A preliminary population viability analysis of the critically endangered blue‐eyed black lemur (Eulemur flavifrons)

Population viability analysis is an important tool to assess the extinction risk in small populations of highly specialized primates. The blue‐eyed black lemur (Eulemur flavifrons) is critically endangered with a restricted range in the north‐western dry deciduous forest of Madagascar, where habitat fragmentation and loss of forest connectivity threaten its survival. We performed a population viability analysis (PVA) of this lemur in Ankarafa Forest in the Sahamalaza Peninsula National Park, north‐western Madagascar, to determine the demographic parameters most influential for population persistence and to assess extinction probabilities. We conducted PVA analyses using different demographic parameters which characterize the species including reproduction, lifespan and population size using the software VORTEX for six scenarios with 100 iterations and simulated over 100 years. The simulations suggested the first extinction within 13 years when the percentage of habitat destruction increased up to 12%. Severe habitat destruction such as fire and logging was the major cause which led to the risk of population extinction. Conservation strategies, in particular measures to reduce habitat destruction, are proposed to ensure the survival of this critically endangered lemur.     

Microhabitat suitability as a tool to improve the success rate of a translocation or reintroduction,case‐study of the bullhead (Cottus perifretum) in Flanders,Belgium

Microhabitat suitability models are useful tools to enhance the reintroduction success of fish. Since 2008, a translocation and reintroduction program has been carried out in Flanders to prevent substantial loss of genetic variability in the Cottus perifretum (bullhead) population, and to meet the goals set by the Habitat Directive. To this end, habitat suitability of potential headstreams was assessed on a macrohabitat and microhabitat scale prior to the reintroduction. On a macrohabitat scale, water quality, habitat structure, food availability, and fish community were screened. Based on microhabitat models for bullhead in the summer period, microhabitat suitability was assessed in headstreams where macrohabitat characteristics showed a high potential for success. Both macro‐ and microhabitat assessment showed that reintroduction of bullheads in the Nellebeek, Bruelbeek, and Mollendaalbeek would most likely lead to self‐sustaining populations. For the Sint‐Annabeek, the microhabitat suitability model, considering depth and stream velocity, estimates that 7.5–9.5% of the headstream is suitable for bullhead. However, when substratum is taken into account, the microhabitat suitability index shows that only 4.3–5.8% of the brook is suitable. The current habitat quality and quantity in the Sint‐Annabeek is estimated to support a mean total population of 812 bullheads. However, the microhabitat suitability can be substantially improved by the artificial deposition of medium‐sized gravel (5–50 mm) and large gravel (50–100 mm). By doing so, the mean estimated population size could increase up to 1,330 individuals. Our results show that habitat improvement is necessary prior to the reintroduction of bullheads in the Sint‐Annabeek.     

Extinction,reintroduction, and restoration of a lizard meta‐population equilibrium in the missouri ozarks

In this issue of Molecular Ecology, Neuwald & Templeton (2013) report on a 22‐year study of natural populations of Collared Lizards (Crotaphytus collaris) that evolved on isolated on rock outcrops (‘glades’) in the Ozark Mountains in eastern Missouri. This ecosystem was originally maintained by frequent fires that kept the forest understory open, but fire‐suppression was adopted as official policy in about 1945, which led to a loss of native biodiversity, including local extinctions of some lizard populations. Policies aimed at restoring biodiversity included controlled burns and re‐introductions of lizards to some glades, which began in 1984. Populations were monitored from 1984–2006, and demographic and genetic data collected from 1 679 lizards were used to documents shifts in meta‐population dynamics over four distinct phases of lizard recovery: 1–an initial translocation of lizards drawn from the same source populations onto three glades that were likely part of one meta‐population; 2–a period of isolation and genetic drift associated with the absence of fires; 3–a period of rapid colonization and population increase following restoration of fire; and 4–stabilization of the meta‐population under regular prescribed burning. This study system thus provides a rare opportunity to characterize the dynamics of a landscape‐scale management strategy on the restoration of the meta‐population of a reintroduced species; long‐term case studies of the extinction, founding, increase, and stabilization of a well‐defined meta‐population, based on both demographic and population genetic data, are rare in the conservation, ecological, and evolutionary literature.     

Seasonal and inter‐island variation in the foraging strategy of the critically endangered Red‐headed Wood Pigeon Columba janthina nitens in disturbed island habitats derived from high‐throughput sequencing

We studied the feeding ecology of the critically endangered Red‐headed Wood Pigeon Columba janthina nitens, a subspecies endemic to a very remote and highly disturbed oceanic island chain, the Ogasawara Islands. An analysis based on high‐throughput sequencing (HTS) was undertaken on 627 faecal samples collected over 2 years from two island habitats, and food availability and the nutrient composition of the major fruits were also estimated. The HTS diet analysis detected 122 food plant taxa and showed clear seasonal and inter‐island variation in the diet of the Pigeons. The results indicated a preference for lipid‐rich fruits, but the diet changed according to the availability of food resources, perhaps reflecting the foraging strategy of the Pigeons in isolated island habitats with poor food resources. Pigeons also frequently consumed introduced plants at certain times of year, perhaps compensating for the lack of preferred native food resources. However, the degree of dependence on introduced plants appeared to differ between the two island habitats, so the different impacts of introduced plant eradication on the foraging conditions for the Pigeons on each island should be considered. HTS diet analysis combined with field data may be useful for monitoring the foraging conditions of endangered species and may also inform an appropriate conservation strategy in oceanic island ecosystems with complicated food webs that include both native and introduced species.     

Fine‐scale genetic structure reflects sex‐specific dispersal strategies in a population of sociable weavers (Philetairus socius)

Dispersal is a critical driver of gene flow, with important consequences for population genetic structure, social interactions and other biological processes. Limited dispersal may result in kin‐structured populations in which kin selection may operate, but it may also increase the risk of kin competition and inbreeding. Here, we use a combination of long‐term field data and molecular genetics to examine dispersal patterns and their consequences for the population genetics of a highly social bird, the sociable weaver (Philetairus socius), which exhibits cooperation at various levels of sociality from nuclear family groups to its unique communal nests. Using 20 years of data, involving capture of 6508 birds and 3151 recaptures at 48 colonies, we found that both sexes exhibit philopatry and that any dispersal occurs over relatively short distances. Dispersal is female‐biased, with females dispersing earlier, further, and to less closely related destination colonies than males. Genotyping data from 30 colonies showed that this pattern of dispersal is reflected by fine‐scale genetic structure for both sexes, revealed by isolation by distance in terms of genetic relatedness and significant genetic variance among colonies. Both relationships were stronger among males than females. Crucially, significant relatedness extended beyond the level of the colony for both sexes. Such fine‐scale population genetic structure may have played an important role in the evolution of cooperative behaviour in this species, but it may also result in a significant inbreeding risk, against which female‐biased dispersal alone is unlikely to be an effective strategy.     

Artificial dispersal of the lichen Crocodia aurata (Lobariaceae) using asexual propagules and gel‐filled gauze packets

Lichens are an essential component of ecosystem processes. Many lichen species are habitat specialists that rely on specific tree substrates and moisture regimes of old‐growth forests and are not found in early‐successional forests, small isolated forest fragments or restoration projects, making them useful bioindicators of forest health. Pressures from habitat loss and fragmentation have affected the viability and survival of lichen species that are often limited by low dispersal ability. As a rule, lichens are rarely included in ecological restoration programmes despite translocation methods being available. We trialled a combination of two of the more successful methods (gauze packets and use of adhesive gels). Three different gelling agents were used in attempt to immobilize living soredia of the lichen Crocodia aurata on trunks of Ti Kouka/Cabbage Tree (Cordyline australis) for long enough for them to develop into thallus lobes. The effectiveness of these methods was tracked over a 2‐year period. Our results show that all three gel treatments were effective at immobilizing soredia in the gauze packets. Lobe formation occurred in all three gel treatments after 36 weeks, with methyl cellulose the most successful with six packets producing lobes, five Ac‐Di‐Sol^® and two agarose packets also producing lobes, out of a possible total 100 gauze packets. Lobe formation was slightly more successful on the south sides of trees (seven of thirteen packets), despite initial survival and vitality of soredia being higher on the north sides of the trees.     

Factors influencing the occurrence of the Southern Long‐nosed Bandicoot (Perameles nasuta Geoffroy) during a population irruption and decline

Modelling the occupancy of species is a key part of the discipline of ecology, with particular efforts often focused on identifying which environmental, vegetation and other factors influence why a given species occurs where it does. Here, based on data gathered between 2003 and 2016, we developed models of the environmental, terrain and vegetation factors associated with site occupancy of the Southern Long‐nosed Bandicoot (Perameles nasuta Geoffroy) at Booderee National Park in the Jervis Bay Territory, south‐eastern Australia. The Long‐nosed Bandicoot is a nocturnal omnivorous marsupial which feeds primarily on subterranean invertebrates and fungi. The species has undergone a major reduction in abundance and site occupancy following a peak irruption in 2006 with the percentage of the sites at which the species was present declining from 74.3% of sites trapped in 2006 to 10.5% of sites trapped in 2016. We found the Long‐nosed Bandicoot was distributed widely across Booderee National Park and occurred in all six broad vegetation types in the reserve (forest, heathland, woodland, shrubland, sedgeland and rainforest). Detection‐occupancy modelling revealed that the persistence and colonisation of sites by the species were negatively associated with the per cent cover of leaf litter, irrespective of broad vegetation type. Occupancy models are an important tool in identifying parts of landscapes most likely to support populations of particular species, such as the Long‐nosed Bandicoot over time, and they may assist management of protected areas to prioritise resources to manage the habitat of those areas.     

Species‐level view of population structure and gene flow for a critically endangered primate (Varecia variegata)

Lemurs are among the world's most threatened mammals. The critically endangered black‐and‐white ruffed lemur (Varecia variegata), in particular, has recently experienced rapid population declines due to habitat loss, ecological sensitivities to habitat degradation, and extensive human hunting pressure. Despite this, a recent study indicates that ruffed lemurs retain among the highest levels of genetic diversity for primates. Identifying how this diversity is apportioned and whether gene flow is maintained among remnant populations will help to diagnose and target conservation priorities. We sampled 209 individuals from 19 sites throughout the remaining V. variegata range. We used 10 polymorphic microsatellite loci and ~550 bp of mtDNA sequence data to evaluate genetic structure and population dynamics, including dispersal patterns and recent population declines. Bayesian cluster analyses identified two distinct genetic clusters, which optimally partitioned data into populations occurring on either side of the Mangoro River. Localities north of the Mangoro were characterized by greater genetic diversity, greater gene flow (lower genetic differentiation) and higher mtDNA haplotype and nucleotide diversity than those in the south. Despite this, genetic differentiation across all sites was high, as indicated by high average F_ST (0.247) and Φ_ST (0.544), and followed a pattern of isolation‐by‐distance. We use these results to suggest future conservation strategies that include an effort to maintain genetic diversity in the north and restore connectivity in the south. We also note the discordance between patterns of genetic differentiation and current subspecies taxonomy, and encourage a re‐evaluation of conservation management units moving forward.     

Estimating the inbreeding level and genetic relatedness in an isolated population of critically endangered Sichuan taimen (Hucho Bleekeri) using genome‐wide SNP markers

Sichuan taimen (Hucho bleekeri) is critically endangered fish listed in The Red List of Threatened Species compiled by the International Union for Conservation of Nature (IUCN). Specific locus amplified fragment sequencing (SLAF‐seq)‐based genotyping was performed for Sichuan taimen with 43 yearling individuals from three locations in Taibai River (a tributary of Yangtze River) that has been sequestered from its access to the ocean for more than 30 years since late 1980s. Applying the inbreeding level and genetic relatedness estimation using 15,396 genome‐wide SNP markers, we found that the inbreeding level of this whole isolated population was at a low level (2.6 × 10^?3 ± 0.079), and the means of coancestry coefficients within and between the three sampling locations were all very low (close to 0), too. Genomic differentiation was negatively correlated with the geographical distances between the sampling locations (p < .001), and the 43 individuals could be considered as genetically independent two groups. The low levels of genomic inbreeding and relatedness indicated a relatively large number of sexually mature individuals were involved in reproduction in Taibai River. This study suggested a genomic‐relatedness‐guided breeding and conservation strategy for wild fish species without pedigree information records.     

Sex‐specific estimates of dispersal show female philopatry and male dispersal in a promiscuous amphibian,the alpine salamander (Salamandra atra)

Amphibians display wide variations in life‐history traits and life cycles that should prove useful to explore the evolution of sex‐biased dispersal, but quantitative data on sex‐specific dispersal patterns are scarce. Here, we focused on Salamandra atra, an endemic alpine species showing peculiar life‐history traits. Strictly terrestrial and viviparous, the species has a promiscuous mating system, and females reproduce only every 3 to 4 years. In the present study, we provide quantitative estimates of asymmetries in male vs. female dispersal using both field‐based (mark–recapture) and genetic approaches (detection of sex‐biased dispersal and estimates of migration rates based on the contrast in genetic structure across sexes and age classes). Our results revealed a high level of gene flow among populations, which stems exclusively from male dispersal. We hypothesize that philopatric females benefit from being familiar with their natal area for the acquisition and defence of an appropriate shelter, while male dispersal has been secondarily favoured by inbreeding avoidance. Together with other studies on amphibians, our results indicate that a species' mating system alone is a poor predictor of sex‐linked differences in dispersal, in particular for promiscuous species. Further studies should focus more directly on the proximate forces that favour or limit dispersal to refine our understanding of the evolution of sex‐biased dispersal in animals.     

Reproductive biology and responses to threats and protection measures of the total population of a Critically Endangered Galápagos plant,Linum cratericola (Linaceae)

We describe a reproductive and population dynamic study of the total population of a Critically Endangered plant over 10 years, during which part of the population was protected from the main threat, feral ungulates. Linum cratericola (Linaceae) was first discovered in 1966 at two sites on Floreana Island, Galápagos. It has since disappeared from one site and survives in three groups of plants at the other, where it has been threatened with extinction by introduced ungulates and invasive plants. Population size, and growth rate and mortality of individual plants, have been monitored since 1997. The population appears highly responsive to changes in threat levels: the three plant groups increased rapidly following protection by fencing and ungulate control, but temporarily declined when feral goat pressure increased and during dry periods. Natural factors that may contribute to population limitation include dry years, grazing by native snails and competition from native vascular plants and cryptogams. Linum cratericola has a single flowering period per year and produces abundant seed with 28% germination after scarification, but with no obvious adaptations for long‐distance dispersal. Potential pollinators included the butterfly Leptotes parrhasioides, the hoverfly Toxomerus crockeri and the carpenter bee Xylocopa darwinii, all endemic to Galápagos. The continued survival of L. cratericola in the wild depends on effective protection from introduced herbivores and invasive plants. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161 , 89–102.     

Origins of recently re‐established and newly discovered populations of the endangered butterfly Shijimiaeoides divinus (Lepidoptera: Lycaenidae) in Oita Prefecture,Japan

The endangered butterfly Shijimiaeoides divinus was believed to have been extirpated from Oita Prefecture, Kyushu, Japan, but was rediscovered in Taketa in recent years. This population is considered to have re‐established as a result of natural dispersal from Kumamoto, a neighboring prefecture located to the west of Oita. Furthermore, another population was recently found in Yufu, Oita Prefecture, which is an area where the species had never been recorded. To elucidate the origins of these two populations newly found from Oita Prefecture, their DNA sequences of the mitochondrial cytochrome c oxidase subunit I (COI) gene were compared with those of other S. divinus populations from Kumamoto Prefecture, Honshu and Korea. The results supported the hypothesis that the Taketa population originated from Kumamoto Prefecture. However, it was not clear whether this population originated from the natural dispersal or deliberate release of individuals. It was also found that the Yufu population was not established by the deliberate release of individuals from Honshu or Korea; however, it remained unclear whether the population of S. divinus was native to Yufu, or originated from other localities in Kyushu.     

Effects of parental number and duration of the breeding period on the effective population size and genetic diversity of a captive population of the endangered Tokyo bitterling Tanakia tanago (Teleostei: Cyprinidae)

The maintenance of genetic diversity is one of the chief concerns in the captive breeding of endangered species. Using microsatellite and mtDNA markers, we examined the effects of two key variables (parental number and duration of breeding period) on effective population size (N_e) and genetic diversity of offspring in an experimental breeding program for the endangered Tokyo bitterling, Tanakia tanago. Average heterozygosity and number of alleles of offspring estimated from microsatellite data increased with parental number in a breeding aquarium, and exhibited higher values for a long breeding period treatment (9 weeks) compared with a short breeding period (3 weeks). Haplotype diversity in mtDNA of offspring decreased with the reduction in parental number, and this tendency was greater for the short breeding period treatment. Genetic estimates of N_e obtained with two single‐sample estimation methods were consistently higher for the long breeding period treatment with the same number of parental fish. Average N_e/N ratios were ranged from 0.5 to 1.4, and were high especially in the long breeding period with small and medium parental number treatments. Our results suggest that the spawning intervals of females and alternative mating behaviors of males influence the effective size and genetic diversity of offspring in bitterling. To maintain the genetic diversity of captive T. tanago, we recommend that captive breeding programs should be conducted for a sufficiently long period with an optimal level of parental density, as well as using an adequate number of parents. Zoo Biol 31:656‐668, 2012. © 2011 Wiley Periodicals, Inc.     

Immunolocalization of keratin‐associated beta‐proteins (beta‐keratins) in the regenerating lizard epidermis indicates a new process for the differentiation of the epidermis in lepidosaurians

The process of keratinocyte differentiation was analyzed in the regenerating epidermis of the lizard Anolis carolinensis, where the genes coding for beta‐proteins (beta‐keratins) are known. The regenerating epidermis forms all epidermal layers found in normal scales (Oberhäutchen‐, beta‐, mesos‐, and alpha‐layer). Three specific proteins representing the larger families of beta‐proteins, glycine‐rich (HgG5, 28% glycine, 3.6% cysteine), glycine‐cysteine medium‐rich (HgGC10, 13% glycine, 14.5% cysteine), and glycine‐cysteine rich (HgGC3, 30.4% glycine, 8.7% cysteine) have been immunolocalized at the ultrastructural level. HgG5 is only present in differentiating beta‐cells, a weak or no labeling is observed in Oberhäutchen and is absent in alpha‐cells. The protein is located in the pale corneous material forming the compact beta‐layer but is absent in mature Oberhäutchen cells. HgGC10 is present among beta‐packets in Oberhäutchen and beta‐cells but disappears in more compact and electron‐pale corneous material. The labeling disappears in mesos‐cells and is present with variable intensity in alpha‐cells, whereas lacunar and clear‐cells are low labeled to unlabeled. HgGC3 is sparse or absent in beta‐cells but is lightly present in the darker corneous material of differentiating and mature alpha‐cells, lacunar‐cells, and clear‐cells. The study suggests that while glycine‐rich proteins (electron‐pale) are specifically used for building the resistant and hydrophobic beta‐layer, cysteine–glycine rich proteins (electron‐denser) are used to form the pliable corneous material present in the Oberhäutchen and alpha‐cells. The differential accumulation of beta‐proteins on the alpha‐keratin cytoskeleton scaffold and not the alternance of beta‐ with alpha‐keratins allow the differentiation of different epidermal layers. © 2012 Wiley Periodicals, Inc.     

Comparative immunolocalization of keratin‐associated beta‐proteins (beta‐keratins) supports a new explanation for the cyclical process of keratinocyte differentiation in lizard epidermis

Lizard epidermis is made of beta‐ and alpha‐layers. Using Western blot tested antibodies, the ultrastructural immunolocalization of specific keratin‐associated beta‐proteins in the epidermis of different lizard species reveals that glycine‐rich beta‐proteins (HgG5) localize in the beta‐layer, while glycine–cysteine‐medium‐rich beta‐proteins (HgGC10) are present in oberhautchen and alpha‐layers. This suggests a new explanation for the formation of different epidermal layers during the shedding cycle in lepidosaurian epidermis instead of an alternance between beta‐keratins and alpha‐keratins. It is proposed that different sets of genes coding for specific beta‐proteins are activated in keratinocytes during the renewal phase of the shedding cycle. Initially, glycine–cysteine‐medium‐rich beta‐proteins with hydrophilic and elastic properties accumulate over alpha‐keratins in the oberhautchen but are replaced in the next cell layer with glycine‐rich hydrophobic beta‐proteins forming a resistant, stiff, and hydrophobic beta‐layer. The synthesis of glycine‐rich proteins terminates in mesos and alpha‐cells where these proteins are replaced with glycine–cysteine‐rich beta‐proteins. The pattern of beta‐protein deposition onto a scaffold of intermediate filament keratins is typical for keratin‐associated proteins and the association between alpha‐keratins and specific keratin‐associated beta‐proteins during the renewal phase of the shedding cycle gives rise to epidermal layers possessing different structural, mechanical, and texture properties.     

Plio‐Pleistocene diversification and genetic population structure of an endangered lizard (the Blue Mountains water skink,Eulamprus leuraensis) in south‐eastern Australia

Aim Although climatic fluctuations occurred world‐wide during the Pleistocene, the severity of glacial and drought events – and hence their influence on animal and plant biogeography – differed among regions. Many Holarctic species were forced to warmer‐climate refugia during glacial periods, leaving the genetic signature of recent expansion and gene flow among modern‐day populations. Montane south‐eastern Australia experienced less extreme glaciation, but the effects of drier and colder climatic conditions over this period on biotic distributions, and hence on the present‐day genetic structure of animal and plant populations, are poorly known. Location South‐eastern Australia. Methods The endangered Blue Mountains water skink (Eulamprus leuraensis) is a viviparous lizard known from fewer than 40 isolated small swamps at 560–1060 m elevation in south‐eastern Australia. We conducted molecular phylogenetic, dating and population genetics analyses using the mitochondrial NADH dehydrogenase 4 (ND4) of 224 individuals of E. leuraensis sampled across the species’ distribution. Results Ancient divergences in haplotype groups between lizards from the Blue Mountains and the Newnes Plateau, and strong genetic differences, even between swamps separated by only a few kilometres, suggest that the species has persisted as a series of relatively isolated populations within its current distribution for about a million years. Presumably, habitat patches similar to current‐day swamps persisted throughout glacial–interglacial cycles in this region, allowing the development of high levels of genetic structuring within and among present‐day populations. Main conclusions Our results suggest that less extreme glacial conditions occurred in the Southern Hemisphere compared with the Northern Hemisphere, allowing cold‐adapted species (such as E. leuraensis) to persist in montane areas. However, additional studies are needed before we can assemble a comprehensive view of the impact of Pleistocene climatic variation on the phylogeography of Southern Hemisphere taxa.     

Isolation of 22 new Haliaeetus microsatellite loci and their characterization in the critically endangered Madagascar fish‐eagle (Haliaeetus vociferoides) and three other Haliaeetus eagle species

We isolated a total of 22 microsatellite loci from two Haliaeetus species: the Madagascar fish‐eagle (Haliaeetus vociferoides) and the bald eagle (Haliaeetus leucocephalus). Five loci were monomorphic in both the Madagascar fish‐eagle (n = 24–43) and the bald eagle (n = 2–8) but were found to be polymorphic in other Haliaeetus species. Haliaeetus loci have proved useful for investigating gene flow in Haliaeetus and Aquila eagles. Ten loci were polymorphic in the critically endangered Madagascar fish‐eagle and will be used to investigate the genetic population structure and mating system in this species.     

Phylogeography of a pearl oyster (Pinctada maxima) across the Indo‐Australian Archipelago: evidence of strong regional structure and population expansions but no phylogenetic breaks

This study investigates the genetic structure and phylogeography of a broadcast spawning bivalve mollusc, Pinctada maxima, throughout the Indo‐West Pacific and northern Australia. DNA sequence variation of the mitochondrial cytochrome oxidase subunit I (COI) gene was analysed in 367 individuals sampled from nine populations across the Indo‐West Pacific. Hierarchical AMOVA indicated strong genetic structuring amongst populations (Φ_ST = 0.372, P < 0.001); however, sequence divergence between the 47 haplotypes detected was low (maximum 1.8% difference) and no deep phylogenetic divergence was observed. Results suggest the presence of genetic barriers isolating populations of the South China Sea and central Indonesian regions, which, in turn, show patterns of historical separation from northern Australian regions. In P. maxima, historical vicariance during Pleistocene low sea levels is likely to have restricted planktonic larval transport, causing genetic differentiation amongst populations. However, low genetic differentiation is observed where strong ocean currents are present and is most likely due to contemporary larval transport along these pathways. Geographical association with haplotype distributions may indicate signs of early lineage sorting arising from historical population separations, yet an absence of divergent phylogenetic clades related to geography could be the consequence of periodic pulses of high genetic exchange. We compare our results with previous microsatellite DNA analysis of these P. maxima populations, and discuss implications for future conservation management of this species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 632–646.