The phenotypic costs of captivity

The breeding of threatened species in captivity for release is a central tool in conservation biology. Given gloomy predictions for biodiversity trends in the Anthropocene, captive breeding will play an increasingly important role in preventing future extinctions. Relative to the wild, captive environments drastically alter selection pressures on animals. Phenotypic change in captive animals in response to these altered selection pressures can incur fitness costs post-release, jeopardising their potential contribution to population recovery. We explore the ways in which captive environments can hinder the expression of wild phenotypes. We also stress that the phenotypes of captive-bred animals differ from their wild counterparts in multiple ways that remain poorly understood. We propose five new research questions relating to the impact of captive phenotypes on reintroduction biology. With better use of monitoring and experimental reintroductions, a more robust evidence base should help inform adaptive management and minimise the phenotypic costs of captivity, improving the success of animal reintroductions.     

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.     

Modeling problems in conservation genetics using captive Drosophila populations: Rapid genetic adaptation to captivity

Long-term captive breeding programs for endangered species generally aim to preserve the option of release back into the wild. However, the success of re-release programs will be jeopardized if there is significant genetic adaptation to the captive environment. Since it is difficult to study this problem in rare and endangered species, a convenient laboratory animal model is required. The reproductive fitness of a large population of Drosophila melanogaster maintained in captivity for 12 months was compared with that of a recently caught wild population from the same locality. The competitive index measure of reproductive fitness for the captive population was twice that of the recently caught wild population, the difference being highly significant. Natural selection over approximately eight generations in captivity has caused rapid genetic adaptation. Captive breeding strategies for endangered species should minimize adaptation to captivity in populations destined for reintroduction into the wild. A framework for predicting the impact of factors on the rate of genetic adaptation to captivity is suggested. Equalization of family sizes is predicted to approximately halve the rate of genetic adaptation. Introduction of genes from the wild, increasing the generation interval, using captive environments close to those in the wild and achieving low mortality rates are all expected to slow genetic adaptation to captivity. Many of these procedures are already recommended for other reasons. © 1992 Wiley-Liss, Inc.     

The efficiency of close inbreeding to reduce genetic adaptation to captivity

Although ex situ conservation is indispensable for thousands of species, captive breeding is associated with negative genetic changes: loss of genetic variance and genetic adaptation to captivity that is deleterious in the wild. We used quantitative genetic individual-based simulations to model the effect of genetic management on the evolution of a quantitative trait and the associated fitness of wild-born individuals that are brought to captivity. We also examined the feasibility of the breeding strategies under a scenario of a large number of loci subject to deleterious mutations. We compared two breeding strategies: repeated half-sib mating and a method of minimizing mean coancestry (referred to as gc/mc). Our major finding was that half-sib mating is more effective in reducing genetic adaptation to captivity than the gc/mc method. Moreover, half-sib mating retains larger allelic and adaptive genetic variance. Relative to initial standing variation, the additive variance of the quantitative trait increased under half-sib mating during the sojourn in captivity. Although fragmentation into smaller populations improves the efficiency of the gc/mc method, half-sib mating still performs better in the scenarios tested. Half-sib mating shows two caveats that could mitigate its beneficial effects: low heterozygosity and high risk of extinction when populations are of low fecundity and size and one of the following conditions are met: (i) the strength of selection in captivity is comparable with that in the wild, (ii) deleterious mutations are numerous and only slightly deleterious. Experimental validation of half-sib mating is therefore needed for the advancement of captive breeding programs.     

Effects of captivity,diet, and relocation on the gut bacterial communities of white‐footed mice

Microbes can have important impacts on their host's survival. Captive breeding programs for endangered species include periods of captivity that can ultimately have an impact on reintroduction success. No study to date has investigated the impacts of captive diet on the gut microbiota during the relocation process of generalist species. This study simulated a captive breeding program with white‐footed mice (Peromyscus leucopus) to describe the variability in gut microbial community structure and composition during captivity and relocation in their natural habitat, and compared it to wild individuals. Mice born in captivity were fed two different diets, a control with dry standardized pellets and a treatment with nonprocessed components that reflect a version of their wild diet that could be provided in captivity. The mice from the two groups were then relocated to their natural habitat. Relocated mice that had the treatment diet had more phylotypes in common with the wild‐host microbiota than mice under the control diet or mice kept in captivity. These results have broad implications for our understanding of microbial community dynamics and the effects of captivity on reintroduced animals, including the potential impact on the survival of endangered species. This study demonstrates that ex situ conservation actions should consider a more holistic perspective of an animal's biology including its microbes.     

Adaptations to Captivity in the Butterfly Pieris brassicae (L.) and the Implications for Ex situ Conservation

Captive breeding has been suggested as a method of conserving many threatened vertebrates, and is increasingly being proposed as a valuable conservation strategy for invertebrates. Potential genetic problems associated with ex situ conservation are widely recognized, but a further issue has received less attention: the possibility that populations will undergo adaptation to the captive environment, rendering them less well adapted to survival in the wild. We investigated six traits related to dispersal and reproduction in a culture of the large white butterfly Pieris brassicae (L.), that had been captive for c. 100–150 generations, and in recently wild stock reared simultaneously in a common environment. Individuals in the captive culture were heavier, with smaller wings and lower wing aspect ratios. Females from the captive culture laid many more eggs in cage experiments, and had higher ovary mass at the time of peak egg production. These differences are consistent with adaptation to captive conditions. Over time, similar evolutionary changes may affect invertebrates reared in ex situ conservation programmes, decreasing the likelihood that these species can be re-established in the wild. Although the timescale over which most vertebrates are likely to adapt to captivity is longer, and the traits involved will be different, invertebrates like P. brassicae may also provide a model of potential problems in long-term ex situ conservation programmes for both invertebrates and vertebrates. We suggest that measures to reduce or slow adaptation to captivity should be introduced alongside measures to reduce deleterious genetic effects in captive populations.     

Effect of captivity on genetic variance for five traits in the large milkweed bug (Oncopeltus fasciatus)

Understanding the changes in genetic variance which may occur as populations move from nature into captivity has been considered important when populations in captivity are used as models of wild ones. However, the inherent significance of these changes has not previously been appreciated in a conservation context: are the methods aimed at founding captive populations with gene diversity representative of natural populations likely also to capture representative quantitative genetic variation? Here, I investigate changes in heritability and a less traditional measure, evolvability, between nature and captivity for the large milkweed bug, Oncopeltus fasciatus, to address this question. Founders were collected from a 100-km transect across the north-eastern US, and five traits (wing colour, pronotum colour, wing length, early fecundity and later fecundity) were recorded for founders and for their offspring during two generations in captivity. Analyses reveal significant heritable variation for some life history and morphological traits in both environments, with comparable absolute levels of evolvability across all traits (0-30%). Randomization tests show that while changes in heritability and total phenotypic variance were highly variable, additive genetic variance and evolvability remained stable across the environmental transition in the three morphological traits (changing 1-2% or less), while they declined significantly in the two life-history traits (5-8%). Although it is unclear whether the declines were due to selection or gene-by-environment interactions (or both), such declines do not appear inevitable: captive populations with small numbers of founders may contain substantial amounts of the evolvability found in nature, at least for some traits.     

Do experiments with captive non-domesticated animals make sense without population field studies? A case study with blue tits' breeding time

A complete understanding of the spatio-temporal variation in phenotypic traits in natural populations requires a combination long-term field studies with experiments using captive animals. Field studies allow the formulation of realistic hypotheses, but have the disadvantage that they do not allow the complete control of many potential confounding variables. Studies with captive animals allow tests of hypotheses that cannot be examined in the field, but have the disadvantage that artificial environments may provoke abnormal behaviour. Long-term studies that follow simultaneously captive and wild bird populations are rare. In a study lasting several years, we show here the unexpected patterns that two populations with a similar breeding time in the wild have non-overlapping breeding times in outdoor aviaries, and that two wild populations separated by a short geographical distance show differences in the expression of natural behaviour in captivity. The experimental design used is exceptional in the sense that the captive populations were held at similar latitudes and altitudes as the wild populations. Our case study shows that studies with captive animals can lead to wrong conclusions if they are carried out without population field studies, and without knowledge of the natural habits and habitats of the species involved. To examine the reliability of experiments with captive animals, comparisons with findings from population field studies are essential.     

Dynamics of genetic adaptation to captivity

Many species require captive breeding to savethem from extinction, with reintroduction intothe wild being the eventual aim of mostprograms. Adaptation to captive environmentstypically results in reduced fitness under wildconditions. Consequently, unintentionaladaptation during captive breeding programs mayseriously compromise the success ofreintroduction programs. However, there islittle experimental evidence on the rate orextent of adaptation for captive populationsmaintained under benign captive conditions forextended periods of time. To investigate thedynamics of genetic adaptation to captivity,large captive populations of Drosophilamelanogaster were assessed for relativefitness under captive conditions for up to 87generations in captivity. Captive fitnessincreased to 3.33 times the initial fitnessover 87 generations. The pattern of adaptationwas curvilinear, with an exponential curveproviding the best fit. Fitness reached 25% ofits maximum within 6 generations, 50% within15 generations, 75% within 31 generations and95% within 67 generations. The model predictedthat the asymptotic level of fitness reachedwould be 3.38 times the initial fitness. Thus,very large genetic adaptations to captivity mayoccur under relatively benign captiveconditions. Captive populations destined forreintroduction need to be managed to minimisegenetic adaptation to captivity.     

Nature versus nurture? Consequences of short captivity in early stages

Biological changes occurring as a consequence of domestication and/or captivity are not still deeply known. In Atlantic salmon (Salmo salar), endangered (Southern Europe) populations are enhanced by supportive breeding, which involves only 6 months of captive rearing following artificial spawning of wild‐collected adults. In this work, we assess whether several fitness‐correlated life‐history traits (migratory behavior, straying rate, age at maturity, and growth) are affected by early exposure to the captive environment within a generation, before reproduction thus before genetic selection. Results showed significant differences in growth and migratory behavior (including straying), associated with this very short period of captivity in natural fish populations, changing even genetic variability (decreased in hatchery‐reared adults) and the native population structure within and between rivers of the species. These changes appeared within a single generation, suggesting very short time of captivity is enough for initiating changes normally attributed to domestication. These results may have potential implications for the long‐term population stability/viability of species subjected to restoration and enhancement processes and could be also considered for the management of zoo populations.     

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.     

Comparative study of gut microbiota from captive and confiscated-rescued wild pangolins

Pangolins are among the most critically endangered animals due to widespread poaching and worldwide trafficking. Captive breeding is considered to be one way to protect them and increase the sizes of their populations. However, comparative studies of captive and wild pangolins in the context of gut microbiota are rare. Here, the gut microbiome of captive and confiscated-rescued wild pangolins is compared, and the effects of different periods of captivity and captivity with and without antibiotic treatment are considered. We show that different diets and periods of captivity, as well as the application of antibiotic therapy, can alter gut community composition and abundance in pangolins. Compared to wild pangolins, captive pangolins have an increased capacity for chitin and cellulose/hemicellulose degradation, fatty acid metabolism, and short-chain fatty acid synthesis, but a reduced ability to metabolize exogenous substances. In addition to increasing the ability of the gut microbiota to metabolize nutrients in captivity, captive breeding imposes some risks for survival by resulting in a greater abundance of antibiotic resistance genes and virulence factors in captive pangolins than in wild pangolins. Our study is important for the development of guidelines for pangolin conservation, including health assessment, disease prevention, and rehabilitation of wild pangolin populations.     

Parks or arks: where to conserve threatened mammals?

Growing deterministic and stochastic threats to many wild populations of large vertebrates have focused attention on the conservation significance of captive breeding and subsequent reintroduction. However, work on both gorillas and black rhinos questions this shift in emphasis. In these species, field-based conservation can be effective if properly supported and, although this is not cheap, per capita costs may still be considerably lower than for ex situ propagation in captivity. Here we attempt to broaden the scope of this debate by contrasting the breeding success and costs of in situ and captive programmes for a range of threatened mammals. Data are scarce, but we find that across nine large-bodied genera, in situ conservation achieves comparable rates of population growth to those seen in established captive breeding programmes. Moreover, comparing budgets of well-protected reserves with zoos' own estimates of maintenance costs and the costs of zoo adoption schemes, we find that per capita costs for effective in situ conservation are consistently lower than those of maintenance in captivity. Captive breeding may be more cost-effective for smaller-bodied taxa, and will often remain desirable for large mammals restricted to one or two vulnerable wild populations. However, our results, coupled with the fact that effective in situ conservation protects intact ecosystems rather than single species, lead us to suggest that zoos might maximize their contribution to large mammal conservation by investing where possible in well-managed field-based initiatives, rather than establishing additional ex situ breeding programmes.     

Do captive waterfowl alter their behaviour patterns during their flightless period of moult?

Many different behavioural changes have been observed in wild waterfowl during the flightless stage of wing moult with birds frequently becoming inactive and reducing time spent foraging. Increased predation risk, elevated energetic demands of feather re-growth and restriction of foraging opportunities are thought to underlie these changes. By studying captive populations of both a dabbling and a diving duck species at the same site, we determined whether captive birds would reflect the behavioural responses of wild waterfowl to moult. The time-budgets of 42 Common Eiders, Somateria mollissima, (a diving duck) and 18 Garganeys, Anas querquedula, (a dabbling duck) were recorded during wing moult (July–August) and non-moult (January) with behaviour recorded under six categories. Despite captivity providing a low predation risk and constant access to food, birds altered their behaviour during the flightless period of wing moult. Time allocated to foraging and locomotion decreased significantly during moult compared to non-moult periods, while resting time increased significantly. Moulting Eiders underwent a greater reduction in time spent foraging and in locomotion compared with Garganeys, which is likely to be in response to a higher energetic cost of foraging in Eiders. It is possible that increased resting in both diving and dabbling ducks reduces their likelihood of detection by predators, while allowing them to remain vigilant. We demonstrate that there is much potential for using captive animals in studies that can augment our knowledge of behaviours of free-living conspecifics, the former being a hitherto under-exploited resource.     

Effect of new founders on retention of gene diversity in captive populations: A formalization of the nucleus population concept

A nucleus population is a small captive population genetically supported by periodic importation of wild caught animals. Periodic importation will allow nucleus populations to maintain the same amount of gene diversity as larger captive populations that do not import wild caught animals. The function of nucleus populations as envisioned by the IUCN/SSC Captive Breeding Specialist Group (CBSG) is to make additional captive space available for endangered taxa not currently maintained in captivity. In this article, mathematical models are developed to assess the effectiveness of the nucleus population concept in reducing the population sizes necessary to maintain appreciable amounts of gene diversity in captive populations. It is shown that the Nucleus I population concept, as defined and promoted by the CBSG, requires an importation rate 10–20 times greater than they have indicated. Whereas nucleus populations are not appropriate for maintenance of significant amounts of gene diversity in long-term breeding programs, small populations can be valuable for research, education, and reintroduction projects with short-term goals. Decisions have to be made on which of the many endangered taxa will be maintained and for what purposes, if captive breeding is to be an effective component of species conservation. © 1993 Wiley-Liss, Inc.     

Effects of inbreeding on reproductive success,performance, litter size,and survival in captive red wolves (Canis rufus)

Captive‐breeding programs have been widely used in the conservation of imperiled species, but the effects of inbreeding, frequently expressed in traits related to fitness, are nearly unavoidable in small populations with few founders. Following its planned extirpation in the wild, the endangered red wolf (Canis rufus) was preserved in captivity with just 14 founders. In this study, we evaluated the captive red wolf population for relationships between inbreeding and reproductive performance and fitness. Over 30 years of managed breeding, the level of inbreeding in the captive population has increased, and litter size has declined. Inbreeding levels were lower in sire and dam wolves that reproduced than in those that did not reproduce. However, there was no difference in the inbreeding level of actual litters and predicted litters. Litter size was negatively affected by offspring and paternal levels of inbreeding, but the effect of inbreeding on offspring survival was restricted to a positive influence. There was no apparent relationship between inbreeding and method of rearing offspring. The observable effects of inbreeding in the captive red wolf population currently do not appear to be a limiting factor in the conservation of the red wolf population. Additional studies exploring the extent of the effects of inbreeding will be required as inbreeding levels increase in the captive population. Zoo Biol 29:36–49, 2010. © 2009 Wiley‐Liss, Inc.     

Conservation Genetics of Threatened Hippocampus guttulatus in Vulnerable Habitats in NW Spain: Temporal and Spatial Stability of Wild Populations with Flexible Polygamous Mating System in Captivity

This study was focused on conservation genetics of threatened Hippocampus guttulatus on the Atlantic coast of NW Iberian Peninsula. Information about spatial structure and temporal stability of wild populations was obtained based on microsatellite markers, and used for monitoring a captive breeding program firstly initiated in this zone at the facilities of the Institute of Marine Research (Vigo, Spain). No significant major genetic structure was observed regarding the biogeographical barrier of Cape Finisterre. However, two management units under continuous gene flow are proposed based on the allelic differentiation between South-Atlantic and Cantabrian subpopulations, with small to moderate contemporary effective size based on single-sample methods. Temporal stability was observed in South-Atlantic population samples of H. guttulatus for the six-year period studied, suggesting large enough effective population size to buffer the effects of genetic drift within the time frame of three generations. Genetic analysis of wild breeders and offspring in captivity since 2009 allowed us to monitor the breeding program founded in 2006 in NW Spain for this species. Similar genetic diversity in the renewed and founder broodstock, regarding the wild population of origin, supports suitable renewal and rearing processes to maintain genetic variation in captivity. Genetic parentage proved single-brood monogamy in the wild and in captivity, but flexible short- and long-term mating system under captive conditions, from strict monogamy to polygamy within and/or among breeding seasons. Family analysis showed high reproductive success in captivity under genetic management assisted by molecular relatedness estimates to avoid inbreeding. This study provides genetic information about H. guttulatus in the wild and captivity within an uncovered geographical range for this data deficient species, to be taken into account for management and conservation purposes.     

Captive Breeding Does Not Alter Brain Volume in a Marsupial Over a Few Generations

Captive breeding followed by reintroduction to the wild is a common component of conservation management plans for various taxa. Although it is commonly used, captive breeding can result in morphological changes, including brain size decrease. Brain size reduction has been associated with behavioral changes in domestic animals, and such changes may negatively influence reintroduction success of captive‐bred animals. Many marsupials are currently bred in captivity for reintroduction, yet the impacts of captive breeding on brain size have never been studied in this taxa. We investigated the impacts of a few generations (2–7) of captive breeding on brain volume in the stripe‐faced dunnart (Sminthopsis macroura), and found that captive breeding in a relatively enriched environment did not cause any changes in brain volume. Nonetheless, we advocate that great care be taken to provide suitable husbandry conditions and to minimize the number of captive generations if marsupial reintroduction programs are to be successful. Zoo Biol 31:82;–86, 2012. © 2011 Wiley Periodicals, Inc.     

Rapid genetic deterioration in captive populations: Causes and conservation implications

Many species require captive breeding to ensuretheir survival. The eventual aim of suchprograms is usually to reintroduce the speciesinto the wild. Populations in captivitydeteriorate due to inbreeding depression, lossof genetic diversity, accumulation of newdeleterious mutations and genetic adaptationsto captivity that are deleterious in the wild.However, there is little evidence on themagnitude of these problems. We evaluatedchanges in reproductive fitness in populationsof Drosophila maintained under benigncaptive conditions for 50 generations witheffective population sizes of 500 (2replicates), 250 (3), 100 (4), 50 (6) and 25(8). At generation 50, fitness in the benigncaptive conditions was reduced in smallpopulations due to inbreeding depression andincreased in some of the large populations dueto modest genetic adaptation. When thepopulations were moved to `wild' conditions,all 23 populations showed a marked decline(64–86%percnt;) in reproductive fitness compared tocontrols. Reproductive fitness showed acurvilinear relationship with population size,the largest and smallest population sizetreatments being the worst. Genetic analysesindicated that inbreeding depression andgenetic adaptation were responsible for thegenetic deterioration in `wild' fitness.Consequently, genetic deterioration incaptivity is likely to be a major problem whenlong-term captive bred populations ofendangered species are returned to the wild. Aregime involving fragmentation of captivepopulations of endangered species is suggestedto minimize the problems.     

Impact of Plant Cover on Fitness and Behavioural Traits of Captive Red-Eyed Tree Frogs (Agalychnis callidryas)

Despite the importance of ex situ conservation programmes as highlighted in the Amphibian Conservation Action Plan, there are few empirical studies that examine the influence of captive conditions on the fitness of amphibians, even for basic components of enclosure design such as cover provision. Maintaining the fitness of captive amphibian populations is essential to the success of ex situ conservation projects. Here we examined the impact of plant cover on measures of fitness and behaviour in captive red-eyed tree frogs (Agalychnis callidryas). We found significant effects of plant provision on body size, growth rates and cutaneous bacterial communities that together demonstrate a compelling fitness benefit from cover provision. We also demonstrate a strong behavioural preference for planted rather than non-planted areas. We also assessed the impact of plant provision on the abiotic environment in the enclosure as a potential driver of these behavioural and fitness effects. Together this data provides valuable information regarding enclosure design for a non-model amphibian species and has implications for amphibian populations maintained in captivity for conservation breeding programmes and research.