Optimal release strategies for captive-bred animals in reintroduction programs: Experimental infections using the guppy as a model organism

Reintroduction of captive-bred individuals for supplementation or re-establishment of wild populations has become increasingly important to prevent the extinction of many endangered species. Despite the importance of reintroductions for conservation biology, few studies have empirically evaluated the potential impacts of reintroductions of naïve organisms on disease outbreaks in native wild populations. Here, we use a model organism, the guppy (Poecilia reticulata) and its ubiquitous parasite (Gyrodactylus turnbulli) to evaluate: (i) the most effective release procedure (i.e. en masse vs. gradual release) that minimises host mortality and parasite load, (ii) the effect of pre-exposure to the parasite on host susceptibility, and (iii) the potential advantage of removing the most susceptible individuals before release. We could not detect a statistically significant difference in host survival rates between release protocols and pre-exposure regime. However, the parasite population went extinct significantly more often when pre-exposed fish were released. Furthermore, the parasite load of individual guppies by the end of the reintroduction was significantly lower in treatments where fish had been pre-exposed to parasites than in treatments with naïve guppies. Additionally, pre-exposure of hosts provided important information about their level of resistance when reintroduced. These findings suggest that pre-exposure to native parasites could be beneficial for the survival rate of captive-bred animals when reintroduced in the wild. We discuss the practicalities of these potential release strategies.     

Widespread selective sweeps affecting microsatellites in Drosophila populations adapting to captivity: Implications for captive breeding programs

Many threatened species are being maintained in captivity to save them from extinction, often with the eventual aim of reintroduction. The objective of genetic management in captivity is to ‘freeze’ evolution i.e. to avoid genetic adaptation to captivity and to retain genetic diversity. Most current genetic management of threatened species addresses the latter, but does not explicitly address the former. The theory underlying current genetic management and its practical implementation assumes neutrality of loci. However, genetic adaptation in captive populations may cause non-neutral behavior at neutral loci due to selective sweeps (hitchhiking) caused by rapid allele frequency changes at linked fitness loci. We compared changes in microsatellite genetic diversity at eight non-coding loci with neutral predictions in 23 pedigreed captive populations of Drosophila melanogaster maintained with effective sizes of 25 (eight replicates), 50 (6), 100 (4), 250 (3) and 500 (2) for 48 generations. Loss of microsatellite heterozygosity was significantly faster (by 12%) than predicted by neutral theory, as assessed by regressing proportion of heterozygosity retained on pedigree inbreeding coefficients. Further, greater than neutral changes were observed for both variances in allele frequencies across replicates (by 25%), and for temporal changes in allele frequencies (by 33%). All eight microsatellite loci showed signals of selectively-driven changes. Rather than having their evolution ‘frozen’, captive populations are undergoing major genome-wide selective sweeps that affect not only fitness loci but linked neutral loci. Captive genetic management for threatened species destined for reintroduction requires modification to explicitly minimize genetic adaptation to captivity.     

Responses of small rodents to habitat restoration and management for the imperiled Florida Scrub-Jay

Debate about the relative merits of single-species management versus more comprehensive approaches has intensified in recent years. In east-central Florida, USA, land managers use prescribed burns and mechanical cutting to manage and restore scrub habitat to benefit the imperiled Florida Scrub-Jay (Aphelocoma coerulescens). However, these land-management techniques may affect non-target taxa, especially the threatened southeastern beach mouse (Peromyscus polionotus niveiventris). We evaluated the collateral effects of single-species land management by trapping P. p. niveiventris and other small rodents in eighteen land-management compartments at Cape Canaveral Air Force Station, Florida during 2004–2005. Compartments were managed using either prescribed burns (N = 5), mechanical cutting (N = 6), checkerboarding (cut and uncut lanes alternating and overlapping, followed by a prescribed burn, N = 4) or left unburned and uncut for >50 year (N = 3). P. p. niveiventris was significantly more abundant in compartments managed with prescribed burns (mean ± SE: 4.2 ± 0.7 individuals/transect) than those managed with cutting alone (1.0 ± 0.3) or not managed for >50 y (0.2 ± 0.1 individuals/transect). In contrast, the cotton mouse (Peromyscus gossypinus) tended to be more abundant in compartments managed with mechanical cutting alone (2.6 ± 0.4 individuals/transect) compared to the other three management strategies (prescribed burns; 1.5 ± 0.4; checkerboarding, 1.1 ± 0.3; not managed, 1.6 ± 0.4 individuals/transect) but these differences were not statistically significant. Abundances of P. p. niveiventris and Florida Scrub-Jay breeding groups were positively correlated (r = 0.655), suggesting that both listed species benefit from similar management techniques. Thus, the mosaic of burned and cut patches used to improve habitat for the Florida Scrub-Jay also benefits an endemic, non-target species. Single-species management may benefit multiple species when restoration improves their shared habitat, which in this case is an endangered, fire-dependent ecosystem: Florida scrub.     

Wild rabbit restocking for predator conservation in Spain

The decline of rabbit (Oryctolagus cuniculus) populations in Mediterranean Spain has been shown to be one of the main threats to rabbit-specialist predators such as the Iberian lynx (Lynx pardina) and the Spanish imperial eagle (Aquila adalberti), two species which are in serious danger of extinction. Consequently, corrective measures such as increasing rabbit populations by restocking have been carried out to help the recovery of predator populations. In order to determine the general applicability of rabbit restocking for predator conservation, we performed three experimental restockings and evaluated their success in relation to season, habitat quality and the number of animals introduced. Rabbits were released either in large or small numbers in all four seasons of the year, and in habitat types defined as `poor' or `rich' according to the food availability for rabbits. For each restocking we evaluated rabbit survival, degree of residency and expected population increase. As a rule, the highest restocking success occurred whenever smaller number of rabbits were released in the richest quality habitat. Restocking during the breeding season was less successful than in other seasons. Problems concerning intraspecific competition, reproductive failure and diseases are discussed.     

Road crossing structures for amphibians and reptiles: Informing design through behavioral analysis

Road traffic causes significant amphibian and reptile mortality, which could be mitigated through the installation of road crossing structures that facilitate safe passage, but only if reptiles and amphibians are willing to use them. Through a series of behavioral choice experiments with frogs and turtles, we examined how aperture diameter, substrate type, length, and light permeability influenced individuals’ preferences for specific attributes of crossing structures, and how individuals responded to various heights of barrier fences. Snapping turtles (Chelydra serpentina), green frogs (Rana clamitans), and leopard frogs (Rana pipiens) preferred larger diameter tunnels (>0.5 m) whereas painted turtles (Chrysemys picta) preferred tunnels of intermediate (0.5-0.6 m) diameter. Green frogs preferred soil- and gravel-lined tunnels to concrete- and PVC-lined tunnels. Painted turtles showed non-random choice of different lengths of tunnel, possibly indicating some avoidance of the longest tunnel (9.1 m); although no species preferred to exit via the longest tunnels (9.1 m), members of all four species used such tunnels. Green frogs preferred tunnels with the greatest light permeability. Fences 0.6 m in height were effective barriers to green frogs, leopard frogs, and snapping turtles, whereas 0.3 m fences excluded painted turtles. We conclude that tunnels > 0.5 m in diameter lined with soil or gravel and accompanied by 0.6-0.9 m high guide fencing would best facilitate road crossing for these and likely other frog and turtle species.     

Conspecific attraction in loggerhead shrikes: implications for habitat conservation and reintroduction

The loggerhead shrike, Lanius ludovicianus, is a declining songbird that forms breeding aggregations. Despite such reports from several populations, only one statistical analysis of loggerhead shrike territory distribution has been published to date. I use a spatio-temporal simulation technique to test for deviations from randomness in the spatial distribution of point data that takes into account date of nest establishment. I apply this model to data on the distribution of shrike nests in Comanche County, Oklahoma, USA, collected over the 1998 and 1999 breeding seasons. When the data are considered without regard to date of nest-establishment, the results are equivocal; nests are significantly aggregated in 1999, but not 1998. However, when order of nest establishment is taken into account, later nests are significantly more likely to be closer than expected to conspecifics in both years. This is true even when the distribution of simple resources, such as suitable nest-trees, is included in the model. These results are consistent with the hypothesis that loggerhead shrikes ‘prospect’ for suitable habitat using the distribution of breeding conspecifics. This aspect of loggerhead shrike breeding ecology should be considered for both habitat conservation and captive breeding and reintroduction programs for this species.     

Removal of introduced predators, but not artificial refuge supplementation, increases skink survival in coastal duneland

Exotic predators can have detrimental impacts on indigenous fauna. Lethal predator control is commonly used to reduce predator impacts, but is not always feasible, effective or ethical. A promising non-lethal alternative is refuge supplementation for prey. We conducted a Before-After Control-Impact (BACI) experiment over 3 years to determine the relative effects of predator removal (by exclosure fencing) and artificial refuge supplementation on survival of McCann’s skink (Oligosoma maccanni) in duneland on Kaitorete Spit (South Island, New Zealand). Skink populations on 0.0625 ha-grids were randomly assigned to four treatment groups, each replicated four times: (a) predator exclosure only; (b) artificial retreats only; (c) exclosure + artificial retreats, and (d) control (no exclosure or artificial retreats), and monitored annually by pitfall trapping. Capture-recapture analysis was used to estimate the difference in annual survival probability between pre- and post-treatment periods. On average, survival increased only at grids that received the exclosure-only treatment (effect size of 0.03 (0.017-0.043; unconditional 95% CI)). Reduction in predator abundance (by lethal predator control or predator exclusion), but not artificial refuge supplementation, is predicted to benefit McCann’s skink. Our findings add to other studies highlighting the detrimental impacts of exotic predators on indigenous prey and calls for improved means of reducing predator impacts.     

Non-commercial collection of spur-thighed tortoises (Testudo graeca graeca): a cultural problem in southeast Spain

Collecting tortoises for the pet trade is one of the factors threatening species of Testudo in the Mediterranean area. The collection of Testudo graeca graeca for pets is described in southeast Spain, where the main European population of this subspecies coincides with an area where keeping tortoises in captivity is a long-established custom. This present paper, based on inquiries made to children, reveals that this practice continues to be a common activity, and estimates a captive population in the order of tens of thousand of tortoises. Tortoises are collected as a result of chance encounters with wild animals by local inhabitants, and without any commercial objectives. The captive breeding and the release of tortoises without any institutional control is also common. These activities could be an important threat for the species. Implications for conservation are discussed and a critical review of the conservation strategies developed in relation to this threat (trade control and re-introduction programmes) are presented. We suggest that environmental education programmes are necessary to reduce casual collection and to change the social perception of tortoises as pets.     

Use of monitoring data and population viability analysis to inform reintroduction decisions: Peregrine falcons in the Midwestern United States

The peregrine falcon (Falco peregrinus anatum) has not yet recolonized natural cliff sites in Illinois and much of the lower Midwestern US, and remains restricted to urban areas. We constructed a landscape-linked population viability analysis using RAMAS/GIS software to compare possible reintroduction strategies for the species. Habitat-specific (i.e. cliff and urban) demographic parameters such as survival, fecundity, and dispersal rates were derived from the Midwest Peregrine Society Database for peregrines in the central Mississippi River region during 1982-2006. We simulated a base scenario of no reintroduction and 18 models of reintroduction with varying cohort sizes, supplementation schedules, and number of reintroduction sites, and used the Lake Superior population to test our model. Our analysis indicated that even without reintroductions in Illinois, the peregrine population in the lower Midwestern region is slowly increasing and is not likely to go extinct. Recolonization of cliff sites in southern Illinois likely will occur via dispersal from urban populations, however further research on dispersal rates between urban areas and cliffs is needed. Analysis indicated that the most cost-effective reintroduction strategy would be priced at approximately $280,000 and would result in only two additional breeding pairs compared to the no-action scenario. Thus, funds would be more effectively used in other management efforts such as habitat preservation. This study provides an example of how post-release monitoring can be used to inform future reintroduction plans.     

Impact of grassland farming intensification on the breeding ecology of an indicator insectivorous passerine, the Whinchat Saxicola rubetra: Lessons for overall Alpine meadowland management

The decline of insectivorous farmland passerines has been attributed mostly to global decrease in arthropod availability, as a result of intensification of agricultural practices. The diminution of the Alpine Whinchat, once a widespread insectivorous passerine, has been ascribed to nest losses due to earlier and more frequent mowings. However, potential conjugated effects of deteriorated arthropod food availability had yet to be investigated. We compared food supply and nestling diet in intensively vs. traditionally managed grassland. Abundance and diversity of arthropods were much lower in intensive areas, where small-sized invertebrates, which do not enter nestling diet, were also predominant. Parents breeding in intensive habitats fed less biomass to nestlings than adults from traditional habitats. Nestling diet was less diverse and dominated by less profitable prey items in intensive than in traditional habitats. Feeding rate did not differ between the two habitats, but foraging distances from nest tended to be greater in intensive farmland. There were no significant differences in clutch sizes and hatching success with respect to management intensity, but fledging success was higher in traditional habitats. The recent intensification of farming practices has led to a decrease in the availability of grassland invertebrates, and of important Whinchat nestling food in particular, affecting parents’ foraging efficiency and reproductive success. Conservation actions must not only reduce nest losses by postponing mowing, but should also promote grassland farming that is less detrimental to invertebrates. Dominant at the study site, organic grassland farming does seemingly not provide sufficient conditions for Alpine Whinchats.     

Grassland nature reserves for breeding wading birds in England and the implications for the ESA agri-environment scheme

The two principal mechanisms available to conserve breeding wading birds on lowland wet grassland in England are nature reserves and agri-environment schemes, particularly the Environmentally Sensitive Area (ESA) scheme. ESAs offer payments to landowners in return for maintaining (‘low tiers’) or enhancing (‘high tiers’) the landscape, biodiversity and historic value of the land. Lowland wet grassland nature reserves managed by the Royal Society for the Protection of Birds (RSPB) have been successful at conserving breeding lapwings and redshank but habitat management usually only results in short-term increases in numbers of breeding snipe. Within ESAs, populations of breeding wading birds fare better on land managed under high tiers than on land managed under low tiers. Land managed under high tiers also supports more pairs of breeding wading birds per £ of ESA grant received than land managed under low tiers. Means of increasing the cost-effectiveness of the ESA scheme in conserving breeding wading birds are discussed in the light of these results.     

Extirpation and reintroduction of fishers (Martes pennanti) in Oregon: implications for their conservation in the Pacific states

Prior to extensive European settlement, the fisher (Martes pennanti) occupied most coniferous forest habitats in Washington, Oregon, and California. Human activities since that time have resulted in the apparent extirpation of fishers throughout much of their historical range in the Pacific states. Fisher extirpations in California and Washington have been documented previously, but no comprehensive assessments of the distribution of fishers in Oregon, the history of their translocation into Oregon, or the conservation of fishers in the Pacific states have been conducted. Our objectives are to (1) review historical information on potential causes for fisher population losses in Oregon, (2) document the history of their translocation into Oregon, (3) describe the distribution of fishers in Oregon relative to those translocations and determine if any were successful, and (4) discuss the implications of our findings for the conservation of fishers in the Pacific states. Our results show that extant populations of fishers in Oregon are restricted to two disjunct and genetically isolated populations in the southwestern portion of the state: one in the southern Cascade Range and one in the northern Siskiyou Mountains. In addition, historical changes in the distribution of fisher occurrence records in Oregon and geographic variation in the genetic composition and size of fishers occurring in southwestern Oregon, show that the population in the southern Cascade Range is reintroduced and is descended from fishers that were translocated to Oregon from British Columbia and Minnesota. The loss of fisher populations from central and northern Oregon and throughout Washington has resulted in the isolation of extant populations in Oregon by >650 km from those occurring in southern British Columbia. Our results demonstrate that the historical continuity in fisher distribution that once provided for genetic interchange among fisher populations in the Pacific states no longer exists.     

Population baseline data for monitoring genetic diversity loss for 2010: A case study for Brassica species in the UK

The Convention on Biological Diversity and the subsequent International Treaty on Plant Genetic Resources for Food and Agriculture have proved a watershed in plant genetic resources (PGR) conservation and consequent initiatives have set various PGR conservation targets to be met by 2010. The aim of our paper is to develop ideas and issues concerning the monitoring of natural genetic resources: particularly in terms of developing a baseline from which to measure levels of genetic diversity. Three species of Brassica (B. nigra, B. oleracea, B. rapa) found wild in the UK were assessed for levels of genetic diversity using AFLP. The relationship between genetic distribution and ecogeographic distribution was considered for each species to determine patterns that may be useful in formulating conservation strategies. Genetic distance between populations of B. nigra and B. rapa were correlated to geographic distance. Levels of genetic polymorphism in B. oleracea were correlated to soil pH while in B. rapa they were correlated to soil coarseness. In terms of PGR conservation these findings may suggest an emphasis toward in situ conservation of a selection of disparate populations would be appropriate where possible as such adaptations may be lost in ex situ collections.     

A nine-year study of successful breeding in a Bonelli’s eagle population in southeast Spain: a basis for conservation

We analyse the factors influencing breeding success in a healthy population of Bonelli’s eagle (Hieraaetus fasciatus) from south-east Spain, a raptor that has suffered a serious decline in Europe. Between 18 and 33 pairs were annually monitored during the period 1994-2002. Several factors that may affect four breeding parameters were studied, namely human presence, vegetation, relief, climatic factors, intra- and inter-specific relationships, diet, prey abundance, nest building, adult mortality and age of reproduction. A consistently high breeding success was registered during the study period (productivity=1.43, SD=0.11), which was probably the result of high adult survival, adequate prey availability and mild weather conditions. However, a certain vulnerability to the presence of golden eagles (Aquila chrysaetos) and to human disturbance was observed. One interesting result was the reduced survival of young chicks on north-facing cliffs owing to colder conditions, which may partially explain the decline of the Bonelli’s eagle populations along its European distribution limits. We discuss the role of this healthy subpopulation in an Iberian metapopulation context, and propose that the potential interference of golden eagles should be taken into account when designing management strategies for Bonelli’s eagles. Finally, we pinpoint some conservation priorities and the importance of reducing the main causes of adult mortality (i.e. shooting and electrocution) to assure successful reproduction and survival of this species.     

Functional conservation units for the endangered Alcon Blue butterfly Maculinea alcon in Belgium (Lepidoptera: Lycaenidae)

To organize and prioritise species-specific conservation efforts, we delineate `functional conservation units' for the threatened Alcon Blue butterfly Maculinea alcon in Belgium. We used detailed distribution data on the butterfly, its host plant and its habitat, present-day population sizes and its mobility and colonization capacity to determine functional conservation units (FCUs) on different spatial scales: FCU-1, i.e., the 12 presently occupied habitat patches plus the area within a range of 500 m surrounding them (the maximum local movement distance, based on mark-release-recapture data), FCU-2, i.e., the areas within a range of 2 km around the occupied habitat patches (the maximum observed colonization capacity) and FCU-3, i.e., potential re-introduction sites (sites where M. alcon went extinct recently). We suggest different management and planning measures for each type of functional conservation unit and discuss translocation and re-introduction as `intensive care' conservation measures for this threatened and sedentary species.     

An unseen foe in arthropod conservation efforts: The case of Wolbachia infections in the Karner blue butterfly

Infection by endosymbiotic bacteria is an underappreciated threat to endangered arthropods with serious implications for captive management programs. We examined the nature of Wolbachia infection in the North American endangered Karner blue butterfly, Lycaeides melissa samuelis, as a case study. Screening for Wolbachia across the range of the species confirmed widespread infection in the western half of the Karner blue’s range. Multilocus sequence typing using six genes confirmed that the infection in the western populations is attributable to a single strain of Wolbachia. This strain was also detected in the closely related Melissa blue butterfly, L. m. melissa, the presumed source of the infection. The infection in the Karner blue butterfly was perfectly correlated with the presence of a foreign mitochondrial DNA variant present in the Melissa blue butterfly, consistent with the hypothesis that the mitochondrial introgression was driven by the spread of Wolbachia. A single individual out of 71 screened from the eastern portion of the range of the Karner blue butterfly was also infected, however this infection was attributable to a different strain. Simulation models of the demographic effects of the spread of Wolbachia infection to uninfected populations and metapopulations suggest that such an infection might further reduce already small population sizes and substantially increase the probability of population extirpation. We discuss threats to other endangered arthropods in the light of this case study and make recommendations for minimizing the impact of endosymbiont infections in conservation plans, especially those including captive propagation and augmentation of endangered arthropod populations.     

An integrated comparison of captive-bred and wild Atlantic salmon (Salmo salar): Implications for supportive breeding programs

Supportive breeding is a strategy consisting in maintaining a pool of locally-adapted wild genitors in captivity whose offspring are released in the wild at an early developmental stage. In this study, we tested the utility of this strategy in preventing phenotypic and genetic divergences between captive-bred and wild animals that could be detrimental for wild populations. Combining microsatellite analyses, morphological measurements and behavioural trials in the laboratory, we compared the progeny of Atlantic salmon (Salmo salar) born in captivity with individuals born in the wild. At all these levels, we found significant differences between the progeny of the two groups. Specifically, allelic frequencies significantly differed between groups, with captive-bred fish tending to be less variable with lower heterozygosity and allelic richness values. The shape of wild-born fish was also different from that of the captive-group, particularly in the depth of the head and the length of the pectoral fins. Finally, captive-bred individuals were, on average, more aggressive than wild-born fish. We demonstrated that this difference was strongly dependent upon the environment as captive-bred fish were more aggressive only when together with their wild conspecifics or with an exotic competitor, the rainbow trout (Oncorhynchus mykiss). Overall, our results showed that both phenotypic and genetic changes can arise even if genitors share a common brood-stock and after only a few months of rearing in a controlled environment. We conclude that the progeny produced in such supportive breeding programs does not meet the criteria necessary to ensure preserving the genetic and ecological integrity of wild populations.     

Dispersal of breeding, adult male Phocarctos hookeri: Implications for disease transmission, population management and species recovery

Dispersal impacts on a range of population parameters making it a key piece of information in species conservation. Despite its importance, dispersal is poorly characterized for many species: pinnipeds are no exception. Understanding dispersal patterns of the New Zealand sea lion Phocarctos hookeri is crucial in the conservation management of the species as its recovery to a non-threatened status hinges on range recolonisation. In this study, we examined the movements of breeding adult male New Zealand sea lions within and following the breeding season of the 2002/03 austral summer using a novel multi colony approach. Based on resightings of 202 individually identifiable adult males, we found (1) a previously unappreciated, high level of dispersal by adult territorial males between breeding colonies during the pupping period and (2) that breeding males disperse to the extremes of the species’ range at the end of female oestrous. Our findings are contrary to the current paradigm of otariid breeding behaviour, which is believed to consist of prolonged, uninterrupted male territoriality based on intense male-male competition and sustained fasting. Adult male dispersal between colonies and across the species range has important implications for adult males as vectors of disease in three recent epizootics, species management and species recovery via recolonisation as males are apparently remaining part of a localized, vulnerable breeding population.     

Dynamics of early wolf and cougar eradication efforts in Montana: implications for conservation

Bounty records from Montana (1902-1930) were used to better understand spatial and temporal response of wolves (Canis lupus) and cougars (Puma concolor) to an eradication program. Number of payments for wolves declined from a high of 4116 in 1903 to 0 by 1928. Numbers of cougar pelts fluctuated, but generally declined from 177 in 1908 to 2 in 1930. An inverse spatial relationship existed between density of payments for wolves and cougars. Payments for wolves were greatest in the Prairie ecoregion, while payments for cougars were greatest in the Montane. The ratio of pup to adult wolves also was greatest in the Prairie ecoregion and least in the montane. If distribution and frequency of bounty payments were a reflection of the distribution and abundance of wolves, populations were highest and most productive in areas where they currently do not occur.     

Amphibians in a human-dominated landscape: the community structure is related to habitat features and isolation

We studied amphibian populations in a human-dominated landscape, in Northern Italy, to evaluate the effects of patch quality and isolation on each species distribution and community structure. We used logistic and linear multiple regression to relate amphibian presence during the breeding season in 84 wetlands to wetland features and isolation. Jackknife procedure was used to evaluate predictive capability of the models. Again, we tested the response of each species to habitat features related to the richest communities. Amphibian presence depends strongly on habitat quality and isolation: the richest communities live in fish-free, sunny wetlands near to occupied wetlands. The negative effects of isolation do not seem to be biased by spatial autocorrelation of habitat features. The system shows strong nestedness: amphibian persistence depends on the contemporary effects of species adaptability and mobility. The commonest species, the pool frog (Rana synklepton esculenta) and the Italian tree frog (Hyla intermedia), are able to move through the matrix using canals and hedgerows, and can maintain metapopulations across the landscape; the rarest species (newts and toads) are more sensitive to habitat alteration, and they are strongly affected by isolation effects. If human exploitation of the landscape continues, only few species, mobile and opportunistic, will persist in this landscape.