Metapopulation dynamics and conservation of the marsh fritillary butterfly: Population viability analysis and management options for a critically endangered species in Western Europe

This study investigates the dynamics and viability of a marsh fritillary butterfly Euphydryas aurinia metapopulation in a Belgian successional landscape. Based on capture-mark-recapture and winter nest census data, we first estimated demography (survival and recruitment rates, population size, density dependence) and dispersal parameters (emigration rate, effect of patch connectivity on dispersal, mortality during dispersal). Then using RAMAS/GIS platform, we parameterised a population viability analysis (PVA) model with these parameters to simulate the future of this metapopulation under different scenarios.The metapopulation does not seem viable even if natural reforestation is controlled by adequate management. In its present state, the patch system is not able to sustain enough individuals: due to the large temporal fluctuations in demographic parameters, a carrying capacity far higher than currently would be necessary to limit extinction risk to 1%, suggesting the existence of an extinction debt for the species in Belgium. The situation of E. aurinia appears much worse compared to two other fritillary species threatened in Belgium, for which similar PVA are available. It is therefore urgent to increase the carrying capacity of the patch system. How and where it is achieved are of secondary importance for the gain in viability: improvement of habitat quality through restoration, or increase of habitat quantity via enlargement of existing patches and/or creation of new habitat in the matrix. A regime of management based on regular re-opening and maintenance of habitat patches may be the only guarantee of long-term persistence for this critically endangered species in Belgium.     

Population management of threatened taxa in captivity within their natural ranges: Lessons from Andean bears (Tremarctos ornatus) in Venezuela

Populations of threatened taxa in captivity within their natural ranges can make important contributions to conservation, but these may be compromised by the inappropriate application of population management goals developed in other contexts. We conducted demographic, genetic, and population viability analyses on the captive population of Andean bears (Tremarctos ornatus) in Venezuela to investigate the management of within-range captive populations in general, and to better integrate this population into the conservation of Andean bears in particular. We found that although the present population is very small and not internally self-sustaining, incorporation of confiscated wild individuals has resulted in a low average number of generations in captivity and low inbreeding, with moderate gene diversity and a high probability of future population persistence. However, past imports from extra-range populations have been from over-represented lineages of unknown origin, which have mixed with under-represented Venezuelan ones, reducing the future value of the Venezuelan population as a source for founder stock. Our analyses indicate that the rate of incorporation of wild recruits is a major factor influencing proxy measures of conservation value, and distinguishing within- from extra-range populations. This implies that, contrary to conventional wisdom, internal self-sustainability can be a misguided goal in within-range populations, which furthermore may not be suitable destinations for surplus animals from captive populations elsewhere.     

An empirical evaluation of the area and isolation paradigm of metapopulation dynamics

Much of metapopulation theory assumes that the persistence of individual populations in a metapopulation, and persistence of the metapopulation as a whole, is best modeled by the area of habitat patches and their isolation. Estimates of isolation typically include a measure of geographic distance and a measure of either population size or patch area. This “area and isolation paradigm” assumes a functional relationship between the area of a patch and its extinction probability, and between isolation of a patch and its colonization probability. Although these assumptions are fundamental to use of incidence function models of metapopulation dynamics, the assumptions have been validated in only a small number of studies. We tested the ability of area and isolation to predict extinction and colonization patterns using multiple-year occupancy data for 10 species from three taxonomic groups (butterflies, amphibians, and birds). We examined 13 potential models of metapopulation dynamics. All models included four basic parameters: occupancy during the first year of the survey, probability of extinction, probability of colonization, and single-visit detection probability. In eight models, each parameter was either constant or time-dependent. Five models included a patch-level covariate of extinction probability (patch area or population size), colonization probability (connectivity, the inverse of isolation), or both. Extinction patterns generally were predicted more effectively as a function of local population size than as a function of patch area, a constant probability of extinction, or a time-dependent probability of extinction. In most cases, inclusion of connectivity as a patch-level covariate did not improve predictions of colonization patterns. We estimated single-visit detection probabilities for all species in our analyses, thus providing evidence-based guidelines for the refinement of future monitoring protocols.     

Risks of a late start to captive management for conservation: Phenotypic differences between wild and captive individuals of a viviparous endangered skink (Oligosoma otagense)

Maintenance of demographically and genetically self-sustaining populations in captivity can assist conservation of threatened species. Captivity can, however, lead to changes in phenotype, though to date this issue has received little attention in reptiles. We compared phenotypic differences in the now critically-endangered Otago skink (Oligosoma otagense) between wild specimens (Otago, southern New Zealand) and in captivity (North Island). Individuals of this long-lived, viviparous species have been maintained up to three generations in captivity, primarily by private herpetoculturists, but increasingly there is interest in integrating management of captive stocks with conservation in situ. For the same snout-vent length, captive skinks pooled across three colonies had a significantly heavier body mass, wider tail base, longer tail (juveniles only), faster growth rate and much slower sprint speed than in the wild. Captive skinks also lacked ectoparasitic mites and haemogregarine parasites, and experienced warmer temperatures with probably greater access to food. Our study demonstrates the importance of not treating captive management for conservation as a tool of last resort. Important questions, if captive-raised animals are to be released to the wild, are is it better for released skinks to run swiftly or to be heavy-bodied, and what role does reinfestation with native parasites have in determining this balance? We also recommend genetic analysis and studbook management of captive stocks, research to determine implications of heavy body mass for reproduction in captivity, and production of at least some offspring for release inside larger enclosures within the local climate.     

Conservation biology for suites of species: Demographic modeling for Pacific island kingfishers

Conservation practitioners frequently extrapolate data from single-species investigations when managing critically endangered populations. However, few researchers initiate work with the intent of making findings useful to conservation efforts for other species. We presented and explored the concept of conducting conservation-oriented research for suites of geographically separated populations with similar natural histories, resource needs, and extinction threats. An example was provided in the form of an investigation into the population demography of endangered Micronesian kingfishers (Todiramphus cinnamominus). We provided the first demographic parameter estimates for any of the 12 endangered Pacific Todiramphus species, and used results to develop a population projection matrix model for management throughout the insular Pacific. Further, we used the model for elasticity and simulation analyses with demographic values that randomly varied across ranges that might characterize congener populations. Results from elasticity and simulation analyses indicated that changes in breeding adult survival exerted the greatest magnitude of influence on population dynamics. However, changes in nestling survival were more consistently correlated with population dynamics as demographic rates were randomly altered. We concluded that conservation practitioners working with endangered Pacific kingfishers should primarily focus efforts on factors affecting nestling and breeder survival, and secondarily address fledgling juveniles and helpers. Further, we described how the generalized base model might be changed to focus on individual populations and discussed the potential application of multi-species models to other conservation situations.     

Conserving the genetic resources of crop wild relatives in European Protected Areas

European native plant diversity is currently suffering erosion and extinction and thus, it is crucial to improve conservation strategies to maintain this essential resource. If unchecked, this genetic erosion and species extinction will cause unnecessary and irreversible harm to the economy and social well being of Europe. Much plant biodiversity is undoubtedly found in the existing 9654 European protected areas that cover 1,066,358 km², but clearly targeted and active conservation of priority plant species is required within these protected areas. To help ensure more efficient long-term sustainable conservation, a novel approach to the in situ conservation of European plants, notably crop wild relatives, is suggested. The purpose of this approach is to know what plant genetic resources (PGR) we have, where they are located and to assess whether the current network of protected areas includes a representative sample of European PGR diversity. The generation of in situ conservation and management plans for PGR populations in existing protected areas can significantly improve the present conservation status. Additionally, the identification of gaps of certain PGR in current protected areas can provide the basis for the designation of new complementary PGR in situ reserves.     

Temporal genetic analysis of the critically endangered oriental white-backed vulture in Pakistan

Populations of oriental white-backed vultures (Gyps bengalensis) in south Asia have declined over 95% since the mid-1990s due to feeding on livestock carcasses that had been treated with diclofenac, an anti-inflammatory pharmaceutical that is fatal to Gyps vultures. To prevent extinction, captive breeding efforts have been initiated; however, given the overall decline, it is not known to what extent levels of genetic diversity currently exist in the remaining populations. Here we document temporal genetic diversity levels during the 2000-2006 interval for the last remaining breeding colony of oriental white-backed vultures in Pakistan, and show with simulations that a much larger captive population size is required than currently maintained to prevent further loss of genetic diversity. Before this species is extinct in the wild, it is crucial that additional individuals are included in the captive population.     

Generations in captivity increases behavioral variance: considerations for captive breeding and reintroduction programs

Long-term maintenance of captive populations followed by release of captive animals into the wild is one of many approaches to endangered species conservation. To assess captivity's effects on behavior, a simulated predator was presented and response behaviors measured in oldfield mice, Peromyscus polionotus subgriseus. The animals tested were from four populations collected from Ocala National Forest, Florida, and held in captivity for varying numbers of generations: 35, 14, 2, and 0 (wild caught). Results show (1) that the more generations a population has been in captivity, the less likely an individual is to take cover after seeing a predator and (2) variance in predator-response behaviors increases with generations in captivity. These results point to two ways in which captivity can compromise animal behavior and, in turn, the success of reintroduction programs. First, because individuals from populations that have been in captivity for multiple generations seek refuge less often than their wild counterparts, they might experience increased mortality in the wild due to predation. Second, increased behavioral variance could translate into decreased survivorship upon reintroduction. Therefore, more individuals will need to be released to reach the targeted wild population size.     

Sampling on private property to evaluate population status and effects of land use practices on the gopher tortoise, Gopherus polyphemus

Although private properties are predicted to play an increasingly significant role in conservation, surveys of species of special concern are rare on these lands. We created a template for a multi-county survey of randomly selected sites and sampled for burrows of the gopher tortoise (Gopherus polyphemus) in south-central Georgia, USA. Current land use was strongly correlated with tortoise population condition. The highest densities of tortoise burrows were found on lands with open-canopied pine stands that were managed with prescribed fire, a practice associated with types of selection forestry and/or wildlife management. Agricultural sites and unburned areas provided poor habitat and pine plantations were only slightly better. Our estimates of tortoise population densities indicated that the current landscape supports less than 20% of the animals present before implementation of modern land use practices. In addition, our estimate for density of active burrows was approximately one third of that projected for the entire state range 20 years ago by Auffenberg and Franz [Auffenberg, W., Franz, R., 1982. The status and distribution of the gopher tortoise (Gopherus polyphemus). In: Bury, R.B. (Ed.), North American Tortoises: Conservation and Ecology (US Fish and Wildlife Service Wildlife Research Report 12). pp. 95-126]. However, some good sites for gopher tortoises remain in south Georgia and our data also suggested that extraordinary conservation actions may not be required if ways can be developed to retain traditional land management practices on private property.     

Phenotypic differentiation in fitness related traits between populations of an extremely rare sunflower: Conservation management of isolated populations

Knowledge of the genetic and demographic consequences of rarity is crucial when evaluating the effects of habitat loss and fragmentation on population viability, and for creating management plans in rare plant species. Reduction in population size and in the number of populations can lead to decreased genetic diversity and increased inbreeding. Genetic diversity is often correlated with fitness and is frequently used to identify populations of greatest conservation concern, or those that may be good candidates for ex situ conservation programs. However, an association between these factors is not always clear, and crossing studies evaluating whether there is phenotypic differentiation among populations in fitness related traits can inform managers of suffering populations or good sources for ex situ materials. Crossing studies can also evaluate the potential for genetic rescue to boost fitness in suffering populations. To address these questions, we conducted two generations of controlled crosses between populations of the extremely rare and fragmented sunflower, Helianthus verticillatus. We measured achene viability, germination, survival, and pollen viability (F₁ only) in 176 F₁ and 159 F₂ families. The populations were differentiated with respect to phenotypic fitness measures with one population having significantly lower achene viability and germination. Also, the potential for genetic rescue was observed as gene flow into the less fit population resulted in higher fitness measures in both the F₁ and F₂. Results are discussed with respect to the importance of combining genetic marker data with crosses and the implications for conservation in disjunct populations of rare species.     

Inbreeding in red-cockaded woodpeckers: Effects of natal dispersal distance and territory location

Inbreeding depression constitutes a significant threat to the viability of small populations. In addition to small size and isolation of populations, short distance dispersal may elevate risk of inbreeding, but empirical evidence is scarce. Inbreeding depression has been demonstrated in the highly endangered red-cockaded woodpecker Picoides borealis. It has been suggested that conservation efforts to support extant populations should aim at spatially aggregating territories to enhance dispersal success. This however may aggravate inbreeding risk because distance between territories and hence dispersal distances become short. We analysed empirical data from a long-term study of the demography of the red-cockaded woodpecker and found that inbreeding risk varied inversely with natal dispersal distance of the mother. Using an individual-based, spatially explicit population model that incorporates simulations of environmental and demographic stochasticity and an empirically derived, species-specific estimate of inbreeding costs, we demonstrated that inbreeding depression significantly elevated extinction risk in this species. On the other hand, even though dispersal distances in populations with spatially aggregated territories were shorter and the proportion of inbred individuals was higher than in other populations of the same size, such populations were still more persistent. Despite the overall adverse effect of inbreeding depression on viability of red-cockaded woodpecker populations, lowering interterritorial distances can be viewed as a valuable conservation tool. Given the small size and isolated location of most extant red-cockaded woodpecker populations however, our findings suggest that inbreeding depression represents a significant threat to the survival of this species.     

Factors affecting persistence of terrestrial orchids in wet meadows and implications for their conservation in a changing agricultural landscape

We examined the occurrence of Dactylorhiza majalis, the most abundant terrestrial orchid species growing in rapidly disappearing wet meadows, at 50 historical sites for 3 years. We aimed to find the most frequent reasons for its recent extinction at many sites. We found that the main reasons for its extinction were absence of mowing, intensive fertilisation and washouts of fertilisers from fields nearby. At extant sites, we studied its biometric characteristics and composition of surrounding vegetation, to determine factors affecting its persistence. Bad performance of persisting populations of this species was associated with prevalence of grasses, low May temperatures and absence of mowing. This confirms, at metapopulation level, what has previously been observed at the level of individual populations. We suggest that the system of agricultural subsidies in the country should change towards more sensitive allocation of funds to those farmers, who will adopt the appropriate management of wet meadows and their surroundings.     

Population viability analysis of European bison populations in Polish and Belarusian parts of Bia?owie?a Forest with and without gene exchange

European bison (Bison bonasus) became extinct in the wild at the beginning of the 20th century. The contemporary Lowland line of bison was founded by seven individuals that survived in captivity. The largest population of Lowland bison live in the Bia?owie?a Forest, but the forest and the population are divided by a border fence between Poland and Belarus. This fence is a barrier to the movement of ungulates. In this study, we used population genetic models to predict the future viability of the Polish and Belarusian bison populations. We determined the founder contribution, founder equivalent, mean inbreeding coefficient, mean kinship, and the proportion of genetic diversity retained in the Belarusian bison population. Although the founding group of the Belarusian population was larger than that of the Polish population, the latter had more favourable genetic parameters. We assessed inbreeding depression for fecundity in free-ranging European bison compared to captive individuals. Using population viability analysis (PVA) we modelled both bison populations with or without gene exchange, and with or without incorporating the kinship of the founders. When founder kinship was included, in both populations the mean number of alleles and the gene diversity retained within extant populations decreased substantially compared to PVA models in which founders were not related. The worst genetic parameters were obtained for the Belarusian population under a scenario in which the founders are related and gene exchange is lacking, which is the closest to the real situation. Creation of passages for animals by partial removal of the border fence would have a favourable effect on the genetic variation and viability of both bison populations, especially the Belarusian.     

An approach for regional threat assessment under IUCN Red List criteria that is robust to uncertainty: The Fiordland bottlenose dolphins are critically endangered

Numerous globally abundant species are exposed to human impacts that threaten the viability of regional populations. Assessing and characterising the risks faced by these populations can have significant implications for biodiversity conservation, given the ecological importance of many such species. To address these risks, the IUCN is starting to conduct assessments of regional populations in addition to species-level assessments of conservation status. Here, we demonstrate a threat assessment process that is robust to uncertainty, applying the IUCN criteria to a regional population of bottlenose dolphins in Fiordland, New Zealand. We compiled available population-specific information to assess the population under the five Red List criteria. We estimated there were 205 Fiordland bottlenose dolphins (CV = 3.5%), using current estimates of abundance for two sub-populations and stochastic modelling of an earlier estimate for the third sub-population. Population trajectory and extinction risk were assessed using stochastic age-structured Leslie matrix population models. The majority of model runs met the criteria for classification as critically endangered (C1: 67.6% of runs) given the number of mature individuals (123; CV = 6.7%) and the predicted rate of population decline (average decline: 31.4% over one generation). The evidence of isolation of the population confirms this was an appropriate regional classification. This approach provided an assessment that was robust to uncertainty.     

Minimum viable population and conservation status of the Atlantic Forest spiny rat Trinomys eliasi

A population viability analysis (PVA) was conducted to assess the minimum viable population (MVP) of the Atlantic Forest spiny rat Trinomys eliasi, a species threatened by habitat loss and restricted geographical distribution. Objectives were to suggest quasi-extinction thresholds, estimate minimum areas of suitable habitat (MASH) and MVPs, and compare results with the species’ current status. The computer package VORTEX was used. The model predicted sizes of 200 animals to achieve demographic stability, but buffering declines in genetic variability required populations of 2000 animals. Estimated MASHs were approximately 250 and 2500 ha for demographic and genetic stability, respectively. Mortality rate and mean litter size were the most sensitive parameters to changes in model assumptions. The protection of known populations and the search for extant populations are the first steps in conservation. T. eliasi's issue could help protecting the coastal shrubland ecosystem of Rio de Janeiro state. Observing IUCN's criteria for listing threatened species, it is suggested that T. eliasi should be ranked as vulnerable in red lists.     

Conservation of European wild rabbit populations when hunting is age and sex selective

Several predator species at risk of extinction in Southwestern Europe are dependent on the population density of European wild rabbits Oryctolagus cuniculus. Rabbit populations in the region, however, have recently undergone dramatic decreases in population density, which may be exacerbated by hunting. Current hunting policies set the autumn-winter season, just before the start of rabbit reproduction, as the main hunting season, and previous theoretical models have estimated that the current hunting season may have the greatest negative impact on rabbit abundance and should be changed. We utilised a model for rabbit population dynamics to determine the effects of the timing of hunting during two seasons, summer and autumn, on the tendency of rabbit populations to be over-harvested and on the number of rabbits hunted. This model included field estimates of age- and sex-selection biases of hunting by shotgun. Scenarios with different hunting rates and sex- and age-selection probabilities of hunting were simulated for populations with different turnover levels and with and without compensatory mortality mechanisms. Field estimations showed that hunting in summer was juvenile-biased whereas autumn hunting was juvenile- and male-biased. In contrast to previous findings, our modelling results suggested that hunting in autumn may be the most conservative option for harvesting of rabbit populations, since these populations were more prone to be over-harvested during the summer. The differences between the two seasons in number of rabbits hunted were dependent on population dynamics and hunting sex- and age-selection probabilities. Our findings suggest that altering of current hunting policies would not optimise the exploitation or conservation of wild rabbit populations, but that the latter may be improved by some changes in the timing of hunting.     

Dynamics of a declining amphibian metapopulation: Survival, dispersal and the impact of climate

Climate can interact with population dynamics in complex ways. In this study we describe how climatic factors influenced the dynamics of an amphibian metapopulation over 12 years through interactions with survival, recruitment and dispersal. Low annual survival of great crested newts (Triturus cristatus) was related to mild winters and heavy rainfall, which impacted the metapopulation at the regional level. Consequently, survival varied between years but not between subpopulations. Despite this regional effect, the four subpopulations were largely asynchronous in their dynamics. Three out of the four subpopulations suffered reproductive failure in most years, and recruitment to the metapopulation relied on one source. Variation in recruitment and juvenile dispersal was therefore probably driving asynchrony in population dynamics. At least one subpopulation went extinct over the 12 year period. These trends are consistent with simulations of the system, which predicted that two subpopulations had an extinction risk of >50% if adult survival fell below 30% in combination with low juvenile survival. Intermittent recruitment may therefore only result in population persistence if compensated for by relatively high adult survival. Mild winters may consequently reduce the viability of amphibian metapopulations. In the face of climate change, conservation actions may be needed at the local scale to compensate for reduced adult survival. These would need to include management to enhance recruitment, connectivity and dispersal.     

Viability of mountain caribou in British Columbia, Canada: Effects of habitat change and population density

Population viability analyses (PVA) are frequently employed to develop recovery plans and inform management of endangered species. Translating results from PVA into meaningful management recommendations often depends on an understanding of how population parameters change with environmental conditions as well as population density. The decline of mountain caribou (Rangifer tarandus caribou) in British Columbia, Canada, is believed to be caused by apparent competition with alternative prey species following changes to the forest age structure from timber harvest and wildfire. In addition, populations have been shown to decline at faster rates at low population density. To evaluate the potential effects of habitat change and population density on population persistence, we used stochastic projection models for 10 distinct populations varying in initial size from <10 to approximately 150 females. In an initial model, we used estimates of vital rates based on information sampled from >350 radiocollared caribou between 1984 and 2004. We then compared the results of the initial model to a set of models that evaluated the effects of habitat conditions and population density via their expected relationships to female adult survival. Assuming that vital rates remain constant over a 200-year time frame, only three populations have high probabilities (>0.95) of extinction. When models incorporate the declines in adult female survival know to occur with increasing proportions of young forest and declining population densities, all 10 populations are predicted to decline to extinction within <200 years. Based on our results, we suggest that PVA models that fail to incorporate the effects of changes in vital rates with habitat and population density may lead to overly optimistic assessments of the probability of population persistence in endangered species.     

Estimates of minimum viable population sizes for vertebrates and factors influencing those estimates

Population size is a major determinant of extinction risk. However, controversy remains as to how large populations need to be to ensure persistence. It is generally believed that minimum viable population sizes (MVPs) would be highly specific, depending on the environmental and life history characteristics of the species. We used population viability analysis to estimate MVPs for 102 species. We define a minimum viable population size as one with a 99% probability of persistence for 40 generations. The models are comprehensive and include age-structure, catastrophes, demographic stochasticity, environmental stochasticity, and inbreeding depression. The mean and median estimates of MVP were 7316 and 5816 adults, respectively. This is slightly larger than, but in general agreement with, previous estimates of MVP. MVPs did not differ significantly among major taxa, or with latitude or trophic level, but were negatively correlated with population growth rate and positively correlated with the length of the study used to parameterize the model. A doubling of study duration increased the estimated MVP by approximately 67%. The increase in extinction risk is associated with greater temporal variation in population size for models built from longer data sets. Short-term studies consistently underestimate the true variances for demographic parameters in populations. Thus, the lack of long-term studies for endangered species leads to widespread underestimation of extinction risk. The results of our simulations suggest that conservation programs, for wild populations, need to be designed to conserve habitat capable of supporting approximately 7000 adult vertebrates in order to ensure long-term persistence.     

Hatch size, somatic growth rate and size-dependent survival in the endangered ploughshare tortoise

Successful conservation requires a good understanding of both the direct and indirect causes of any decline in population size. Harvests of wild populations often target the largest, oldest individuals that have the greatest economic value. If these individuals contribute disproportionately more to recruitment than conspecifics, the harvest will cause a greater reduction in population viability than initially anticipated. The ploughshare tortoise, endemic to Madagascar, has been reduced to <600 individuals due to exploitation and habitat loss. A trial release of captive-bred juveniles has been carried out but the relative suitability of individuals for release, in terms of body size, was not considered. Using data from a long-term mark-recapture study of an unharvested wild population of ploughshare tortoises, we found that larger juveniles were significantly more likely to survive their first year of life than smaller tortoises. Juveniles that survived beyond their first year of life generally grew at the same rate, but had a significantly larger hatch size (mean = 41.7 mm), compared with juveniles that did not survive (mean = 39.3 mm). The conservation implications of these results are that release of captive-bred ploughshare tortoises is likely to be more successful if larger individuals are released. Previous studies have reported larger female ploughshare tortoises laying larger eggs which hatch larger juveniles. This study shows individuals with a larger hatch size retain their size advantage over smaller conspecifics and are more likely to survive their first year of life. This suggests a harvest that targets the largest females in the ploughshare tortoise population could be highly detrimental to population viability.