Reintroduced Population Research Articles

Microsatellite and mitochondrial DNA variation defines island genetic reservoirs for reintroductions of an endangered Australian marsupial, Perameles bougainville

Natural populations of the endangered western barred bandicoot (Perameles bougainville) now exist on only two islands in Shark Bay, Western Australia. Our aim was to investigate genetic diversity in natural, reintroduced, and captive populations of the bandicoots and to assess the extent of divergence between the populations. The contemporary isolation of the natural populations has resulted in heterogeneity of allele frequency between the islands, which has acted to maintain a higher combined diversity than would be expected from either population on its own. These findings highlight how remnant island populations can act as genetic reservoirs to maximize diversity for reintroductions into a species former range. Although diversity is high between island populations, diversity within populations, based on six microsatellite loci, are amongst the lowest ever recorded for populations of marsupials. The mtDNA sequence data indicate that the two remaining natural populations show only minor divergence from each other, with the five haplotypes separated by just single base pairs. The reintroduced population and captive colonies show evidence for the loss of diversity related to genetic drift operating on small isolated populations.

Captive breeding and the reintroduction of Mexican and red wolves

Mexican and red wolves were both faced with extinction in the wild until captive populations were established more than two decades ago. These captive populations have been successfully managed genetically to minimize mean kinship and retain genetic variation. Descendants of these animals were subsequently used to start reintroduced populations, which now number about 40-50 Mexican wolves in Arizona and New Mexico and about 100 red wolves in North Carolina. The original captive Mexican wolf population was descended from three founders. Merging this lineage with two other captive lineages, each with two founders, has been successfully carried out in the captive population and is in progress in the reintroduced population. This effort has resulted in increased fitness of cross-lineage wolves, or genetic rescue, in both the captive and reintroduced populations. A number of coyote-red wolf hybrid litters were observed in the late 1990s in the reintroduced red wolf population. Intensive identification and management efforts appear to have resulted in the elimination of this threat. However, population reintroductions of both Mexican and red wolves appear to have reached numbers well below the generally recommended number for recovery and there is no current effort to re-establish other populations.

Genetic rescue and inbreeding depression in Mexican wolves

Although inbreeding can reduce individual fitness and contribute to population extinction, gene flow between inbred but unrelated populations may overcome these effects. Among extant Mexican wolves (Canis lupus baileyi), inbreeding had reduced genetic diversity and potentially lowered fitness, and as a result, three unrelated captive wolf lineages were merged beginning in 1995. We examined the effect of inbreeding and the merging of the founding lineages on three fitness traits in the captive population and on litter size in the reintroduced population. We found little evidence of inbreeding depression among captive wolves of the founding lineages, but large fitness increases, genetic rescue, for all traits examined among F1 offspring of the founding lineages. In addition, we observed strong inbreeding depression among wolves descended from F1 wolves. These results suggest a high load of deleterious alleles in the McBride lineage, the largest of the founding lineages. In the wild, reintroduced population, there were large fitness differences between McBride wolves and wolves with ancestry from two or more lineages, again indicating a genetic rescue. The low litter and pack sizes observed in the wild population are consistent with this genetic load, but it appears that there is still potential to establish vigorous wild populations.

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.

Junk ingestion and nestling mortality in a reintroduced population of California Condors Gymnogyps californianus

AbstractIngestion of foreign anthropogenic material, here called junk, has been documented in many avian taxa but has become especially problematic in some Old World Gyps vulture populations within the last 30 years. Here, we document the effects of ingested junk on a reintroduced population of the Critically Endangered California Condor Gymnogyps californianus in southern California, U.S.A. Of 13 breeding attempts to date (2001–2005), only one has resulted in successful fledging. Of nests where either the nest substrate was sifted (n = 10) or nestlings (n = 8) were examined, all but one held junk. Nine nestlings hatched in the wild between 2002 and 2005; of these six died at or near nests and two were removed from the wild for health reasons. Four dead nestlings and two removed from the wild held substantial quantities of junk. In two cases, junk ingestion was determined to be the cause of death. Five of six dead nestlings had elevated hepatic copper levels (150–531 ppm dry weight) although the significance of this, if any, remains undetermined. In comparison with historic condor nests (n = 69), junk was more prevalent and of greater size and quantity in reintroduced condor nests. To date, junk ingestion has been the primary cause of nest failure in the reintroduced condor population and threatens the reestablishment of a viable breeding population in southern California.

SalmonellaTyphimurium in Hihi, New Zealand

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Competitive behaviour and feeding rate in a reintroduced population of Griffon VulturesGyps fulvus

Intraspecific competitive behaviours were studied in a reintroduced population of Griffon VulturesGyps fulvusin order to describe the pattern of competition between ages and sexes, assess the effect of reintroduction on competitive behaviour, and study the potential consequences of food management on competition. There was no evidence for a difference in feeding or display rates between age classes. However interaction rates, aggressiveness and dominance were higher in old adults than in the other age classes. No difference in the pattern of competition was found between sexes. There was no difference in the competitive ability (feeding rate and dominance) of reintroduced and wild‐bred individuals. Feeding rates increased with resource availability. Group size also increased with food mass, but was lower than the theoretical maximum number of birds. This may be evidence of competition by interference where some individuals are able to increase their feeding rate by the exclusion of others. An increase in both the number of carcasses and the number of feeding sites is thus recommended to induce dispersal and reduce this competition.

Susceptibility of Bush Stone-curlews (Burhinus grallarius) to sodium fluoroacetate (1080) poisoning

Although baiting for feral predators with sodium fluoroacetate (1080) benefit native fauna over much of Australia by reducing the abundance of those predators, there is a potential risk of poisoning to non-target species. Bush Stone-curlews (Burhinus grallarius) have declined over much of mainland southern Australia owing to predation by Red Foxes (Vulpes vulpes), but they have the potential to eat and be affected by 1080 baits. This paper explores the extent to which 1080-baiting programs may have an adverse effect on extant or reintroduced populations of Bush Stone-curlews. Our study used Bush Stone-curlews from a population that was not adapted to naturally occurring 1080, so our results are likely to be relevant throughout the range of the species. We determined the approximate lethal dose (ALD) of 1080 for Bush Stone-curlews to be 10–15 mg kg−1. Thus a Bush Stone-curlew weighing 700 g would need to eat between three and four baits, each containing 3 mg of 1080, to receive an ALD. In unforced trials, the Bush Stone-curlews in our study did not eat (undosed) meat or grain baits. Dying food blue did not deter Bush Stone-curlews from eating it. Thus, sole reliance on blue dyes to deter non-target species from taking baits seems unwise. Our results indicate that reintroduction programs for Bush Stone-curlew are unlikely to be affected by concurrent 1080-baiting for feral animal control.

Dispersal, survival, and reproduction of wild-born, yearling swift foxes in a reintroduced population

From 1998 to 2002, the Blackfeet Tribe and Defenders of Wildlife reintroduced 123 captive-reared swift foxes ( Vulpes velox (Say, 1823)) to the Blackfeet Reservation in northern Montana. Because yearling swift foxes are colonizers of vacant habitats and are at the periphery of range expansion, we estimated 1st-year survival and explored aspects of dispersal to ascertain the contribution of wild-born juveniles to the reintroduction effort. First-year survival (post den emergence) of swift foxes averaged 0.38 and 0.36 for 2003–2004 and 2004–2005, respectively. Half of the females that survived to 1 June of their 1st year reproduced. Most dispersal (77%) and mortality (85%) occurred in autumn, with 80% of mortalities attributable to predation. Dispersal distance was not different among sexes and averaged 10.4 km. Understanding the contribution of yearling swift foxes — the colonizers — to reestablishing populations is important because several entities are currently reintroducing swift foxes and some states have expanding populations.

Age estimation of pouch young and growth of the burrowing bettong, Bettongia lesueur, (Marsupialia: Potoroidae) on Heirisson Prong, Shark Bay, Western Australia

Measurements of hind foot length, weight, head length and tail length were collected from pouch young, young at foot, sub-adults and adults of a reintroduced population of the vulnerable burrowing bettong, Bettongia lesueur, on Heirisson Prong, Shark Bay, Western Australia. A key based on qualitative characteristics was used to age individuals and a Richards growth function was fitted to plots of hind foot length versus age. The patterns of growth and morphological characteristics were similar for males and females. Both sexes exhibited a growth pattern typical of a medium-sized macropod with an initial slow phase of growth followed by a rapid phase that slowed as adult size was reached. The growth curves are suitable for broad estimates of the age of wild-caught animals from pouch young to early adulthood.

Activity Patterns and Foraging Behavior of the Endangered Grand Cayman Blue Iguana,Cyclura lewisi

The historic rarity of the critically endangered Grand Cayman blue iguana, Cyclura lewisi, has prevented detailed research on this species prior to this decade. This study primarily used focal animal observations, transect sweeps, and radio-telemetry to document the behavioral ecology of a captive-bred, reintroduced population of adult C. lewisi in a botanic park on Grand Cayman. Activity budgets and foraging budgets are presented for each sex in each season, and for all data combined. Distributions of basking time and active time differed between the two seasons. Iguanas both emerged earlier and retreated later in the summer than in the fall. Of the small percentage of time spent active, iguanas mostly foraged and engaged in locomotion. Iguanas spent little time in trees or bushes or inside of retreats during the day. Observations of extensive tongue-touching of retreats, substrates, and feces suggest an importance of chemosensory ability in C. lewisi. Iguanas primarily consumed plant matter, of which the majority was non-cultivated plants in the park and surrounding area. Limited geophagy, coprophagy, and consumption of invertebrates were observed. Supplemental feeding contributed little to the overall diet of iguanas, but appeared to make iguanas more aggressive towards humans. Iguanas were heavily habituated to human and vehicular disturbances, which were common occurrences. Aspects of the behavioral ecology of C. lewisi reported here will assist in the conservation of this and other endangered iguanas.

Moderate inbreeding depression in a reintroduced population of North Island robins

AbstractReintroductions of threatened species are increasingly common in conservation. The translocation of a small subset of individuals from a genetically diverse source population could potentially lead to substantial inbreeding depression due to the high genetic load of the parent population. We analysed 12 years of data from the reintroduced population of North Island robins Petroica longipes on Tiritiri Matangi Island, New Zealand, to determine the frequency of inbreeding and magnitude of inbreeding depression. The initial breeding population consisted of 12 females and 21 males, which came from a large mainland population of robins. The frequency of mating between relatives (f&gt;0; 39%, n=82 pairs) and close relatives (f=0.25; 6.1%) and the average level of inbreeding (f=0.027) were within the range reported for other small island populations of birds. The average level of inbreeding fluctuated from year to year depending on the frequency of close inbreeding (e.g. sib–sib pairs). We found evidence for inbreeding depression in juvenile survival, with survival probability estimated to decline from 31% among non‐inbred birds (f=0) to 11% in highly inbred juveniles (f=0.25). The estimated number of lethal equivalents based on this relationship (4.14) was moderate compared with values reported for other island populations of passerines. Given that significant loss of fitness was only evident in highly inbred individuals, and such individuals were relatively rare once the population expanded above 30 pairs, we conclude that inbreeding depression should have little influence on this robin population. Although the future fitness consequences of any loss of genetic variation due to inbreeding are uncertain, the immediate impact of inbreeding depression is likely to be low in any reintroduced population that expands relatively quickly after establishment.

Cub adoption by a translocated Louisiana black bear

Abstract We documented the adoption of a cub by a female Louisiana black bear (Ursus americanus luteolus) after the cub was apparently abandoned by its biological mother. The adoption and presumed abandonment took place in a reintroduced population and involved recently translocated bears. We are unaware of previous published descriptions of free ranging female black bears adopting cubs without human intervention.

Estimating the Viability of a Reintroduced New Zealand Robin Population as a Function of Predator Control

Wildlife managers often have a good understanding of the threats faced by populations, but they need to know the intensity of management required for populations to survive. Managers therefore need quantitative projections for populations under different management regimes rather than just qualitative comparisons. However, quantitative projections are subject to tremendous uncertainty, particularly for small populations monitored for short time spans. We assess the level of predator control needed for a reintroduced population of North Island robins (Petroica longipes) to grow, accounting for uncertainty associated with parameter estimation, model structure, and demographic stochasticity. The robin population grew when exotic rats were reduced to low levels ( 1 if rat tracking were 20% probability of further decline in 5 years even when the expected λ was 1.2. With all forms of uncertainty included, 41% of simulations projected a further decline over 5 years if the rat tracking rate were 10%. This proportion was reduced to 30% if initial population size was increased to 20 pairs. Our analysis therefore showed it was most likely that the robin population would grow if intensive rat control were reinstated, particularly if the population was supplemented, but there was substantial risk the population would continue to decline under such management.

Habitat selection and feeding ecology of the cheetah (Acinonyx jubatus) in thicket vegetation: is the cheetah a savanna specialist?

AbstractHabitat selection and feeding ecology of a reintroduced population of cheetahs Acinonyx jubatus were studied in a 16 000 ha game reserve in the Eastern Cape Province (South Africa). Seventy per cent of the reserve is characterized by very dense thicket vegetation (valley bushveld) and the remainder is open and savanna‐like. The results illustrated a strong effect of sex and group size on the behaviour of cheetahs. The coalition (three adult males) killed significantly larger animals (55% of kills weighed more than 65 kg) than single female cheetahs (less than 2% of kills weighed more than 65 kg). Female cheetahs showed temporal and spatial avoidance of lions by hunting at dawn and dusk and positioning their home ranges [95% utilization distribution (UDs)] significantly farther from the pride of lions than did the coalition. The coalition hunted earlier and later than female cheetahs, and 46% of their kills were made in darkness. In addition, their home range overlapped that of the lions and they showed neither temporal nor spatial avoidance of the lions. The rates of kleptoparasitism were lower and the kill retention times were longer than those reported elsewhere in Africa, and it is suggested that this is a consequence of the cover provided by the thicket vegetation and prey size. The home ranges (95% UDs) of female cheetahs incorporated more thicket vegetation than that of the coalition, indicating that the coalition is less susceptible to predation than single females. These data suggest that cheetahs possess greater behavioural flexibility than previously reported, that they can hunt successfully in thicket vegetation, sometimes in darkness, that they are not restricted to killing small to medium‐sized prey, and that they may not be savanna specialists.

Foraging and Feeding Ecology of the Gray Wolf (Canis lupus): Lessons from Yellowstone National Park, Wyoming, USA1–3

The foraging and feeding ecology of gray wolves is an essential component to understanding the role that top carnivores play in shaping the structure and function of terrestrial ecosystems. In Yellowstone National Park (YNP), predation studies on a highly visible, reintroduced population of wolves are increasing our understanding of this aspect of wolf ecology. Wolves in YNP feed primarily on elk, despite the presence of other ungulate species. Patterns of prey selection and kill rates in winter have varied seasonally each year from 1995 to 2004 and changed in recent years as the wolf population has become established. Wolves select elk based on their vulnerability as a result of age, sex, and season and therefore kill primarily calves, old cows, and bulls that have been weakened by winter. Summer scat analysis reveals an increased variety in diet compared with observed winter diets, including other ungulate species, rodents, and vegetation. Wolves in YNP hunt in packs and, upon a successful kill, share in the evisceration and consumption of highly nutritious organs first, followed by major muscle tissue, and eventually bone and hide. Wolves are adapted to a feast-or-famine foraging pattern, and YNP packs typically kill and consume an elk every 2-3 d. However, wolves in YNP have gone without fresh meat for several weeks by scavenging off old carcasses that consist mostly of bone and hide. As patterns of wolf density, prey density, weather, and vulnerability of prey change, in comparison with the conditions of the study period described here, we predict that there will also be significant changes in wolf predation patterns and feeding behavior.

Breeding Biology and Success of a Reintroduced Population of the Critically Endangered Puaiohi (Myadestes Palmeri)

AbstractThe ultimate success of reintroduction programs for endangered species depends on the ability of reintroduced animals to breed in the wild. We studied the nesting success and breeding biology of a reintroduced population of Puaiohi (Myadestes palmeri) on the island of Kaua'i, Hawaii. Thirty-four captive-bred Puaiohi were released into the Alaka'i Swamp in 1999-2001 and monitored using radiotelemetry. Ten females and two males paired with wild and other released birds, including one polygynous trio. From March to September, 31 nests were built. Mean clutch size was 2.0 eggs, daily nest survival was 0.97 ± 0.01 (mean ± SE) and overall nest success was 0.40 ± 0.02. We confirmed predation, most probably by rats (Rattus spp.), as the greatest cause of nest failure, occurring at 38% of active nests with known fates, and causing the death of two nesting adult females. Ground-based rodent control proved ineffective at protecting nest attempts. Successful nests fledged an average of 1.4 young each (n = 10), and 85% of fledglings survived at least two weeks. Importantly, breeding behavior and success were comparable to those of wild Puaiohi. This is the first record of breeding in the wild from captive-bred endangered Hawaiian passerines. The ability of captive-bred Puaiohi to survive and breed successfully in the wild bodes well for future releases of this and other endangered passerines, but high predation rates on nests and nesting females highlights the importance of maintaining and restoring safe habitat for recovery.Biología y Éxito Reproductivo de una Población Reintroducida de Myadestes palmeri, una Especie en Peligro Crítico

Dynamics of Hybridization and Introgression in Red Wolves and Coyotes

Hybridization and introgression are significant causes of endangerment in many taxa and are considered the greatest biological threats to the reintroduced population of red wolves (Canis rufus) in North Carolina (U.S.A.). Little is known, however, about these processes in red wolves and coyotes (C. latrans). We used individual-based simulations to examine the process of hybridization and introgression between these species. Under the range of circumstances we considered, red wolves in colonizing and established populations were quickly extirpated, persisted near the carrying capacity, or had intermediate outcomes. Sensitivity analyses suggested that the probabilities of quasi extinction and persistence of red wolves near the carrying capacity were most affected by the strength of two reproductive barriers: red wolf challenges and assortative mating between red wolves and coyotes. Because model parameters for these barriers may be difficult to estimate, we also sought to identify other predictors of red wolf population fate. The proportion of pure red wolves in the population was a strong predictor of the future probabilities of red wolf quasi extinction and persistence. Finally, we examined whether sterilization can be effective in minimizing introgression while allowing the reintroduced red wolfpopulation to grow. Our results suggest sterilization can be an effective short-term strategy to reduce the likelihood of extirpation in colonizing populations of red wolves. Whether red wolf numbers are increased by sterilization depends on the level of sterilization effort and the acting reproductive barriers. Our results provide an outline of the conditions likely required for successful reestablishment and long-term maintenance of populations of wild red wolves in the presence of coyotes. Our modeling approach may prove generally useful in providing insight into situations involving complex species interactions when data are few.

Captive breeding and the fitness of reintroduced species: a test of the responses to predators in a threatened amphibian

Summary Although captive breeding and reintroduction is a high‐profile management tool for many threatened species, it is unclear how long‐term captive breeding can influence fitness attributes such as natural defences to predators. Induced defences that have evolved in the Mallorcan midwife toad Alytes muletensis in response to introduced predators were compared in natural and reintroduced populations that had a common ancestry, and in short‐term and long‐term captive populations that differed in ancestry. Defences against predators were maintained in a reintroduced population derived from stock that had passed through three to eight generations of captive breeding prior to release into a predator‐free area. Heterozygosity did not differ between natural and reintroduced populations, but the reintroduced population displayed lower allelic richness. A comparison between populations maintained for different lengths of time in captivity revealed a significant reduction in one defensive trait in stock maintained for more than eight generations. Neutral genetic variation (i.e. heterozygosity and allelic richness) did not differ between the short‐term captive population and a natural population, but there was a significant loss of genetic variation in the long‐term captive population. Synthesis and applications. The results suggest that relatively high levels of heterozygosity and important fitness attributes can be maintained for a few generations in breeding programmes for threatened species despite small numbers of founders and the absence of natural selection. Nevertheless, both fitness and heterozygosity may eventually start to deteriorate in the long term, and this may have implications for reintroduction strategies.

Estimates of Elk Summer Range Nutritional Carrying Capacity Constrained by Probabilities of Habitat Selection

We used habitat-selection data from a reintroduced population of elk (Cervus elaphus) in northeastern Nevada, USA, to develop a resource-selection function to adjust nutritional carrying capacity estimates. Constrained estimates provide population levels that minimize overuse of key foraging communities. We estimated economic nutritional carrying capacity (INCC) for 236-kg lactating cow elk in autumn 1999 and 2000 to reflect expected animal performance under maintenance (2,550 kcal/kg DM) and good (2,750 kcal/kg DM) levels of standing digestible energy. We used our resource-selection function to redistribute INCC densities (RSFD) for aspen (Populus tremuloides), conifer, curl-leaf mountain mahogany (Cercocarpus ledifolius), sagebrush (Artemisia spp.)–herb, and snowbrush ceanothus (Ceanothus velutinus) cover types across the summer range and then adjusted original INCC estimates according to these RSFD when expected densities exceeded original INCC estimates. Maintenance performance INCC estimates were 2,533 cow elk (95% CI: 1,327–3,739) in 1999 and 1,655 (95% CI: 886–2,424) in 2000. Good performance INCC estimates were 2,264 cow elk (95% CI: 1,150–3,378) in 1999 and 1,100 (95% CI: 384–1,816) in 2000. The best habitat model provided evidence that forage availability and distance to water influenced habitat selection. Adjustments in INCC for 1999 and 2000 and at both performance levels corresponded to decreases of 18–35% in original INCC estimates. Decreases were attributed to more cow elk predicted by RSFD to be in aspen, conifer, and sagebrush–herb cover types than predicted by INCC. Each year, RSFD predicted that fewer elk would use mahogany and snowbrush cover types than original INCC models. The adjusted carrying capacity estimates provided population levels that should avoid appreciable alteration of aspen, conifer, and sagebrush–herb communities while ensuring nutritious resources during lean periods. Our paper provides a critical refinement for nutritional carrying capacity models through incorporating prediction of animal selection of nutritional resources.