Do native species limit survival of reintroduced Atlantic salmon in historic rearing streams?

Reintroduction of extirpated populations creates a unique context that can exacerbate the effects of interactions among species. Thus, reintroduced populations may be particularly vulnerable to predators and competitors, including native species with which they historically coexisted. In this study, we evaluated the effect of native fishes on survival of reintroduced Atlantic salmon (Salmo salar) in the Connecticut River basin, where the native salmon population is extinct. Juvenile salmon are stocked annually in many Connecticut River tributaries. We sampled salmon reintroduction sites across tributaries with different fish communities to determine whether native fish reduce the success of salmon reintroductions (N = 19 site-years). Increased density of slimy sculpin (Cottus cognatus), a native generalist predator, was associated with reduced recruitment of reintroduced salmon. Salmon first-summer survival declined with increased sculpin density across sites, and low first-summer survival led to reduced densities of overyearling salmon the subsequent year. Hierarchical partitioning analysis showed that the negative relationship between sculpin and salmon was independent of potentially confounding variation in other fish community or habitat characteristics. Negative effects of native, historically-sympatric species, particularly generalist predators, can impede restoration of extirpated populations.     

Captive breeding promotes aggression in an endangered Mexican fish

We compared the behaviour of wild and captive-bred butterfly splitfins (Ameca splendens), an endangered freshwater fish, to investigate whether captive breeding results in the behavioural divergence of wild and captive individuals. In a first experiment, we examined whether the captive environment allows for the similar expression of behaviours observed in wild fish. The foraging, courtship and aggressive behaviour of fish in their natural habitat (in Mexico) was compared with that of their counterparts that have been bred at London Zoo, UK, for 40 years. These in situ observations revealed that wild fish were preoccupied with searching for food whereas captive fish engaged more in aggressive interactions. In a subsequent laboratory experiment we compared the behaviour of wild-caught and captive-bred fish under standard conditions in two novel habitats: structured (enriched) and unstructured (bare) aquaria. Overall, captive-bred butterfly splitfins displayed higher levels of aggression than wild-caught fish. The relationship between aggression and habitat structure was influenced by density; captive-bred males were more aggressive when observed in structured habitats than unstructured ones, but only when they were stocked at a high density. We also found an effect of tank structure on foraging behaviour, with individuals spending more time foraging in unstructured tanks than structured tanks. There was no effect of captive breeding or habitat structure on courtship behaviour.Our findings suggest that captive environments can promote the development of aggressive behaviour which may affect the suitability of captive-bred fishes for reintroduction into the wild.     

Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa

The emergence of the infectious disease chytridiomycosis is a major factor responsible for amphibian extinctions in pristine habitats. However, some populations coexist with Batrachochytrium dendrobatidis (Bd), the agent of chytridiomycosis, and others go extinct when Bd arrives. Variation of pathogen severity among populations may be explained by differences of antimicrobial skin peptides and anti-Bd skin bacteria. Previous work showed that a population of the frog Rana sierrae had a high proportion of individuals with at least one species of cultured anti-Bd skin bacteria and was coexisting with Bd for more than 6 years. A population of the closely related sister species Rana muscosa had a significantly lower proportion of individuals with anti-Bd bacteria, and the following year, it went extinct due to Bd. We extended previous work to include another sampling of the R. sierrae population coexisting with Bd and found that, although the anti-Bd bacterial community somewhat differed, both populations had a high proportion of individuals with antifungal bacteria. We also included a population of R. muscosa that was naïve of Bd and predicted to go extinct once Bd emerged since that was the fate of neighboring populations. However, the naïve R. muscosa population had a high proportion of antifungal bacteria, which suggested that the population might survive if Bd emerged. Two years later, the population was surviving with Bd endemic. Variation in the proportion of individuals with anti-Bd skin bacteria appears to explain why some populations persist when Bd emerges in a population.     

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.     

Successful reintroductions of the endangered long-lived Sargent’s cherry palm, Pseudophoenix sargentii, in the Florida Keys

The 1991-1994 reintroductions of Florida endangered Pseudophoenix sargentii to 13 Florida Keys sites represent a rare example of a successful multi-agency long-term effort to conserve a long-lived palm. To assess reintroduction success, we compared population demographics with and without reintroduced plants and conducted population viability analyses. Since 1991, the wild population has increased 6.4-fold. Survival from 2000-2004 was 94%, growth was positive (λ = 1.013), and there was no predicted extinction risk. Recent wild population growth is attributed to good seedling recruitment and removing the greatest threats. After 14 years, reintroductions had 43% survival, increased total plants in the wild by 27%, and expanded the species’ distribution. Reintroduced plants had faster maturation rates, improved population age structure, and enhanced population growth (λ = 1.032). Success varied with transplant year, location, microsite, and original transplant size. Failures in 1991 and at some historic sites emphasize the need for a multi-year, multi-site approach to reintroductions to buffer against stochastic losses. Rockland hammocks and the tops of coastal berms had greatest plant growth and survival. Large transplants had the greatest survival. Because no reintroduced plants are reproductive, transitions between stages are extremely slow, and plants may require >30 years to mature, continued institutional dedication to long-term monitoring will be required to assess whether the populations are self-sustaining. Horticultural expertise and ex situ collections complimented support of land managing agencies for the species’ preservation. These first rare plant reintroductions to Florida State Parks opened avenues for more plant conservation efforts and public interpretation.     

An experimental study on the effects of an introduced parasite in Darwin’s finches

It is widely recognised that the main threats to the biota of the Galápagos Islands stem from newly introduced diseases, plants and animals. Introduced organisms may lead to the rapid extinction of naïve insular populations. Previous research on Galápagos showed that the parasitic larvae of the fly Philornis downsi occurred in virtually all nests of land bird species examined, with high nestling mortality (27% of all broods) in relation to high parasite infestation. In this study, we used an experimental approach to measure the fitness impacts of the fly larvae in two species of Darwin’s finch (Geospizinae). We created parasite-reduced nests by applying a 1% pyrethrin solution to the nest during the early nesting phase, and measured: (1) nestling growth, (2) nestling haemoglobin (Hb) concentration and (3) fledging success. A single insecticide treatment was sufficient to reduce parasite intensity to nearly zero, and revealed reduced mass gain and reduced fledging success in parasitized nests compared to parasite-reduced nests. This is the first experimental study of fitness impacts by Philornis on its host species. The results are discussed in the light of short-term protection measures for nests of rare finch species in the Galápagos archipelago.     

Can small, isolated primate populations be effectively reinforced through the release of individuals from a captive population?

Since November 1997 the Madagascar Fauna Group (MFG) has released 13 captive-bred black and white ruffed lemurs (Varecia variegata variegata) into the Betampona reserve in eastern Madagascar. Five of the thirteen are currently surviving, including one male who has integrated into a wild group. Five of the released lemurs fell victim to predation by fossa (Cryptoprocta ferox), one died of malnutrition, one disappeared from the reserve and one was withdrawn from the release programme. Ten of the released lemurs survived for more than one year post release, although all required varying levels of supplementary feeding. One pair bred twice—the first time the infants did not survive, but on the second occasion triplets were successfully raised beyond weaning. One of the triplets (male) is still surviving. One male has integrated into a wild group and sired a single infant in 2002 and a female released in 2001 gave birth to twins sired by a wild male also in 2002. The release programme has thus achieved a major objective of reinforcing the existing wild population. To date there is no significant difference in survival rates between animals born and raised in free-ranging environments and those raised in cages, between animals greater than or less than 5 years old at time of release, or between males and females.     

The success of a soft-release reintroduction of the flightless Aldabra rail (Dryolimnas [cuvieri] aldabranus) on Aldabra Atoll, Seychelles

Humans and introduced mammalian predators have caused local extinctions and range reductions in the rallid genus Dryolimnas (endemic to western Indian Ocean islands); today two subspecies survive, one on Madagascar and one on three islands (ca. 8000 birds) of Aldabra Atoll. Domestic cats (Felis catus) still occur on Aldabra and their presence poses a significant potential threat to the rails. Reintroduction to cat-free islands would significantly improve their conservation status. In 1999, 20 rails were captured and brought to now cat-free Picard Island (the third largest island of Aldabra Atoll). Two rails died in captivity but all 18 remaining birds were released and survived beyond the first breeding season. Eight pairs had bonded and bred successfully within 2 months of release, producing a minimum of 13 chicks. Eleven monitored pairs produced 20 chicks in 2000/2001, with 1-year-old birds breeding successfully. Average chick production was significantly higher in the reintroduced population than in the source population in both breeding seasons. The reintroduced population at the end of the 2001 breeding season was at least 51, an increase of 283% in 18 months. Around 20 pairs are expected to attempt breeding on Picard in the third season after reintroduction, with excellent prospects for continued, exponential population growth in the medium-term. The soft-release reintroduction protocol allowed monitoring of individual birds' health before release into the wild. This is believed to have played a crucial role in the success of the reintroduction by allowing individuals to acclimatise and providing additional energetic reserves for the period between release and self-sufficiency. A soft-release is recommended as the conservative and precautionary method of choice for avian reintroductions and translocations.     

Keeping fit on the ark: assessing the suitability of captive-bred animals for release

Reintroduction programs are widespread but have low success rates, particularly when captive-bred animals are used. There are high financial costs, and important ethical concerns about animal welfare. We have explored the concept of utilizing a behavioural approach to assess the suitability of captive-bred animals for release. We compared the behaviours of wild-bred and captive-bred animals in identical novel environments, using bank voles, Clethrionomys glareolus, as a model. The wild animals provided an adaptive baseline against which the behaviour of captive-bred individuals was compared. Although captive-bred voles displayed some wild-type behaviours - nest building and burrowing - despite lacking previous opportunities to do so, they were unable to utilize a key food resource and were less dominant. We suggest that a similar approach could be applied to species of conservation concern in order to rank available animals in terms of likely suitability for release. It could also help to identify characteristics that appear deficient in captive-bred animals, or to evaluate the impact of interventions such as environmental enrichment.     

High genetic diversity and heterogeneous parasite load in the earthworm Lumbricus terrestris on a German meadow

In parasite-host dynamics, parasites exert frequency-dependent selection on their hosts by favouring rare alleles that may confer resistance against infection. Therefore host populations that suffer strong parasite stress should maintain higher levels of genetic variability. We studied the Lumbricus terrestris-Monocystis sp. host-parasite system at a microgeographical scale. Using three polymorphic microsatellite loci on one large earthworm population sampled at 26 different sites (281 genotypes), we tested the relationship between parasite load and genetic variation in natural samples of the common earthworm L. terrestris. Our analysis yielded the following: (1) parasite load varied significantly across sites in this population; (2) there was no consistent evidence for heterozygote deficiency (observed heterozygosities ranged between 0.74 and 0.87), indicating a low level of inbreeding; (3) there was no significant genetic structuring among sample sites; (4) we could not identify a significant association between parasite load and population genetic diversity; (5) there was considerable population differentiation (15.17%) between our German samples and a Canadian L. terrestris reference population. Our study provides insight into the population genetics of one of the most economically important soil organisms on a microgeographic scale.     

Factors associated with survival of reintroduced riparian brush rabbits in California

The riparian brush rabbit (Sylvilagus bachmani riparius) is an endangered species found in dense, brushy habitat in the California’s Central Valley. We implemented a reintroduction program to bolster populations at a Federal Wildlife Refuge and to assess factors influencing mortality and subsequent survival of released individuals. Between July 2002 and July 2005, we reintroduced 325 captive-bred individuals to unoccupied habitat within their historic range using a soft-release strategy and monitored their subsequent survival with radiotelemetry. Longer time in soft-release pens resulted in increased monthly survival. Rabbits were most susceptible to post-release mortality during the first 4 weeks following reintroduction and both body mass and length of time in the soft-release enclosure influenced this relationship. When we controlled for release mortality during this acclimation period, subsequent monthly survival probabilities were most strongly influenced by release year (year 1 vs. years 2 and 3) and by a catastrophic flooding event; length of time in the soft-release enclosure remained an important variable in longer-term survival. Cause of mortality was unknown for the majority of deaths (61.9%), but predation (including presumptive predation) was the greatest known cause of death in translocated rabbits (26.4%). Reintroduction programs should employ an adaptive management approach with ongoing monitoring of target animals and concurrent analysis to allow managers to adjust methods as conditions dictate.     

Effects of the introduced parasite Philornis downsi on nestling growth and mortality in the medium ground finch (Geospiza fortis)

Invasive species have the potential to detrimentally affect native ecosystems by out competing or directly preying upon native organisms, and have been implicated in the extinction of endemic populations. One potentially devastating introduced species in the Galápagos Islands is the parasitic fly Philornis downsi. As larvae, P. downsi parasitize nestling birds and have been associated with high nestling mortality and reduced growth rates. Here I document nestling growth and mortality in a bimodal population of the medium ground finch, Geospiza fortis. Observations were conducted over three years, and under variable ecological conditions. Annual parasite prevalence in nests ranged from 64% to 98%, and nestling mortality in nests with parasites ranged from 16% to 37%. Parasite load and parasite load per nestling follow a skewed distribution with many nests having relatively few parasites, and few nest having many. Parasite load, however, was not correlated with onset of breeding, clutch size, the number of nestlings, nestling survival or fledgling success. Parasite load per nestling, on the other hand, was correlated with clutch initiation date and the proportion of nestlings that died in parasitized nests. Neither nestling size nor growth rate differed between parasitized and unparasitized nests. In addition, male and female beak morphology was not correlated with parasite load, breeding variables or nestling survival. Thus, while overall mortality due to parasitism is high, ecological conditions and possible host defenses may potentially counter some of the detrimental affects of P. downsi on nestling size and growth. These results taken together suggest that parasitism of P. downsi larvae on nestling G. fortis has the potential to lead to large population declines.     

How successful are plant species reintroductions?

Reintroduction of native species has become increasingly important in conservation worldwide for recovery of rare species and restoration purposes. However, few studies have reported the outcome of reintroduction efforts in plant species. Using data from the literature combined with a questionnaire survey, this paper analyses 249 plant species reintroductions worldwide by assessing the methods used and the results obtained from these reintroduction experiments. The objectives were: (1) to examine how successful plant species reintroductions have been so far in establishing or significantly augmenting viable, self-sustaining populations in nature; (2) to determine the conditions under which we might expect plant species reintroductions to be most successful; (3) to make the results of this survey available for future plant reintroduction trials. Results indicate that survival, flowering and fruiting rates of reintroduced plants are generally quite low (on average 52%, 19% and 16%, respectively). Furthermore, our results show a success rate decline in individual experiments with time. Survival rates reported in the literature are also much higher (78% on average) than those mentioned by survey participants (33% on average). We identified various parameters that positively influence plant reintroduction outcomes, e.g., working in protected sites, using seedlings, increasing the number of reintroduced individuals, mixing material from diverse populations, using transplants from stable source populations, site preparation or management effort and knowledge of the genetic variation of the target species. This study also revealed shortcomings of common experimental designs that greatly limit the interpretation of plant reintroduction studies: (1) insufficient monitoring following reintroduction (usually ceasing after 4 years); (2) inadequate documentation, which is especially acute for reintroductions that are regarded as failures; (3) lack of understanding of the underlying reasons for decline in existing plant populations; (4) overly optimistic evaluation of success based on short-term results; and (5) poorly defined success criteria for reintroduction projects. We therefore conclude that the value of plant reintroductions as a conservation tool could be improved by: (1) an increased focus on species biology; (2) using a higher number of transplants (preferring seedlings rather than seeds); (3) taking better account of seed production and recruitment when assessing the success of reintroductions; (4) a consistent long-term monitoring after reintroduction.     

Habitat characteristics of adult frosted elfins (Callophrys irus) in sandplain communities of southeastern Massachusetts, USA

Changes to land use and disturbance frequency threaten disturbance-dependent Lepidoptera within sandplain habitats of the northeastern United States. The frosted elfin (Callophrys irus) is a rare and declining monophagous butterfly that is found in xeric open habitats maintained by disturbance. We surveyed potential habitat for adult frosted elfins at four sites containing frosted elfin populations in southeastern Massachusetts, United States. Based on the survey data, we used kernel density estimation to establish separate adult frosted elfin density classes, and then used regression tree analysis to describe the relationship between density and habitat features. Adult frosted elfin density was greatest when the host plant, wild indigo (Baptisia tinctoria), density was >2.6 plants/m² and tree canopy cover was <29%. Frosted elfin density was inversely related to tree cover and declined when the density of wild indigo was <2.6 plants/m² and shrub cover was ?16%. Even small quantities of non-native shrub cover negatively affected elfin densities. This effect was more pronounced when native herbaceous cover was <36%. Our results indicate that management for frosted elfins should aim to increase both wild indigo density and native herbaceous cover and limit native tree and shrub cover in open sandplain habitats. Elimination of non-native shrub cover is also recommended because of the negative effects of even low non-native shrub cover on frosted elfin densities. The maintenance of patches of early successional sandplain habitat with the combination of low tree and shrub cover, high host plant densities, and the absence of non-native shrubs appears essential for frosted elfin persistence, but may also be beneficial for a number of other rare sandplain insects and plant species.     

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.     

Does the acephaline gregarine Monocystis sp. modify the surface behaviour of its earthworm host Lumbricus terrestris?

The earthworm Lumbricus terrestris has relatively low dispersal rates. This can represent a challenge for the internal gregarine parasite Monocystis, the dispersal of which often depends on the host. Mating of Monocystis can also be restricted to parasite stages within the current host individual. Adaptations, including host behavioural modification, that improve parasite transmission and simultaneously avoid inbreeding within a single host individual should be favoured by selection. We used a correlative approach to investigate the question of parasitic manipulation in this Gregarine-Lumbricid system. We observed mature earthworms (n=24) for 3 weeks while recording various measures of activity (surface activity, burrowing activity, surfacing delay, number of surface visits) and correlated parasite load with these activity measures. We found a significant positive correlation between surface activity and midden (or cast) production, which suggests a simple method for assessing the overall activity of local earthworm populations. However, we found no evidence of behavioural manipulation of any measure of host activity. We discuss these results in the context of inbreeding depression and host-parasite coevolution.     

Re-test of Rhinocyllus conicus host specificity, and the prediction of ecological risk in biological control

Biological control is proposed as an ecological strategy to manage the threat of invasive plants, especially in natural areas. To pursue this strategy, we need to know that the host specificity criteria used to evaluate ecological risk with deliberate introduction of an exotic insect for biocontrol are sufficient to predict potential impact on native species. Host specificity is defined by adult feeding and oviposition preferences and larval development. One way to evaluate the criteria is to re-examine case histories where ecological effects are recorded, such as that of Rhinocyllus conicus Frölich. This flower head weevil, released in North America in 1968 to control exotic thistles like Musk thistle (Carduus nutans L), is now reducing seed production by multiple native North American thistle species (Cirsium spp.), and local population density of Platte thistle (Cirsium canescens Nutt.). We hypothesized that host specificity of R. conicus has changed since pre-release testing, providing an explanation for the unexpected magnitude of the documented ecological effects. Instead, when we re-tested host specificity of weevils naturalized over 28 generations, we found that host specificity has not changed. Naturalized adults of R. conicus showed strong feeding and oviposition preference for Musk thistle over Platte thistle. In addition, larval development by these weevils was faster and more successful (to larger size) on Musk thistle than on Platte thistle. Thus, our results indicate that a change in host specificity cannot explain the unexpectedly large build-up of R. conicus and significant ecological effect on Platte thistle. We conclude that accurate prediction of the potential level of impact on native host plants in the field requires further ecological information in addition to host specificity.     

The effects of captive experience on reintroduction survival in carnivores: A review and analysis

This review focuses on the success and survivorship of captive-born versus wild-caught carnivores used in reintroductions. Previous reviews have suggested that reintroduction projects using captive-born animals are less likely to be successful than projects translocating wild-caught animals. The purpose of this paper is to examine this statistically and investigate how captivity may affect the survival of reintroduced carnivores. We examined results published in previous reviews, and found evidence to support that reintroduction projects using wild-caught animals are significantly more likely to succeed than projects using captive-born animals. We further compiled our own review of 45 case studies in carnivore reintroduction projects (in 17 species across 5 families) to investigate survival rates rather than overall project ‘success’. We found that (1) wild-caught carnivores are significantly more likely to survive than captive-born carnivores in reintroductions; (2) that humans were the direct cause of death in over 50% of all fatalities and (3) that reintroduced captive-born carnivores are particularly susceptible to starvation, unsuccessful predator/competitor avoidance and disease.     

Changes in Mycobacterium spp. population structure and pyrene mineralization in polycyclic aromatic hydrocarbon-amended soils

The effect of pyrene and phenanthrene contamination on soil Mycobacterium spp. community structure was examined using PCR-amplification of 16S rRNA genes with primers specific for the fast-growing group of Mycobacterium spp. and separation of phylotypes by temperature gradient gel electrophoresis (TGGE). The degradative potential of the soil microbial community was measured over time by mineralization of ¹⁴C-pyrene added to the contaminated soils. PCR-TGGE profiles, in combination with band sequencing and phylogenetic analysis of the prominent phylotypes, indicated shifts in the Mycobacterium spp. community during incubation. Reductions in species diversity and enrichments of specific populations were observed in all pyrene- and phenanthrene-treated soils, in contrast to the relatively stable control soil profiles. Mineralization studies indicated the shortest acclimation periods and the highest initial rates of pyrene degradation occurred in soils pre-exposed to phenanthrene, or a mixture of phenanthrene and pyrene, for 14 weeks. Pre-exposure of soil microorganisms to a single dose of pyrene for the same length of time also decreased the acclimation period for the degradation of pyrene. Monthly application of either pyrene or phenanthrene to soils, however, resulted in an increase in pyrene degradative potential 6 weeks after the first pre-exposure, but a decrease in degradative potential 14 weeks after the first pre-exposure. Similar PCR-TGGE profiles were obtained from soils with comparable pyrene mineralization curves or degradative potentials.