private collections within the Arabian peninsula be screened genetically. We urge caution when captive animals of unknown provenance are used to investigate the phylogenetics of cryptic species groups.     

The Appropriateness of Puppet-Rearing Birds for Reintroduction

Abstract: Captive propagation and reintroduction programs for rare and endangered species rarely include testing of techniques prior to initiation of recovery efforts. To experimentally test the effects of rearing social, altricial birds with or without a conspecific, parental model (a puppet), we used Common Ravens ( Corvus corax ) in southwestern Idaho as surrogates for the endangered Hawaiian Crow ( Corvus hawaiiensis ) and Mariana Crow ( Corvus kubaryi ). A puppet is believed to reduce sexual and filial imprinting on human caretakers. We raised 49 ravens without a puppet and 25 ravens with a puppet. We initiated puppet-rearing when birds were 7 days of age and continued until 60 days of age, when nestlings could eat well on their own. The influence of puppet-rearing was tested as part of a factorial design that also tested for the effects of conspecific tutoring and age at release. Rearing ravens with a puppet did not affect social behaviors prior to release, dispersal from the release area, or integration with wild birds after release. Ravens raised with a puppet, however, were more fearful of caretakers and more vigilant prior to release, characteristics that may have improved their chances for survival after release. It is important for researchers to consider the species and the desired pre- and post-release behaviors to determine if rearing with a puppet is appropriate for their recovery efforts. These considerations can be taken into account by using a surrogate species prior to recovery efforts and creative management approaches in the initial phases of an endangered species recovery program.     

Mortality in the pheasant Phasianus colchicus during the breeding season

Summary Mortality of wild radio-tagged pheasants was analysed over six breeding seasons (1984–1987 and 1989–1990) in the Revinge area in southernmost Sweden. The aim of the study was to compare morphology and behaviour of birds found dead with those that survived the breeding season (from the first week of April to 30 June). The pheasants were kept over winter in an outdoor enclosure, equipped with radio transmitters, and released during the first week of April. In all, 49 females and 43 males were found dead and the average breeding-season mortality was 25% in males and 26% in females (not including birds that disappeared). The main predators were goshawk Accipiter gentilis and red fox Vulpes vulpes. Mortality among males peaked in late April whereas female mortality was highest in late May. Measurements of morphology included: length of tail, tarsus and wing, body mass and for males, spur length. The only morphological trait that differed between survivors and non-survivors was spur length in males; survivors had longer spurs. This difference was only found when allometric effects of age and body size on spur length were controlled for. Attractiveness and spacing behaviour of non-surviving males were recorded by telemetry from release until the last day of life, and compared with the average performance of survivors in that year. Non-surviving males moved shorter distances between days but did not differ from survivors in calling activity and attractiveness. Calling activity was higher in males that died early in the season compared to those dying late in the season. No differences were found between surviving and non-surviving females.     

The effects of parasites on male ornaments and female choice in the lek-breeding black grouse (Tetrao tetrix)

Summary We describe the results of two studies of parasitic infection in the black grouse (Tetrao tetrix). The first deals with our own observations of lekking black grouse in which the parasite levels of two blood parasites, the protozoan Leucocytozoon lovati and microfilaria, probably produced by a nematode worm Splendidofilaria tuvensis, were scored. We also obtained measures of age, survival, number of copulations, body mass and length of the ornamental tail feathers (the lyre) of the lekking males. The second study analysed the data from Lund (1954) which involved eight gut parasites obtained from birds which were killed. In the first study we found higher levels of infection of Leucocytozoon in adults relative to young birds. Parasites had no effect on male survival and there was no correlation in infection between the two types of parasites. Birds infected with microfilaria had shorter tail ornaments. There was no relationship between parasitic infection and mating success. However, the data indicated that such a trend indeed may exist for Leucocytozoon and the most successful males on the leks were less often infected by Leucocytozoon than other males. Results of the second study showed a negative relationship between parasite load (a combined measure of all parasites) and both ornamental tail feather length and body mass. These observations are compatible with, but not conclusive evidence for, the hypothesis of Hamilton and Zuk (1982) on the evolution of secondary sexual characters, where females choose to mate with genetically resistant males which show their resistance by expressing larger and more showy secondary sexual characters. Alternative explanations for the observed patterns are: females avoid infected males for some immediate benefit; and/or parasite loads are indicators of general stress rather than genetical resistance. Under the latter hypothesis females could mate with more vigorous males for reasons unrelated to parasite resistance.     

Differences in reproductive success between laboratory and wild-derived golden hamsters (Mesocricetus auratus) as a consequence of inbreeding

All laboratory golden hamsters (Mesocricetus auratus) originated from a sibling pairing back in 1930. Due to this extreme founder event, domestic golden hamsters are presumed to be one of the most bottlenecked animal populations. Nevertheless, domestic hamsters show no obvious signs of inbreeding depression in commonly used breeding stocks. To explore the existence of potentially masked inbreeding effects, we compared the reproductive success of laboratory (lab) and wild-derived (wild) golden hamsters. We allowed oestrus females to mate consecutively with lab and wild males. The resulting offspring was genotyped using microsatellites to assess paternity. Finally, we compared male reproductive success to genetic variability, sexual behaviour and different sperm characteristics. Both hamster strains exhibited the expected large difference in genetic diversity (H _wild =0.712±0.062 vs H _lab =0.007±0.007. The reproductive success of wild males dramatically exceeded that of lab males (87% of pups were sired by wild males). Sexual behaviour of wild and lab males only varied in the number of long intromissions (intromissions without ejaculation at the end of the mating). No significant differences were observed in relation to mounting, ejaculation and intromission. There were also no apparent differences in sperm motility, velocity and density or testis histology between wild and lab hamsters. We conclude that the reduced reproductive success of lab males represents a hidden inbreeding effect, although its precise physiological cause remains unclear. These results provide first evidence for a major fitness disadvantage in captive golden hamsters.     

Seasonal variation in the duetting behaviour of rufous-and-white wrens (<Emphasis Type="Italic">Thryothorus rufalbus</Emphasis>)

Seasonal variation in animal signalling behaviour has been well documented and has contributed much to our understanding of male signals. In contrast, we know little about seasonal variation in female signals or signals produced jointly by males and females, such as the vocal duets of birds. Here, we examine how singing behaviour changes in relation to time of year and breeding stage in rufous-and-white wrens (Thryothorus rufalbus), neotropical songbirds where both males and females sing and where breeding partners coordinate songs to produce vocal duets. We recorded a colour-marked population of birds over an extended time period encompassing multiple breeding stages. Across all time frames and breeding stages, males sang at higher rates than females and male solos were more common than duets or female solos. Males and females showed divergent seasonal patterns of singing. Females sang more often early in the year, during the pre-breeding season, and female song tapered off as the breeding season progressed. Duetting followed a parallel pattern, which resulted from females showing less duet responsiveness to their partner’s songs later in the year. Male independent song rate peaked at the onset of the rainy season – a time when females become fertile – and males showed the highest level of duet responsiveness during this period. Our results suggest that early in the year, duets appear to be cooperative displays, functioning in joint territory defence and/or the coordination of breeding activities. When females are fertile, however, increased duet responsiveness by males is consistent with mate or paternity guarding.