Captive Housing during Water Vole (Arvicola terrestris) Reintroduction: Does Short-Term Social Stress Impact on Animal Welfare?

Background

Animals captive bred for reintroduction are often housed under conditions which are not representative of their preferred social structure for at least part of the reintroduction process. Specifically, this is most likely to occur during the final stages of the release programme, whilst being housed during transportation to the release site. The degree of social stress experienced by individuals during this time may negatively impact upon their immunocompetence.

Methodology/Principal Findings

We examined two measure of stress - body weight and Leukocyte Coping Capacity (LCC) - to investigate the effects of group size upon captive-bred water voles destined for release within a reintroduction program. Water voles were housed in laboratory cages containing between one and eight individuals. LCC scores were negatively correlated with group size, suggesting that individuals in larger groups experienced a larger degree of immuno-suppression than did individuals housed in smaller groups or individually. During the course of the study mean body weights increased, in contrast to expectations from a previous study. This was attributed to the individuals sampled being sub-adults and thus growing in length and weight during the course of the investigation.

Conclusions/Significance

The reintroduction process will inevitably cause some stress to the release cohort. However, for water voles we conclude that the stress experienced may be reduced by decreasing group size within captive colony and/or transportation housing practises. These findings are of significance to other species'' reintroductions, in highlighting the need to consider life-history strategies when choosing housing systems for animals being maintained in captivity prior to release to the wild. A reduction in stress experienced at the pre-release stage may improve immunocompetence and thus animal welfare and initial survival post-release.     

Changes in locomotor and foraging skills in captive-born, reintroduced golden lion tamarins (Leontopithecus rosalia rosalia)

The behavior of reintroduced, captive-born animals is understudied, limiting the scientific understanding and utility of reintroduction as a conservation tool. This work describes changes in locomotor and foraging behaviors in captive-born golden lion tamarins over the first 18 months after their release into the wild. The subjects included 73 individuals living in and around the Poco das Antas Biological Reserve in Brazil between 1984 and 1996. The differences between animals that survived 6 months after release and those that did not indicate that initial deficiencies in locomotor and foraging abilities are related to survival. Behavioral changes in both juvenile and adult individuals during the first 6 and 18 months after release appear to be primarily related to locomotor abilities; however, the effect of provisioning on foraging abilities is unknown. Juvenile animals showed a larger number of changes relative to adults during the first 6 and 18 months, suggesting that placing tamarins into complex environments early in development may promote the expression of natural behaviors and increase survival opportunities after their release. However, when this is not possible, the best mechanism for reintroducing adult members of this species involves intensive post-release support rather than pre-release training, which confers few behavioral advantages. Recommendations for future reintroductions with this and other species include introducing animals to complex environments early in development, and collecting data systematically.     

Movement behavior and passive dispersal of a reintroduced population of alligator snapping turtles

Maladaptive movement behavior is a leading cause of failure for reptile reintroductions, thus characterizing movement for translocated populations is important to project success. From 2014–2016 we radio-tracked 183 immature reintroduced alligator snapping turtles (Macrochelys temminckii) using very high frequency telemetry in a stream in southern Illinois, USA. We assessed environmental, temporal, morphometric, and microhabitat factors influencing movement, including post-release dispersal from reintroduction sites, movement probability, and step length. We used directional statistics to investigate the effects of precipitation and age on directional movement in the stream. Numerous factors influenced active movement, including ambient temperatures, time since release, use of log jams, turtle size, and age. Precipitation had an age-biased effect on movement. Directional analyses suggested that movement was largely passive as turtles were swept downstream with increased discharge. Overall, the behavior of reintroduced alligator snapping turtles was similar to that reported in wild populations. Passive downstream transport has implications for reintroduced and natural populations as a force for unintentional emigration in channelized streams under current conditions and future high flow regimes.     

Evaluating wildlife translocations using genomics: A bighorn sheep case study

Wildlife restoration often involves translocation efforts to reintroduce species and supplement small, fragmented populations. We examined the genomic consequences of bighorn sheep (Ovis canadensis) translocations and population isolation to enhance understanding of evolutionary processes that affect population genetics and inform future restoration strategies. We conducted a population genomic analysis of 511 bighorn sheep from 17 areas, including native and reintroduced populations that received 0–10 translocations. Using the Illumina High Density Ovine array, we generated datasets of 6,155 to 33,289 single nucleotide polymorphisms and completed clustering, population tree, and kinship analyses. Our analyses determined that natural gene flow did not occur between most populations, including two pairs of native herds that had past connectivity. We synthesized genomic evidence across analyses to evaluate 24 different translocation events and detected eight successful reintroductions (i.e., lack of signal for recolonization from nearby populations) and five successful augmentations (i.e., reproductive success of translocated individuals) based on genetic similarity with the source populations. A single native population founded six of the reintroduced herds, suggesting that environmental conditions did not need to match for populations to persist following reintroduction. Augmentations consisting of 18–57 animals including males and females succeeded, whereas augmentations of two males did not result in a detectable genetic signature. Our results provide insight on genomic distinctiveness of native and reintroduced herds, information on the relative success of reintroduction and augmentation efforts and their associated attributes, and guidance to enhance genetic contribution of augmentations and reintroductions to aid in bighorn sheep restoration.     

Mixed‐source reintroductions lead to outbreeding depression in second‐generation descendents of a native North American fish

Reintroductions are commonly employed to preserve intraspecific biodiversity in fragmented landscapes. However, reintroduced populations are frequently smaller and more geographically isolated than native populations. Mixing genetically, divergent sources are often proposed to attenuate potentially low genetic diversity in reintroduced populations that may result from small effective population sizes. However, a possible negative tradeoff for mixing sources is outbreeding depression in hybrid offspring. We examined the consequences of mixed‐source reintroductions on several fitness surrogates at nine slimy sculpin (Cottus cognatus) reintroduction sites in south‐east Minnesota. We inferred the relative fitness of each crosstype in the reintroduced populations by comparing their growth rate, length, weight, body condition and persistence in reintroduced populations. Pure strain descendents from a single source population persisted in a greater proportion than expected in the reintroduced populations, whereas all other crosstypes occurred in a lesser proportion. Length, weight and growth rate were lower for second‐generation intra‐population hybrid descendents than for pure strain and first‐generation hybrids. In the predominant pure strain, young‐of the‐year size was significantly greater than any other crosstype. Our results suggested that differences in fitness surrogates among crosstypes were consistent with disrupted co‐adapted gene complexes associated with beneficial adaptations in these reintroduced populations. Future reintroductions may be improved by evaluating the potential for local adaptation in source populations or by avoiding the use of mixed sources by default when information on local adaptations or other genetic characteristics is lacking.     

Behavioral Adaptation of Pan troglodytes troglodytes

As wild primate populations decline, numbers of orphaned primates, sanctuaries, and attempts to release primates back to the natural environment increase. Release projects frequently are poorly documented despite IUCN guidelines recommending post-release monitoring and systematic data collection as central to the process. Since 1996, Habitat Ecologique et Liberté des Primates (HELP) has been releasing wild-born orphaned chimpanzees into natural habitat in the Conkouati-Douli National Park, Republic of Congo. HELP developed a post-release monitoring system as an integral component. We present activity budgets and diet of released chimpanzees, and compared them to those of wild chimpanzee, as primary indicators of successful release. Feeding, moving, and resting dominated activity budgets, reflecting the overall patterns in wild populations. Diet was diverse and dominated by fruit, and the released chimpanzees showed specialization on a smaller number of species, as in many wild communities. The high survival rates of the chimpanzees and overall success of the release program are attributed to careful planning and post-release support facilitated via the monitoring process. Systematic post-release data collection monitoring has confirmed that wild-born chimpanzees can adjust behaviorally and nutritionally to the wild. Survival statistics of the reintroduced chimpanzees—confirmed 56%, possible 88%— reflect the behavioral adaptability.2nd revision March 11, 2005An erratum to this article can be found at     

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.     

Selection of radio transmitter and attachment method for post-release monitoring of captive-bred reintroduced Red-billed Curassow Crax blumenbachii, Brazil

Long-term monitoring of reintroduced individuals is a central component of many endangered species reintroduction programs. Radio-telemetry techniques are rarely used to monitor reintroduced captive-bred Cracids and few data exist regarding possible adverse effects of radio-tagging Cracids. In this study, we identify an appropriate radio transmitter design and develop a suitable attachment method that minimizes anthropogenic influence and enables long-term, post-release monitoring (2–3 years) of reintroduced captive-bred Red-billed Curassows in the Brazilian Atlantic Rainforest. We also review studies about the effects of different VHF radio transmitter models on survival, reproduction, behavior, and physiology of Galliformes.     

Patterns of ancestry and genetic diversity in reintroduced populations of the slimy sculpin: implications for conservation

Reintroductions are a common approach for preserving intraspecific biodiversity in fragmented landscapes. However, they may exacerbate the reduction in genetic diversity initially caused by population fragmentation because the effective population size of reintroduced populations is often smaller and reintroduced populations also tend to be more geographically isolated than native populations. Mixing genetically divergent sources for reintroduction purposes is a practice intended to increase genetic diversity. We documented the outcome of reintroductions from three mixed sources on the ancestral composition and genetic variation of a North American fish, the slimy sculpin (Cottus cognatus). We used microsatellite markers to evaluate allelic richness and heterozygosity in the reintroduced populations relative to computer simulated expectations. Sculpins in reintroduced populations exhibited higher levels of heterozygosity and allelic richness than any single source, but only slightly higher than the single most genetically diverse source population. Simulations intended to mimic an ideal scenario for maximizing genetic variation in the reintroduced populations also predicted increases, but they were only moderately greater than the most variable source population. We found that a single source contributed more than the other two sources at most reintroduction sites. We urge caution when choosing whether to mix source populations in reintroduction programs. Genetic characteristics of candidate source populations should be evaluated prior to reintroduction if feasible. When combined with knowledge of the degree of genetic distinction among sources, simulations may allow the genetic diversity benefits of mixing populations to be weighed against the risks of outbreeding depression in reintroduced and nearby populations.     

Inbreeding in reintroduced populations: the effects of early reintroduction history and contemporary processes

Maintaining genetic variation and minimizing inbreeding are central goals of conservation genetics. It is therefore crucial to understand the important population parameters that affect inbreeding, particularly in reintroduction programs. Using data from 41 reintroduced Alpine ibex (Capra ibex ibex) populations we estimated inbreeding since the beginning of reintroductions using population-specific Fst, and inbreeding over the last few generations with contemporary effective population sizes. Total levels of inbreeding since reintroduction of ibex were, on average, close to that from one generation of half-sib mating. Contemporary effective population sizes did not reflect total inbreeding since reintroduction, but 16% of variation in contemporary effective population sizes among populations was due to variation in current population sizes. Substantial variation in inbreeding levels among populations was explained by founder group sizes and the harmonic mean population sizes since founding. This study emphasizes that, in addition to founder group sizes, early population growth rates are important parameters determining inbreeding levels in reintroduced populations.     

Assessing release protocols for Canada lynx reintroduction in colorado

Reintroductions are a common strategy to restore ecosystem integrity, especially when top predators are involved. Reintroductions are often time consuming, expensive, and controversial, and thus understanding what aspects are important for a successful program is needed. Focusing on the example of the reintroduction of Canada lynx (Lynx canadensis) to Colorado, we investigated how different release protocols (RP) affected mortality within the first year post-release. We found that average monthly mortality in the study area during the first year decreased with time in captivity from 0.205 (95% CI = 0.069, 0.475) for lynx having spent up to 7 days in captivity to 0.028 (95% CI = 0.012, 0.064) for lynx spending >45 days in captivity before release. Our results also suggest that keeping lynx in captivity beyond 5–6 weeks accrued little benefit in terms of monthly survival. We found that, on a monthly average basis, lynx were as likely to move out (P = 0.196, SE = 0.032) as well as back onto (P = 0.143, SE = 0.034) the reintroduction area during the first year after release. Mortality was 1.6 times greater outside of the study area, suggesting that permanent emigration and differential mortality rates on and off reintroduction areas should be factored into sample size calculations for an effective reintroduction effort. A post-release monitoring plan is critical to providing information to assess aspects of RP and to improve survival of individuals. Future lynx and other carnivore reintroductions may use our results to help design reintroduction programs including both the release and post-release monitoring protocols. © 2011 The Wildlife Society.     

Ecosystem‐level effects of keystone species reintroduction: a literature review

The keystone species concept was introduced in 1969 in reference to top‐down regulation of communities by predators, but has expanded to include myriad species at different trophic levels. Keystone species play disproportionately large, important roles in their ecosystems, but human‐wildlife conflicts often drive population declines. Population declines have resulted in the necessity of keystone species reintroduction; however, studies of such reintroductions are rare. We conducted a literature review and found only 30 peer‐reviewed journal articles that assessed reintroduced populations of keystone species, and only 11 of these assessed ecosystem‐level effects following reintroduction. Nine of 11 publications assessing ecosystem‐level effects found evidence of resumption of keystone roles; however, these publications focus on a narrow range of species. We highlight the deficit of peer‐reviewed literature on keystone species reintroductions, and draw attention to the need for assessment of ecosystem‐level effects so that the presence, extent, and rate of ecosystem restoration driven by keystone species can be better understood.     

Reproduction and population density affect humoral immunity in bank voles under field experimental conditions

Density dependence is a common feature in the dynamics of animal populations. Availability of food resources critical to immunity is likely to be one of the mechanisms mediating the effect of population density on individual fitness. The ability to mount an immune response to an antigen is also affected by levels of immunosuppressive hormones associated with reproduction or mediating the response to ecological and social stress. We assessed variation in condition and intensity of humoral immune response to a T-cell-dependent antigen in bank voles (Clethrionomys glareolus) by experimentally altering population density before immunisation. Consistent with our prediction, males had lower humoral immunocompetence in the breeding than in the non-breeding season. Contrary to our expectation, males did not show enhanced immunocompetence and females showed depressed humoral immune response under experimentally lowered population density. Variation of immune response in relation to population density depended on sex, with females but not males showing lower immune response under experimentally reduced density. We conclude that humoral immunity of bank voles was affected by reproduction and social environment rather than by population density. Received: 2 November 1999 / Accepted: 22 March 2000     

Reproducing Bobcats to Cumberland Island, Georgia

Many felids are threatened by loss of habitat, lack of genetic diversity, and over-exploitation. The reintroduction of bobcats (Felis rufus) to Cumberland Island, Georgia provided an opportunity to reintroduce a mid-sized felid without the concern for species survival that is paramount with endangered species. We captured bobcats from the coastal plain region of Georgia, briefly held them in captivity, and released them on Cumberland Island. We describe and evaluate the protocols and techniques used to accomplish the reintroduction. Future reintroductions of felids should consider the problem of post-release dispersal, although our island was relatively isolated and inhibited dispersal. Also, any reintroduction effort should invest effort and resources into post-release monitoring of the population. Empirical knowledge about the effects of spatial distribution, genetics, population dynamics, especially mechanisms of population regulation, behavior, and environmental conditions on the viability of populations is critical to the conservation of endangered species. Future research of the bobcats on Cumberland Island will be able to address aspects of the population and genetic dynamics of a small, insular felid population.     

Survival and Breeding Transitions for a Reintroduced Bison Population: a Multistate Approach

Abstract: The iconic plains bison (Bison bison) have been reintroduced to many places in their former range, but there are few scientific data evaluating the success of these reintroductions or guiding the continued management of these populations. Relying on mark-recapture data, we used a multistate model to estimate bison survival and breeding transition probabilities while controlling for the recapture process. We tested hypotheses in these demographic parameters associated with age, sex, reproductive state, and environmental variables. We also estimated biological process variation in survival and breeding transition probabilities by factoring out sampling variation. The recapture rate of females and calves was high (0.78 ± 0.15 [SE]) and much lower for males (0.41 ± 0.23), especially older males (0.17 ± 0.15). We found that overall bison survival was high (>0.8) and that males (0.80 ± 0.13) survived at lower rates than females (0.94 ± 0.04), but as females aged survival declined (0.89 ± 0.05 for F ≥15 yr old). Lactating and non-lactating females survived at similar rates. We found that females can conceive early (approx. 1.5 yr of age) and had a high probability (approx. 0.8) of breeding in consecutive years, until age 13.5 years, when females that were non-lactating tended to stay in that state. Our results suggest senescence in reproduction and survival for females. We found little support for the effect of climatic covariates on demographic rates, perhaps because the park's current population management goals were predicated from drought-year conditions. This reintroduction has been successful, but continued culling actions will need to be employed and an adaptive management approach is warranted. Our demographic approach can be applied to other heavily managed large-ungulate systems with few or no natural predators.     

Natural expansion versus translocation in a previously human‐persecuted bird of prey

Many threatened species in Europe have been expanding their distributions during recent decades owing to protection measures that overcome historical human activity that has limited their distributions. Range expansion has come about via two processes, natural expansion from existing range and reintroductions to new ranges. Reintroductions may prove to be a better way to establish populations because individuals are less subject to competitive relationships lowering breeding success than individuals expanding from existing populations. Whether this is true, however, remains uncertain. We compared success of breeding pairs of an expanding and a reintroduced population of spanish imperial eagles monitored for over 15 years in the south of Spain. We found significant differences in productivity between breeding pairs of each population. Newly established territories in reintroduction areas were almost three times more productive than new territories established as individuals expanded out from an existing population. We conclude that among these eagle populations reintroduced to new areas may fare as well or better than individuals expanding out form existing populations.     

The effects of gene flow and population isolation on the genetic structure of␣reintroduced wild turkey populations: Are genetic signatures of source populations retained?

To counter losses of genetic diversity in reintroduced populations, species sometimes are reintroduced into networks of populations with the potential to exchange individuals. In reintroduced populations connected by gene flow, patterns of genetic structure initiated by the founding event may become obscured, and populations may eventually follow an isolation-by-distance model of genetic differentiation. Taking advantage of well-documented reintroduction histories of wild turkey populations in Indiana, we assessed the degree to which gene flow among reintroduced populations has obscured genetic signatures left by the founding events. Using a suite of nuclear microsatellite loci and sequence data from the mitochondrial control region, we characterized the level of genetic diversity and degree of genetic structure within and among: (1) reintroduced populations in isolated northern Indiana Fish and Wildlife Areas, (2) reintroduced populations in southern Indiana Fish and Wildlife Areas, where the distribution of populations is more continuous, and (3) source populations used for these reintroductions. We also utilized individual-based assignment tests to determine the relative contribution of source populations to the current distribution of alleles in reintroduced populations. Our results indicate that wild turkey reintroductions in Indiana have left distinct genetic signatures on populations that are detectable even after several decades. Although we found some case-specific evidence for gene flow, particularly in regions where populations are in close proximity, our data indicate on overall paucity of gene flow at a regional scale. Such post-reintroduction genetic monitoring has immediate implications for the design of optimal strategies to reintroduce wildlife for conservation and management.     

Genetic variation in a network of natural and reintroduced populations of Griffon vulture (Gyps fulvus) in Europe

It is generally considered that limiting the loss of genetic diversity in reintroduced populations is essential to optimize the chances of success of population restoration. Indeed, to counter founder effect in a reintroduced population we should maximize the genetic variability within the founding group but also take into account networks of natural populations in the choice of the reintroduction area. However, assessment of relevant reintroduction strategies requires long-term post-release genetic monitoring. In this study, we analyzed genetic data from a network of native and reintroduced Griffon vulture (Gyps fulvus) populations successfully restored in Southern Europe. Using microsatellite markers, we characterized the level of genetic diversity and degree of genetic structure within and among three native colonies, four captive founding groups and one long-term monitored reintroduced population. We also used Bayesian assignment analysis to examine recent genetic connections between the reintroduced population and the other populations. We aimed to assess the level of fragmentation among native populations, the effectiveness of random choice of founders to retain genetic variability of the species, the loss of genetic diversity in the reintroduced population and the effect of gene flow on this founder effect. Our results indicate that genetic diversity was similar in all populations but we detected signs of recent isolation for one native population. The reintroduced population showed a high immigration rate that limited loss of genetic diversity. Genetic investigations performed in native populations and post-released genetic monitoring have direct implications for founder choice and release design.     

Techniques for restoring fen vegetation on cut‐away peatlands in North America

Question: Which restoration measures (reintroduction techniques, reintroduction timing and fertilization) best enable the establishment of fen species on North American cut‐away peatlands? Location: Rivière‐du‐Loup peatland, southern Québec, Canada. Methods: In total, eight treatments which tested a combination of two reintroduction techniques, two reintroduction timings and the use of phosphorus fertilization were tested in a field experiment within a completely randomized block design. Results: Sphagnum transfer, a reintroduction technique commonly used for bog restoration in North America, was effective for establishing Sphagnum and Carex species. The hay transfer method, commonly used for fen restoration in Europe, was much less successful, probably due to questionable viability of reintroduced seeds. The treatments which included light phosphorus fertilization, had a higher Carex cover after three growing seasons. The timing of the reintroductions had no impact on the success of vegetation establishment. However, vegetation reintroduction should be carried out in the spring while the ground is still frozen to minimize other ecological impacts. Conclusions: The success of the diaspore reintroduction technique on small‐scale units indicates that a large‐scale restoration of fens using this technique is feasible.