Polygyny and female breeding failure reduce effective population size in the lekking Gunnison sage-grouse

Populations with small effective sizes are at risk for inbreeding depression and loss of adaptive potential. Variance in reproductive success is one of several factors reducing effective population size (N_e) below the actual population size (N). Here, we investigate the effects of polygynous (skewed) mating and variation in female breeding success on the effective size of a small population of the Gunnison sage-grouse (Centrocercus minimus), a ground nesting bird with a lek mating system. During a two-year field study, we recorded attendance of marked birds at leks, male mating success, the reproductive success of radio-tagged females, and annual survival. We developed simulations to estimate the distribution of male reproductive success. Using these data, we estimated population size () and effective population size N_e for the study population. We also simulated the effects of population size, skewed vs. random mating, and female breeding failure on N_e. In our study population, the standardized variance in seasonal reproductive success was almost as high in females as in males, primarily due to a high rate of nest failure (73%). Estimated N_e (42) was 19% of in our population, below the level at which inbreeding depression is observed in captive breeding studies. A high hatching failure rate (28%) was also consistent with ongoing inbreeding depression. In the simulations, N_e was reduced by skewed male mating success, especially at larger population sizes, and by female breeding failure. Extrapolation of our results suggests that six of the seven extant populations of this species may have effective sizes low enough to induce inbreeding depression and hence that translocations may be needed to supplement genetic diversity.     

Effects of supplementary feeding on the offspring sex ratio of kakapo: a dilemma for the conservation of a polygynous parrot

The kakapo (Strigops habroptilus) is a large, flightless, nocturnal parrot, endemic to New Zealand. It is critically endangered, with a world population of ca. 62 individuals and a male-biased adult sex ratio. The species has a polygynous “lek” mating system and adult males typically weigh 30-40% more than females. The kakapo is subject to intensive conservation efforts, including the provision of supplementary food to wild birds to encourage successful nesting. There is mounting evidence that, in polygynous species with large variance of male reproductive success, females in better condition may maximise their fitness by producing more offspring of the larger, more costly sex to be reared. We used data on the sex ratio of progeny of female kakapo that had or had not received supplementary food, to test the hypothesis that supplementary feeding might cause a male-biased offspring sex ratio. There was a significant excess of males in the clutches of females provided with supplementary food, suggesting that changes need to be made to the feeding regime to increase recruitment of females. This is an example of applying evolutionary theory to a practical conservation problem.     

Sex differences in population genetics, home range size and habitat use of the parti-colored bat (Vespertilio murinus, Linnaeus 1758) in Switzerland and their consequences for conservation

When habitats are declining, niche segregation by demographic groups, such as the two sexes, can have a profound impact on the extinction risk of a species as a whole. Thus, differences in the requirements of demographic groups are of importance in conservation. We combined behavioural and genetic data to investigate whether the sexually segregated parti-colored bat (Vespertilio murinus) exhibits sex-specific niche partitioning. We use our data to evaluate implications for conservation of this potentially vulnerable species in Switzerland, the western boundary of its range. Using radio-telemetry, we found sex-specific differences in habitat use. Foraging females strongly relied on lakes while foraging males displayed more flexibility in their habitat use. Moreover, males covered significantly larger foraging areas than females. Sequencing 341 base pairs of the mitochondrial D-loop of 247 individuals revealed sex-specific differences in the genetic structure of colonies, but no such difference was observed for three nuclear micro-satellite markers. We found high mtDNA diversity in two Swiss male colonies and one German female colony, but low mtDNA diversity in two Swiss female colonies. Our genetic data suggest that considerable gene flow occurs via male dispersal and mating. At the same time immigration of females into the existing female colonies in Switzerland is rare compared to the immigration of new males into male colonies. Since we found the sexes in Vespertilio murinus to differ markedly in their ecology, population genetics, and behaviour, we conclude that sex-specific conservation plans are required to protect this species efficiently.     

The importance of mating system in translocation programs: reproductive success of released male bridled nailtail wallabies

Translocation is an important tool for the conservation of species that have suffered severe range reductions. The success of a translocation should be measured not only by the survival of released animals, but by the reproductive output of individuals and hence the establishment of a self-sustaining population. The bridled nailtail wallaby is an endangered Australian macropod that suffered an extensive range contraction to a single remaining wild population. A translocated population was established and subsequently monitored over a four year period. The aim of this study was to measure the reproductive success of released males using genetic tools and to determine the factors that predicted reproductive success. Captive-bred and wild-caught animals were released and we found significant variation in male reproductive success among release groups. Variation in reproductive success was best explained by individual male weight, survival and release location rather than origin. Only 26% of candidate males were observed to sire an offspring during the study. The bridled nailtail wallaby is a sexually dimorphic, polygynous macropod and reproductive success is skewed toward large males. Males over 5800 g were six times more likely to sire an offspring than males below this weight. This study highlights the importance of considering mating system when choosing animals for translocation. Translocation programs for polygynous species should release a greater proportion of females, and only release males of high breeding potential. By maximizing the reproductive output of released animals, conservation managers will reduce the costs of translocation and increase the chance of successfully establishing a self-sustaining population.     

Mating system in a gopher tortoise population established through multiple translocations: Apparent advantage of prior residence

Population manipulations such as translocation are becoming increasingly important tools in the management of rare and declining species. Evaluating the effectiveness of such manipulations requires comprehensive monitoring of population processes, including dispersal, survivorship, and reproduction. We investigated the mating system of a translocated population of gopher tortoises (Gopherus polyphemus) established through multiple releases, which occurred primarily during 1987–1994. During 2006–2007, we sampled and genotyped 27 candidate males (candidate sires), 34 candidate females (candidate dams), and 121 offspring from 19 clutches at five polymorphic microsatellite loci to determine the relative frequency of multiple paternity and to estimate individual reproductive success. Multiple paternity was detected in 57% of clutches genotyped, and females of single-sire clutches and females of multiple-sire clutches were of similar size. Reproductive success varied among male tortoises, and successful sires were significantly larger than males to which no offspring were attributed. Among successful sires, previously established males sired a disproportionate number of the offspring sampled, despite being significantly smaller than subsequently released males. The high variance in individual reproductive success and the apparent reproductive advantage associated with prior residence observed in this gopher tortoise population has important implications for the design of future translocation projects.     

Management implications of capybara (Hydrochoerus hydrochaeris) social behavior

Capybaras (Hydrochoerus hydrochaeris) are the world’s largest rodent. Free-living populations are commercially harvested for their meat and leather in Colombia, Venezuela and Argentina; however, there is concern that legal and illegal harvesting is not sustainable. Since capybaras are considered an economic resource, there have been several attempts to explore the effect of different hunting strategies on its population dynamics. Two previous population models have been developed with this goal; however neither included capybara social behavior that may affect population dynamics. We developed an age-structured, density-dependent model of capybara herd dynamics to explore the demographic consequences of different hunting strategies. We then added infanticide and female reproductive suppression to explore the demographic consequences of such behavior. We conducted five different simulations and used ANOVA to estimate the effect of hunting females, hunting males, hunting both males and females, and the independent effects of reproductive suppression and infanticide on population size after 50 years. Our model suggests that suppression has the largest effect on population size, followed by hunting females and males hunting, female hunting, male hunting and infanticide. Thus, to develop more realistic harvesting models, managers should determine the degree of reproductive suppression and the frequency of infanticide by males.     

Protecting more than the wetland: The importance of biased sex ratios and habitat segregation for conservation of the Hine’s emerald dragonfly, Somatochlora hineana Williamson

Within species habitat use may depend on age, season or sex of an individual. The distribution of males and females may vary both temporally and spatially due to differences in the costs of reproduction and the distribution of critical resources. Conservation of a species requires knowledge of the habitat use of both sexes in order to predict the population size and protect all habitats that a species requires. Adult dragonfly populations often have highly male-biased sex ratios at the breeding habitat. This bias has been attributed to females using alternative habitats to avoid male harassment, or to high female mortality. We monitored adult Hine’s emerald dragonfly (Somatochlora hineana Williamson) populations, in breeding and non-breeding habitats in Door County, Wisconsin and found significant differences in habitat use between males and females. Males primarily used wetland habitats, while females primarily used dry meadows and marginal breeding habitats, only coming into wetlands to lay-eggs or find mates. We assessed food resources in the different habitats and found that high quality insect prey (primarily adult Diptera) were more available in the wetland habitat, indicating that these areas were likely a more productive foraging area for adult dragonflies. The fact that females appear to avoid the wetland habitat is consistent with the hypothesis that male harassment alters female distribution patterns. Consideration of the patterns of habitat use by S. hineana indicates the need to develop a broader understanding of the importance of non-wetland areas in the conservation of wetland species.     

High levels of hatching failure in an insular population of the South Island robin: a consequence of food limitation?

Endangered birds in insular environments like New Zealand are often translocated to predator-free offshore islands for conservation purposes. Some translocated populations however exhibit reduced fecundity, and it has been suggested that either inbreeding (due to small number of founders) or resource shortages (due to high population density) may limit reproductive success. For example, the South Island robin (Petroica a. australis) population on Motuara Island (59 ha) was founded by only five birds but has increased to ∼600 individuals, or a density >10 times that of the mainland. Despite this apparent success, the rate of hatching failure in this population is three times higher than in mainland populations, with more than a third of eggs failing to hatch. To test if elevated hatching failure is the result of food limitation, we carried out a food supplementation experiment by providing females with mealworms equivalent to ∼50% of their daily energy requirements. Food supplementation had no effect on hatching success, clutch size, incubation attentiveness or nest size. Egg volume increased with food supplementation in one of the two years of this study, but both egg volume and incubation attentiveness were unrelated to rate of hatching failure. As previous genetic analyses confirmed that the bottlenecked population of robins on Motuara Island have significantly less genetic variation than their source population, we conclude that inbreeding depression, and not food limitation, is the most likely explanation for their high rate of hatching failure. We suggest that the experimental translocation of genetically dissimilar individuals be considered as a possible remedy for low productivity in island populations that were initiated with few founders.     

Sperm storage and low incidence of multiple paternity in the European pond turtle, Emys orbicularis: A secure but costly strategy?

The freshwater pond turtle, Emys orbicularis, has recently suffered from population declines throughout its range, mainly due to habitat destruction. The mating strategies of this species were studied using genetic data from successive clutches within and between years. To test for the occurrence and frequency of multiple paternity and sperm storage, genetic paternity at six microsatellite markers was assessed in 114 embryos and hatchlings from single and subsequent clutches of 11 females (including clutches from the same or consecutive years). Multiple paternity was rare and only found in two out of 20 clutches from 11 females. All annual successive clutches and 58% of the clutches in the next year, were fertilized with sperm from the same male. The use of stored sperm is thus a frequent strategy in E. orbicularis. However, hatching rate, hatchling mass, and hatchling length decreased in clutches fertilized by stored sperm, suggesting sperm depletion or deterioration through time. The occurrence of stored sperm despite an associated reduced reproductive output indicated that mating and/or the fertilization process is costly to females. The low incidence of multiple paternity may simply be the residual consequence of the capacity to store viable sperm. These results provide important and innovative insights for the conservation of E. orbicularis. In threatened populations, management strategies may aim to enhance effective copulations in order to increase the reproductive output of females.     

Future prospects for the rare, late-flowering Gentianella germanica and Gentianopsis ciliata in Dutch nutrient-poor calcareous grasslands

We discuss the population biology of two calcareous grassland gentians, Gentianella germanica and Gentianopsis ciliata, in relation to the habitat management currently practiced in The Netherlands. There, at the margin of their range, both species are rare. Gentianella germanica persists on six remaining locations, whereas Gentianopsis ciliata, with two populations, is nearly extinct. Gentianella germanica is a strict biennial, Gentianopsis ciliata an iteroparous perennial. Both species depend on insects for seed production and suffer from low insect visitation. Pollination experiments in one Dutch population demonstrated that Gentianopsis ciliata is self-compatible, but hardly sets any seed under natural conditions due to pollen limitation. The low reproductive success of both species is partly due to the low pollinator densities at their late flowering time, partly caused by the small population size of the gentians themselves, and partly a result of mowing too early. The latter has destroyed the seed crop of several subsequent years in one population of Gentianopsis ciliata and some of Gentianella germanica. In Gentianella germanica, the early mowing and low insect visitation seems to have resulted in selection of less herkogamous and consequently more autofertile individuals. The perspectives for Gentianopsis ciliata are currently extremely poor in The Netherlands. Under the present circumstances, extinction will most likely occur within 10-20 years. Population reinforcement (seeding, artificial cross-pollination with nearby populations) should be considered if we want to conserve this species. For both gentians, but also of other flagship species of nutrient-poor calcareous grasslands, the total grassland area needs to be enlarged and must constitute an interconnected network of reserves. The traditional management method, sheep grazing, is to be preferred over mowing, but only if the flock visits each grassland patch or reserve for only a short time of less than a day, and with intervals of more than 2 weeks between visits. If mowing is preferred for other reasons, it should be done rotationally, and not before October.     

Geographic differentiation of morphological traits and isozymes in the Mediterranean island endemic Anchusa crispa: implications for the conservation of a protected species

Understanding population differentiation and genetic diversity within population is critical to the development of conservation programmes for threatened species. The protected species, Anchusa crispa Viv. occurs on coastal sand dunes in three disjunct geographical groups of populations: two populations on the east coast of Corsica, several populations around a single estuary on the west coast of Corsica and at a number of sites in north-west Sardinia, where two different subspecies occur. In this study we quantify differentiation of reproductive traits and isozymes among regions and populations on Corsica and between subspecies on Sardinia. No isozyme variation was detected within any of the studied populations nor among populations from a given geographic region. Two loci showed geographic differentiation between regions on Corsica. On Sardinia, the two subspecies showed no isozyme differentiation, and, depending on the loci examined, are similar to one or other of the two regions on Corsica. Reproductive traits show significant differentiation between geographic regions on Corsica, but little variation among populations within a region. In populations on the west coast of Corsica, flowers are small and have a stigma situated at the same level as the apex of the anthers whereas on the east coast, flowers are larger and have the stigma below the anthers. On Sardinia, A. crispa subsp. crispa has a floral morphology similar to the Corsican plants, whereas subspecies maritima has larger flowers with the stigma positioned above the anthers (approach-herkogamy). Quantitative variation in floral morphology thus agrees with the separation of two taxonomic entities on Sardinia and geographic variation in reproductive traits and isozymes has important ramifications for the sampling of populations for conservation programmes.     

Landscape changes influence the reproductive behaviour of a key ‘capital breeder’ snake (Boa constrictor occidentalis) in the Gran Chaco region, Argentina

Many wild reptile species are threatened by habitat loss. However, the way in which changes in landscape patterns influence intraspecific ecological processes is not completely understood. Boa constrictor occidentalis is an endangered species and has a special conservation value since it is endemic of dry forests in the Gran Chaco region. Because the Gran Chaco is largely threatened due to habitat loss it is necessary to know how landscape changes influence this species. Therefore, we evaluated the effects of forest loss and landscape composition on the reproductive life-history parameters. Landscape changes were assessed by analyzing satellite imagery and reproductive parameters were determined by ultrasound images of the reproductive structures. The obtained results indicate that habitat loss may affect body condition, clutch size and testicular volume of the Argentine boa constrictor. We also found that the spatial pattern of vegetation influences the distribution of females and males in the landscape. Matting aggregations are scarce in shrublands. Therefore, our study shows that forest loss could enhance vulnerability to extirpation through constraints placed on reproduction. We encourage resource managers to evaluate sensitive reproductive life-history parameters as well as habitat deterioration to asses the conservation status of the populations of the Argentine boa constrictor. Since the Gran Chaco forest, a key habitat to the species’ reproduction, is largely threatened, strong conservation action is needed to halt and reverse forest loss in this region.     

Genetic and demographic responses of fragmented Acacia dealbata (Mimosaceae) populations in southeastern Australia

Genetic and demographic studies of fragmented populations of common plant species often reveal negative impacts that are likely to constrain persistence. Examining species that are broadly representative of functional groups within fragmented landscapes is one approach to providing a better understanding of how these processes will influence vegetation persistence. Acacias are a significant component of the Australian flora, with Acacia dealbata being a common and representative species of fragmented landscapes across New South Wales. Previous reproductive assessments of fragmented A. dealbata populations indicated significant constraints for small populations through low reproductive output mediated by fertilisation success. This study examined genetic diversity, mating system, and progeny growth parameters of the seed crops produced by these populations to assess whether further constraints to persistence could be detected. Spatially explicit simulation studies were also conducted to assess the persistence likelihood of fragmented populations. Landscape parameters such as population size and plant density were useful predictors for some of the genetic and demographic responses, but a poor response signal was generally observed. Strong evidence for a self-incompatibility mechanism was observed in A. dealbata and is likely to be the major driver of population persistence. Self-incompatibility in small populations limits mate availability and eliminates inbred progeny early in the reproductive cycle leading to poor reproductive output. The simulation data provides further evidence that mate limitation in smaller populations (<200 plants and 40 S alleles) constrains reproductive output and persistence. These data indicate that introducing new germplasm to smaller populations can dramatically improve their persistence likelihood.     

Sex-specific roost movements and population dynamics of the vulnerable long-fingered bat, Myotis capaccinii

The roosts of many IUCN-listed cave-roosting bat species are under threat from tourist development in SE Europe and other regions of the world. Much-needed conservation strategies require, among other information, an understanding of their roost movements and population dynamics, which can now be obtained relatively quickly using advanced models. We have studied the long-fingered bat, Myotis capaccinii, an obligate cave-dweller, in Dadia National Park, Greece. The species formed colonies of up to a few thousand individuals and was highly mobile, frequently switching summer roosts up to 39 km apart, even during late pregnancy. The bats migrated to distant hibernacula including a cave in Bulgaria 140 km NW of the Park. Adult recapture probabilities varied with season and sex: low female recapture rates in autumn, relative to spring and summer, indicated non-random temporary emigration following nursery colony dispersal. The opposite pattern was seen in males: increasing recapture rates in the autumn suggest that males gather in these roosts to mate with females in transit. Adult survival (0.86-0.94) was similar in females and males, similar in winter and summer, and comparable to recent estimates for other bats based on similar modelling techniques. Sex-based differences in juvenile recapture suggest female philopatry and male-biased dispersal. Our work shows that protection of M. capaccinii roosts must extend beyond the Park’s and indeed the country’s boundaries: its conservation requires large-scale, trans-national integrated conservation plans. Our results will apply to many other warm-temperate species with similar life history cycles.     

Does reproductive plasticity in Lumbricus rubellus improve the recovery of populations in frequently inundated river floodplains?

Flooding events often eradicate all of the individuals of the earthworm species Lumbricus rubellus living in river floodplains, although earthworm cocoons usually survive immersion, permitting populations to recover after the flood waters recede. Yet, if the area is flooded again before earthworms hatching from cocoons or migrating from adjacent areas reach reproductive maturity, it is unlikely that their populations will recover. The objective of this study is to determine the importance of the length of the dry period for population recovery in L. rubellus. Earthworms were collected at three floodplain sites along the Rhine River that were frequently, moderately or seldom flooded. Reproductively mature L. rubellus from the frequent flooded site were half the weight and probably younger than those from the other sites. A mechanistic population model was used to estimate the time for earthworm development from hatching to reproductive maturity, and to calculate the probability of population recovery after flooding. The model results show that the probability of extinction increases when the dry period is not long enough for individuals to reach reproductive maturity. When this condition is met population extinction is virtually absent resulting from the high lifetime reproductive output of L. rubellus. Parameterization of the model with site-specific data indicate that population survival on the site with the shortest dry period drastically decreases if worms mature at the weight measured at the other sites. The results therefore strongly suggest that the dry period is critical for population recovery in river floodplains and that earthworm populations have adapted to local (site-specific) conditions.     

Genetic consequences of animal translocations: A case study using the field cricket, Gryllus campestris L.

Animal relocations have become a common tool in nature conservation, but the genetic consequences of such projects have rarely been studied in insects. As both natural and artificial formation of new populations may lead to genetic drift (founder effect), decreased genetic diversity and increased rates of inbreeding, genetic analyses can provide valuable information to evaluate the success of a relocation project. The field cricket (Gryllus campestris) has been subjected to reintroduction and translocation projects in England and northern Germany. Here, we present a microsatellite study on the population genetics of one recently established population of this species in comparison with several older populations and some recently colonized sites. Our results show that the translocation did not result in a significant loss of genetic diversity, when compared to source and other natural populations suggesting that translocation of a high number of nymphs from different subpopulations may be a suitable method to decrease the loss of genetic diversity and reduce the risk of inbreeding. Furthermore, the translocation had no negative effect on the source population, which reached a new maximum population size in 2006. An assignment test showed that individuals from the translocated population (F4 generation) were still assigned to the source populations, whereas two young subpopulations that originated by natural colonization from the central population about ten years ago already formed separate genetic clusters. As the strong fragmentation of G. campestris populations in northern Germany hampers natural colonization of newly created potential habitats, translocation projects seem to be an appropriate method to preserve this species.     

Habitat fragmentation reduces plant fitness by disturbing pollination and modifying response to herbivory

In fragmented landscapes plant species are often confined to remnants of formerly more widespread habitats, with many of their populations being small and isolated. This study experimentally examined the effects of population size and isolation on pollination, herbivory and reproductive success in the forest herb Phyteuma spicatum (Campanulaceae). In an experiment in which population size and isolation were manipulated using plants from the same origin, population size positively affected pollinator visitation, but did not alter the generally high levels of herbivory. As a result, seed production was higher in large populations. Conversely, plants originating from 14 natural populations of varying size and degree of isolation did not differ in reproductive success when grown in the same environment, suggesting similar attractiveness to pollinators and reproductive potential. The intensity of herbivory, however, was higher in progeny of small populations, at least in terms of the proportion of biomass removed. In both experiments, there were no effects of population isolation. The results suggest (1) that small population size decreases reproductive success via direct negative effects on plant-pollinator interactions, (2) that this pattern is not offset by herbivory, but (3) that herbivory enforces fragmentation effects on pollination by further reducing the number of flowering individuals and (4) that habitat fragmentation may influence plant fitness by affecting plant response to herbivory. The effects of habitat fragmentation on plant populations in present-day landscapes are thus complex, illustrating the need for more integrated studies in conservation biology that take into account both mutualistic and antagonistic plant-animal interactions.     

Socio-spatial behaviour of an African lion population following perturbation by sport hunting

Hunting of individuals from a population can affect its demography and socio-spatial parameters. This study provided opportunities to assess such effects, and may help to improve the conservation of populations threatened by conflict and over-use. We treated the periods before and after a moratorium on the trophy hunting of lions around Hwange National Park, Zimbabwe, as a quasi-experimental opportunity to examine changes in lion socio-spatial behaviour during and after perturbation. Changes in ranging behaviour coincided with the release from heavy mortality from hunting outside the Park and were likely to be due to changes in the perturbation regime, rather than factors such as prey abundance, which did not change over the study period. Lion home range sizes decreased in both sexes after the moratorium. Overlap between groups decreased in males but increased in females. Variation in home range size reduced both annually and seasonally for both sexes. Home range centres became more closely distributed. Lions increased the use of denser vegetation cover classes (>30%) and decreased the use of open cover classes (10–30%). Lions increased the use of areas within 2–5 km of water, and decreased their use of the >20 km class. Perturbation therefore appeared to influence the socio-spatial behavior of the lion population. Managers considering the use of moratoria as a conservation tool must anticipate changes in the behavior and distribution of the target species.     

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.