Effect of Migration or Inbreeding Followed by Selection on Low-Founder-Number Populations: Implications for Captive Breeding Programs

Using the housefly, Musca domestica (L), as a model system, we tested the ability of two extremes in the range of possible captive breeding protocols to yield sustainable populations following founding with low founder numbers. The protocols tested included two levels of migration as well as inbreeding followed by selection, each with appropriate controls. Each low-founder-number population was founded with two pairs of flies. The maximum migration scheme had 50% migration per generation, and the minimum migration populations experienced a migration rate of 2.5% per generation. The control level of migration was 0%. A fourth low-founder-number treatment was designed to test the effect of inbreeding followed by selection. Two sets of high-founder-number control groups were also derived from the stock population. Two fitness measures, viability and productivity of the populations, were recorded at the fifth generation. Populations in the minimum-migration and zero migration treatment groups had lower fitness than populations in any other treatment for both measures. Populations that experienced inbreeding and selection for high fitness levels, high levels of migration, or large high-founder-number populations were equally fit. These results demonstrate that a captive-breeding scheme that contains substantial levels of migration or inbreeding followed by selection can yield highly adapted populations.     

Rapid Loss of Genetic Variation in Large Captive Populations of Drosophila Flies: Implications for the Genetic Management of Captive Populations

Levels of variation in eight large captive populations of D. melanogaster (census sizes ∼ 5000) that had been in captivity for periods from 6 months to 23 years (8 to 365 generations) were estimated from allozyme heterozygosities, lethal frequencies, and inversion heterozygosities and phenotypic variances, additive genetic variances ( V _A), and heritabilities ( h ²) for sternopleural bristle numbers. Correlations between all measures of variation except lethal frequencies were high and significant. All measures of genetic variation declined with time in captivity, with those for average heterozygosities, V _A, and h ² being significant. The effective population size ( N _e) was estimated to be 185–253 in these populations, only 0.037–0.051 of census size (N). Levels of allozyme heterozygosities declined rapidly in two large captive populations founded from another wild stock, being reduced by 86% and 62% within 2.5 years in spite of being maintained at sizes of approximately 1000 and 3500. Estimates of N _e/ N for these populations were only 0.016 and 0.004. Two estimates of N _e/ N for captive populations of D. pseudoobscura from data in the literature were also low at 0.036 and 0.012. Consequently, the rate of loss of genetic variation in captive populations and endangered species may be more rapid than hitherto recognized. Merely maintaining captive populations at large census sizes may not be sufficient to maintain essential genetic variation.     

Designing the Ark: Setting Priorities for Captive Breeding

Zoos can help conserve only a small minority of the species threatened with extinction. Clear and rational criteria for identifying which threatened taxa zoos should focus on are therefore essential. Current priorities for ex situ conservation stress the importance of large vertebrates. We show that this hampers the efficient use of resources because such species are less likely to breed well in captivity than smaller-bodied taxa and, despite longer generation lengths, are more costly to maintain in long-term breeding programs. Moreover, although reintroduction to the wild frees zoo space for other species and is the ultimate aim of captive breeding, zoos show no tendency to target species for which continued habitat availability makes reintroduction a realistic prospect. We suggest that zoos adopt selection criteria that reflect the economic and biological realities of captive breeding and reintroduction if they are to maximize their contribution to species conservation, and we present data on the preferences of zoo visitors indicating that doing so need not adversely affect zoo attendance.     

Experimental Tests of Captive Breeding for Endangered Species

Abstract: Several captive breeding regimes were compared for their ability to maintain fitness ( larval viability) and genetic variation in small populations of the housefly ( Musca domestica L.). Populations were either maintained at constant sizes of 40, 200, or 2000 individuals or initiated with two pairs of flies and allowed to grow to 40 individuals ( low-founder-number populations). Low-founder-number populations without migration exhibited low larval viability (22%) after 24 generations, compared to larger populations maintained at either 200 (49%) or 2000 (69%) individuals, and suffered high extinction, with only 44% of the lines surviving 24 generations. Low-founder-number populations subjected to two additional founder ( bottleneck) episodes, reducing them to two pairs of flies, suffered little additional loss in fitness or extinction compared to the single-founder treatments. Migration as low as one individual per generation (2.5% migration) significantly offset both reduced fitness and rate of extinction. Conversely, fitness was not significantly increased for low-founder-number populations when founders were selected from the top performing 20% of pairs under full-sib mating. Populations maintained at 40 individuals were not sustainable, exhibiting low larval viability (35%) and a high extinction rate (40%) over 24 generations, similar to the extinction rates for populations initiated with only four founders. Although none of the populations maintained at 200 individuals went extinct, their fitness was reduced by 20% compared to a large control population maintained at 2000 individuals. Electrophoretic variation was significantly correlated with fitness across treatments, but the correlation of fitness to narrow-sense heritability of two morphometric traits was not significant.     

Captive Breeding, Reintroduction, and the Conservation of Amphibians

Abstract: The global amphibian crisis has resulted in renewed interest in captive breeding as a conservation tool for amphibians. Although captive breeding and reintroduction are controversial management actions, amphibians possess a number of attributes that make them potentially good models for such programs. We reviewed the extent and effectiveness of captive breeding and reintroduction programs for amphibians through an analysis of data from the Global Amphibian Assessment and other sources. Most captive breeding and reintroduction programs for amphibians have focused on threatened species from industrialized countries with relatively low amphibian diversity. Out of 110 species in such programs, 52 were in programs with no plans for reintroduction that had conservation research or conservation education as their main purpose. A further 39 species were in programs that entailed captive breeding and reintroduction or combined captive breeding with relocations of wild animals. Nineteen species were in programs with relocations of wild animals only. Eighteen out of 58 reintroduced species have subsequently bred successfully in the wild, and 13 of these species have established self‐sustaining populations. As with threatened amphibians generally, amphibians in captive breeding or reintroduction programs face multiple threats, with habitat loss being the most important. Nevertheless, only 18 out of 58 reintroduced species faced threats that are all potentially reversible. When selecting species for captive programs, dilemmas may emerge between choosing species that have a good chance of surviving after reintroduction because their threats are reversible and those that are doomed to extinction in the wild as a result of irreversible threats. Captive breeding and reintroduction programs for amphibians require long‐term commitments to ensure success, and different management strategies may be needed for species earmarked for reintroduction and species used for conservation research and education.     

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.     

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.     

Managing the Abundance and Diversity of Breeding Bird Populations through Manipulation of Deer Populations

Abstract: Deer densities in forests of eastern North America are thought to have significant effects on the abundance and diversity of forest birds through the role deer play in structuring forest understories. We tested the ability of deer to affect forest bird populations by monitoring the density and diversity of vegetation and birds for 9 years at eight 4-ha sites in northern Virginia, four of which were fenced to exclude deer. Both the density and diversity of understory woody plants increased following deer exclosure. The numerical response of the shrubs to deer exclosure was significantly predicted by the soil quality (ratio of organic carbon to nitrogen) at the sites. Bird populations as a whole increased following exclosure of deer, particularly for ground and intermediate canopy species. The diversity of birds did not increase significantly following exclosure of deer, however, primarily because of replacement of species as understory vegetation proceeded through successional processes. Changes in understory vegetation accounted for most of the variability seen in the abundance and diversity of bird populations. Populations of deer in protected areas are capable of causing significant shifts in the composition and abundance of bird communities. These shifts can be reversed by increasing the density and diversity of understory vegetation, which can be brought about by reducing deer density.     

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.     

Extinction Rates in Archipelagoes: Implications for Populations in Fragmented Habitats

To study the effect of habitat fragmentation on population viability, I used extinction rates on islands in archipelagoes and estimated the relative probability of extinction per species on single large islands and sets of smaller islands with the same total area. Data on lizards, birds, and mammals on oceanic islands and mammals on mountaintops and in nature reserves yield similar results. Species are likely to go extinct on all the small islands before they go extinct on the single, large island. In the short term, the analysis indicates that extinction probabilities may be lower on a set of small islands. This is perhaps an artifact due to underestimation of extinction rates on small islands and/or the necessity of pooling species in a focal taxon to obtain estimates of extinction rates (which may obscure area thresholds and underestimate the slope and curvature of extinction rates as a function of area). Ultimately, cumulative extinction probabilities are higher for a set of small islands than for single large islands. Mean and median times to extinction tend to be shorter in the fragmented systems, in some cases much shorter. Thus, to minimize extinction rates in isolated habitat remnants and nature reserve systems, the degree of fragmentation should be minimized