Conservation biogeography of ecologically interacting species: the case of the Iberian lynx and the European rabbit

Aim To relate the recent Iberian lynx decline to changes in the distribution of the European rabbit after the haemorrhagic disease outbreak of 1989. As Iberian rabbits evolved in two geographically separated lineages, being the recent lynx range practically restricted to the southwestern lineage, we also test if differential range dynamics exists for these lineages, with the consequent implications for lynx conservation and reintroduction planning. Location The Iberian Peninsula. Methods We modelled environmental favourability for the lynx based on its distribution before 1989, and for the rabbit using distribution data collected primarily after 1989, and validated them using independent abundance data. We compared both models and combined them in a lynx occurrence forecast. We correlated the prevalence of southwestern rabbit lineage with the environmental favourability for the rabbit. Results The environmental lynx model correlated with past lynx abundance data, but did not reflect its recent strong range contraction. The rabbit model correlated with recent rabbit abundance, but was negatively correlated with the environmental model for the lynx. The combination of both models forecasted lynx occurrence in a few separated nuclei, which encompass all recent lynx records. The prevalence of rabbit's southwestern lineage correlated negatively with favourability for the rabbit. Main conclusions The region to which the lynx became confined before 1989 is currently less favourable for rabbits, whereas more favourable areas remain outside lynx reach. This differential favourability correlates with rabbit phylogeographical structure, suggesting that the southwestern lineage is facing more unfavourable conditions or is less resilient to recent diseases. The loss of concordance between lynx distribution and the whole rabbit phylogeographical structure has prevented lynx persistence in northeastern rabbit lineage areas, which should be considered in lynx reintroduction planning. Similar conservation problems could affect other ecologically interacting species whose distributions’ overlapping has sharply diminished.     

Proximate and ultimate causes of dispersal in the Iberian lynx Lynx pardinus

Most studies on the causes of animal dispersal focus on speciesof birds or small mammals, but there are few such studies onsolitary carnivores. A complete picture of the causes of animaldispersal is not possible without considering cases on a representativeset of animals. The Iberian lynx is a medium-size, solitarycarnivore that inhabits metapopulations, where dispersal playsa prominent role. Between 1983 and 1998 we studied the proximateand ultimate causes of dispersal in Iberian lynx in the Doñanametapopulation (southwestern Spain), based on radio-trackingof 49 individuals. Saturation of limited breeding areas in thissmall population leads to high dispersal rates in both sexes.Most lynxes dispersed from their natal area between 12 and 24months of age. Males younger than 1 year old tended to dispersein a higher proportion than females of the same age. However,high dispersal rates for both sexes by the age of 2 years andthe lack of differences in the dispersal distances do not supportinbreeding avoidance as an ultimate cause of dispersal. Dispersalmainly started between January and June (24/29 cases), whenmost social interactions occur, which supports the social subordinationhypothesis. Lynxes left the natal range at an earlier age fromthe local population with higher density, which supports intraspecificcompetition for resources as a cause for dispersal. However,prey seems not to be the limiting resource because dispersalmostly started during the season of increasing prey density,and individual probability of dispersal increases with preydensity in the natal area. Dispersers suffered higher mortalitythan nondispersing lynxes of the same age, due mostly to anthropogeniccauses. About half of the dispersers successfully settled ina territory at distances that differed between areas of origin,but not between sexes. Distances reached, shorter than thosereported for other similar-size solitary felids, are limitedby anthropogenic barriers that prevent connection with closermetapopulations.     

An experimental study of translocation success and habitat improvement in wild rabbits

The translocation of wild animals is a strategy frequently used in the conservation and management of natural populations. The aim of this study was to evaluate the impact of translocation (population supplementation) and habitat improvement on the abundance of European wild rabbit Oryctolagus cuniculus . We used eight open plots with different habitat treatments: two with increased shelter, two with increased food, two with increased shelter and food and two without habitat treatment (control plots). We translocated wild rabbits during 3 consecutive years, each year in four of the eight plots, with the remaining plots serving as control for the translocation treatment. Rabbit abundance (translocated plus native rabbits) was calculated by means of pellet counts, and the results were evaluated mainly by generalized linear mixed models. We found that rabbit abundance was determined primarily by habitat improvement. Rabbits were more abundant in treated than in control plots, and most abundant in the plots where food availability was increased. This effect persisted throughout the year. Translocation also increased abundance, but this effect was the strongest where shelter and food had also been improved and declined and disappeared after breeding. These findings suggest that the habitat is an important factor for rabbit abundance, with food availability being the prime factor regulating densities. Moreover, translocations on their own are only effective in the short term in situations in which factors limiting population growth (e.g. disease and predation) have not been corrected. Translocations should be carried out in conjunction with improvements in release habitat as rabbit densities will depend on the maximum carrying capacity of the habitat.     

Postglacial dispersal of the European rabbit (Oryctolagus cuniculus) on the Iberian peninsula reconstructed from nested clade and mismatch analyses of mitochondrial DNA genetic variation

Nested clade analysis was applied to cytochrome b restriction site data previously obtained on 20 natural populations of the European rabbit across the Iberian Peninsula to test the hypothesis of postglacial dispersal from two main refugia, one in the northeast and the other in the southwest. Apart from historical fragmentation that resulted in geographic discontinuity of two distinct mitochondrial DNA (mtDNA) clades A and B, patterns of haplotype genetic variability have been shaped mostly by restricted gene flow via isolation by distance. The distribution of tip versus interior haplotypes suggests that dispersal occurred from both the southwestern and northeastern groups. Dispersal from the southwest had a north and northwest direction, whereas from the northeast it had mostly a western and southern orientation, with subsequent overlap in a southeastern-northwestern axis across the Iberian Peninsula. The analysis of the pairwise mismatch distribution of a 179-181-bp fragment of the mtDNA control region, for seven of those populations, further supports the idea that major patterns of dispersal were in the direction of central Iberia. Additionally, rabbit populations do not show signs of any significant loss of genetic diversity in the recent past, implying that they maintained large population sizes and structure throughout the ice ages. This is congruent with the fact that the Iberian Peninsula was itself a glacial refugium during Quaternary ice ages. Nonetheless, climatic oscillations of this period, although certainly milder than in northern Europe, were sufficient to affect the range distributions of Iberian organisms.     

Foraging requirements of the endangered long-fingered bat: the influence of micro-habitat structure, water quality and prey type

Myotis capaccinii is one of the most endangered Mediterranean bats. We radio tracked 21 adult individuals to assess foraging range and analyse micro-habitat selection around a nursery roost in central Italy. Habitats were characterized by development of riparian vegetation, distance between banks, degree of water clutter and levels of water pollution (expressed by macro-benthic bioindicators). Diet was also analysed to see whether prey rarity might account for species decline. Myotis capaccinii proved highly mobile: the maximum straight line distance between roost location and the farthest foraging fix recorded on one night was c . 21 km, whereas this variable averaged 7.5 km for the entire study. In general, the species preferred calm waters bordered by well-developed riparian vegetation and large (>5 m) inter-bank distances. Such factors determined the overall quality of foraging sites. Although diet was dominated by pollution-tolerant insects such as Chironomus midges, bats preferred less polluted waters. Our study also confirmed the occurrence of piscivory in this bat. Of the factors potentially responsible for species endangerment, the most likely are general habitat degradation, that is alteration of riparian vegetation and pollution, and cave roost loss. Given the large ecological niche overlap, increasing Myotis daubentonii may be outcompeting M. capaccinii . The most urgent actions to preserve M. capaccinii are extensive restoration of riparian vegetation and strict roost protection. Our study offers indications about where, and how, restoration of riparian vegetation may translate into best conservation results.     

European rabbit population trends and associated factors: a review of the situation in the Iberian Peninsula

• 1 European rabbits are considered a keystone species in the Iberian Peninsula. Their populations have sharply declined over the past century, mainly due to habitat loss and the arrival of two viral diseases: myxomatosis in the 1950s and rabbit haemorrhagic disease (RHD) at the end of the 1980s. For the conservation of the Iberian Mediterranean ecosystem, it is important to determine whether rabbit populations are recovering two decades after the RHD outbreak, and to identify the factors associated with population recovery.
• 2 Here, we review the current knowledge on recent rabbit population trends in the Iberian Peninsula and the factors associated with these trends.
• 3 Although most rabbit populations are still declining in the Iberian Peninsula, a few seem to have recovered. In general, positive trends have been recorded in species‐friendly habitats characterized by non‐fragmented landscapes, interspersed patches of Mediterranean scrubland, good pastures and/or crops, soft soils that are suitable for warren construction and a Mediterranean climate with relatively high rainfall. Additionally, rabbits seem to be recovering better in areas where management practices (e.g. low hunting pressure, habitat management and predator control) are applied to increase their numbers.
• 4 From these findings, it is possible to identify five broad objectives for rabbit conservation in the Iberian Peninsula. First, it is clearly necessary to establish a long‐term programme for monitoring rabbit abundance and trends on a large scale. Second, the conservation and restoration of open Mediterranean scrubland should be a priority for stabilizing and maintaining existing healthy rabbit populations. Third, despite the lack of experimental evidence, management activities aimed at increasing the quantity and quality of both refuge and food should continue to be implemented. Fourth, legislation on the timing of the hunting season should be revisited following recommendations made by scientists. Finally, experimental approaches are required to investigate whether the control of generalist predators is a successful strategy to allow rabbit populations to recover.

     

Habitat use by the inland carpet python (Morelia spilota metcalfei: Pythonidae): Seasonal relationships with habitat structure and prey distribution in a rural landscape

Abstract Squamate reptiles are significant components of woodland vertebrate communities in eastern Australia, but their ecology is poorly understood. We investigated seasonal variation in habitat use by the Inland Carpet Python, Morelia spilota metcalfei Wells and Wellington (Pythonidae), a threatened snake that inhabits the woodland environments of the Murray–Darling Basin. Nine pythons were radiotracked within and near the Mount Meg Flora and Fauna Reserve in north‐eastern Victoria to investigate how habitat structure and prey distribution (namely, that of the European Rabbit, Oryctolagus cuniculus L. (Leporidae)) influenced seasonal movement patterns. Data were analysed over three spatial scales to allow firm interpretations regarding resource selection. Pythons exhibited distinct seasonal trends in habitat use. During the cooler spring months, snakes chose warm, well‐insulated microhabitats, primarily rocky outcrops on north‐ and north‐west‐facing hillsides. Pythons moved widely during the summer months, apparently in search of prey. Snake localities could be readily linked to rabbit distribution at this time. Specifically, snakes moved to more open, disturbed habitats that contained a high density of rabbits, and consistently selected microhabitats in close proximity to rabbit burrows. In autumn, habitat use was transitional, as snakes progressively returned to the rocky hillsides where they overwintered. Thus, trends in habitat use were influenced by the snakes' thermoregulatory and foraging strategies. Careful management of specific habitats and feral prey populations is required to conserve populations of this endangered snake.     

Capercaillie in the Alps: genetic evidence of metapopulation structure and population decline

In the Alps, the capercaillie is distributed in a metapopulation pattern with local populations on mountain ranges separated by farmland valleys. Habitat deterioration, primarily related to human land use, resulted in population declines and range contractions became obvious. At the edge of a species' range, lower connectivity and less gene flow may render populations more susceptible to decline and extinction than in the core of the range. If this were true for the capercaillie in the Alps, edge populations should be subject to limited gene flow and should show genetic signs of a more severe population decline than core populations. To test this hypothesis, we used microsatellite DNA typing techniques. We assessed genetic variation within and among 18 local capercaillie populations across the Alps in relation to geographical distribution within the metapopulation system. All populations showed high levels of genetic variation in terms of average number of alleles, allelic richness and heterozygosity. Excess heterozygosity suggested a recent population decline, that was more pronounced in edge than core populations. We found high gene flow, but also significant differentiation among populations. Differentiation among edge populations was related to geographical distance, and appeared to be a recent process, most probably caused by reduced gene flow after population decline. In the core group, the high mountains of the central Alps seem to limit dispersal, and genetic drift was the most likely explanation for the observed differentiation among populations. We conclude that maintaining connectivity within the metapopulation system is vital for capercaillie conservation in the Alps.     

Genetic structure of an insect-pollinated and bird-dispersed tropical tree in vegetation fragments and corridors: implications for conservation

In the vegetation corridors that connect small remnants of undisturbed primary forest in the Lavras landscape (Brazil), Protium spruceanum is a representative of a mass-flowering insect-pollinated and bird-dispersed tree. Allozyme variation was quantified from five forest remnants (N = 150) from secondary vegetation corridors linking them (N = 80) to generate information for genetic conservation. The species adhered to H-W equilibrium in all fragments in most of the loci. The results indicated high gene diversity in the fragments and corridors positively correlated with the plant density (r = 0.742, R ² = 0.551, d.f. = 4). We did not find evidence of inbreeding within fragments nor overall The genetic differentiation among remnants was low Evidence of recent bottlenecks by anthropogenic disturbance was detected in fragments (P < 0.05, Wilcoxon sign-rank test). The minimal viable population was estimated for conservation in situ, indicating fragments with possibilities of maintaining genetic equilibrium diversity in the short term (except F3) and in the long term (only F5). The ratios was also calculated to contribute to vegetation enrichment, area recovery or creation of new vegetation corridors. We found high levels of gene diversity in the vegetation corridors, genetic identity with the fragments and absence of inbreeding. Thus, our results suggest that landscape management strategies should therefore consider both the creation of new vegetation corridors and the protection of extant ones.     

Influence of weather conditions on fly abundance and its implications for transmission of rabbit haemorrhagic disease virus in the North Island of New Zealand

Blowflies (Diptera: Calliphoridae) and flesh flies (Diptera: Sarcophagidae) are potential vectors of rabbit haemorrhagic disease virus (RHDV) in New Zealand. The associations between habitat and weather factors on the abundance of these flies were investigated. Between October 1999 and June 2001, flies were trapped on open pasture and in dense vegetation patches on farmland in the Himatangi area of the North Island. Five calliphorid species were trapped commonly at scrub edges and the most abundant sarcophagid, Oxysarcodexia varia Walker, was trapped mainly on open pasture. An abundance peak of O. varia was probably associated with the occurrence of a rabbit haemorrhagic disease (RHD) outbreak in the study area. Overall abundance of flies varied according to habitat and species, and species numbers differed between seasons and years. The all-day minimum temperature 3 weeks before trapping was a significant variable in all models of fly abundance, whereas average rainfall did not affect fly abundance. The all-day temperature range was significant only for O. varia. The influence of other climatic factors varied between fly species. Climate dependent variations in fly abundance may contribute to the risk of transmission of RHD, which occurred intermittently on the site during the study period.     

Population genetic structure of rock ptarmigan in the 'sky islands' of French Pyrenees: implications for conservation

Expected consequences of global warming include habitat reduction in many cool climate species. Rock ptarmigan is a Holarctic grouse that inhabits arctic and alpine tundra. In Europe, the Pyrenean ptarmigan inhabits the southern edge of the species' range and since the last glacial maximum its habitat has been severely fragmented and is restricted to high-alpine zones or 'sky islands'. A recent study of rock ptarmigan population genetic in Europe found that the Pyrenean ptarmigan had very low genetic diversity compared with that found in the Alps and Scandinavia. Habitat fragmentation and reduced genetic diversity raises concerns about the viability of ptarmigan populations in the Pyrenees. However, information on population structuring and gene flow across the Pyrenees, which is essential for designing a sound management plan, is absent. In this study, we use seven microsatellites and mitochondrial control region sequences to investigate genetic variation and differentiation among five localities across the Pyrenees. Our analyses reveal the presence of genetic differentiation among all five localities and a significant isolation-by-distance effect that is likely the result of short dispersal distances and high natal and breeding philopatry of Pyrenean ptarmigan coupled with severe habitat fragmentation. Furthermore, analysis of molecular variance, principal component analysis and Bayesian analysis of genetic structuring identified the greatest amount of differentiation between the eastern and main parts of the Pyrenean chain separated by the Sègre Valley. Our data also show that the Canigou massif may host an isolated population and requires special conservation attention. We propose a management plan which includes the translocation of birds. If a sky island structure affects genetic divergence in rock ptarmigan, it may also affect the genetic structure of other sky island species having low dispersal abilities.     

Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx

Noninvasive methods using genetic markers have been suggested as ways to overcome difficulties associated with documenting the presence of elusive species. We present and assess a novel, reliable and effective molecular genetic technique for the unequivocal genetic identification of faeces from the endangered Iberian lynx (Lynx pardinus). From mitochondrial DNA (mtDNA) cytochrome b and D-loop region sequences, we designed four species-specific primers (for products 130-161 bp long) that were considered to be likely to amplify degraded DNA. We compared two DNA extraction methods, various DNA amplification conditions and the robustness and specificity of the primer pairs with 87 lynx samples from 5 potentially different lynx populations and with 328 samples of other carnivore species. The utility of the identification technique was tested with faeces of different ages, with faeces from controlled field experiments, and with faeces collected from locales with possible lynx populations from throughout the state of Andalusia, Spain (8052 km2). Faecal mtDNA extraction was more efficient using PBS wash of the faeces instead of a faeces homogenate. Our assay increased from 92.6 to 99% efficiency with a second amplification and a reduction in template concentration to overcome polymerase chain reaction (PCR) inhibition. Our assay never produced false positives, and correctly identified all lynx faeces. Of 252 faeces samples of unknown species collected throughout Andalusia, 26.6% (from three different areas) were classified as Iberian lynx, 1.4% showed evidence of PCR inhibition and 1.2% were of uncertain origin. This method has proven to be a reliable technique that can be incorporated into large-scale surveys of Iberian lynx populations and exemplifies an approach that can easily be extended to other species.     

生境片断化对植物种群遗传结构的影响及植物遗传多样性保护

生境片断化是指大而连续的生境变成空间隔离的小种群的现象。生境片断化对植物种群遗传效应包括生境片断化过程中的取样效应及其后的小种群效应（遗传漂变、近交等）。理论研究表明,生境片断化后,植物种群的遗传变异程度将降低,而残留的小种群间的遗传分化程度将升高。然而对一些植物的研究表明,生境片断化对植物种群的遗传效应要受其他一些因素的影响,如世代长度、片断化时间、片断种群的大小、基因流的改变等。最后,针对生境     

Mitochondrial DNA variation among populations of Oedura reticulata (Gekkonidae) in remnant vegetation: implications for metapopulation structure and population decline

Restriction fragment length polymorphism (RFLP) analysis of mitochondrial DNA was used to examine the regional population structure of a species of gecko (Oedura reticulata) in vegetation remnants within the Western Australian wheatbelt. The species exhibited considerable polymorphism within and between populations with 22 haplotypes recognized among 12 populations. Phylogenetic analysis of haplotypes and clustering of nucleotide divergence among populations demonstrated little regional structure within the species with several haplotypes present in all three regions surveyed. This contrasted markedly with variation in haplotype frequency among populations which showed a high degree of independence between populations indicating that current levels of maternal gene flow are low and that the populations are too small to prevent genetic drift. This conclusion is supported by generally lower numbers of haplotypes in remnant populations than in nearby nature reserves. These findings, combined with demographic data from a previous study, suggest that post-fragmentation populations of O. reticulata are unable to form a metapopulation structure in the habitat that remains and that stochastic extinction forces alone will be sufficient to severely reduce the regional distribution of this species. This study demonstrates that mtDNA is a useful tool for detecting contemporary population phenomena and can provide qualitative information of practical importance to wildlife managers.     

Genetic diversity,genetic structure and phylogeography of the Iberian endemic Gypsophila struthium (Caryophyllaceae) as revealed by AFLP and plastid DNA sequences: connecting habitat fragmentation and diversification

Iberian gypsum outcrops are highly fragmented and ecologically challenging environments for plant colonization. As gypsophytes occur exclusively in such habitats, they are ideal models for the study of both the effects of habitat fragmentation and selection on population genetic diversity and structure. In this study, we used amplified fragment length polymorphism (AFLP) and plastid DNA sequences to investigate the phylogeographical history of the Iberian plant Gypsophila struthium (Caryophyllaceae), a widespread endemic restricted to Iberian gypsum outcrops. Gypsophila struthium consists of two subspecies that differ in the architecture of their inflorescence and have mostly allopatric ranges. Gypsophila struthium subsp. struthium occurs in central, eastern and south‐eastern Iberia, whereas G. struthium subsp. hispanica occurs in northern and eastern areas. AFLPs revealed low but significant genetic differentiation between the subspecies, probably as a result of a recent diversification during the Pliocene–Pleistocene. In the geographical contact zone between the taxa, the Bayesian analyses revealed populations with mixed ancestries and genetic clusters predominantly of one or the other subspecies, indicating incomplete reproductive barriers between them. Plastid DNA haplotypes revealed strong geographical structure and testified to processes of isolation by distance and continuous range expansion for some haplotype clades. The Bayesian analyses of the population structure of AFLP data and nested clade phylogeographical analysis (NCPA) of plastid haplotypes revealed that the putative ancestral range corresponded to central and eastern populations of G. struthium subsp. struthium, with those lineages contributing through more recent expansion to increased genetic diversity and structure of the south‐eastern and eastern ranges of this subspecies and to the diversification of G. struthium subsp. hispanica in northern and eastern gypsum outcrops. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 654–675.     

Landscape and weather determinants of prey availability: implications for the Lesser Kestrel Falco naumanni

Spatial and temporal variation in prey abundance have been shown to impact the time of breeding and breeding success of birds. Understanding the ecological requirements of preferred prey can help develop management measures to improve food supply for target species. For the colonial Lesser Kestrel Falco naumanni, mole crickets Gryllotalpa spp. are one of the most important prey items during the mate‐feeding period. Lesser Kestrel colonies with higher mole cricket consumption had earlier egg‐laying dates, suggesting that differences between individuals in the time of breeding could be caused by differences in the diet. Moreover, the mean number of mole crickets in pellets was significantly correlated with clutch size (in one of the studied years) and egg volume. Thus, the impact of environmental variables and land use on mole crickets is likely to be relevant to Lesser Kestrel conservation. Weekly consumption of mole crickets was higher following an increase in either precipitation or minimum temperature values. Furthermore, mole cricket consumption was higher in colonies surrounded by higher quality soils and in wetter areas and years. Predicted probability of mole cricket occurrence in surveyed watercourse margins suggested a positive relationship between soil penetrability and mole cricket occurrence. Among variables that might be the target of management, the presence of riparian vegetation positively influenced the occurrence of mole crickets, whilst tillage and sowing of streambeds were revealed as the most important threats. We suggest that the maintenance of native vegetation in the margins of watercourses could improve soil resilience to erosion, increase water retention, soil penetrability and fertility, and provide a food supply and shelter for mole crickets. Overall, the implementation of such recommendations is likely to benefit other farmland species known to consume mole crickets, including several endangered species.     

Influence of volcanic activity on the population genetic structure of Hawaiian Tetragnatha spiders: fragmentation, rapid population growth and the potential for accelerated evolution

Volcanic activity on the island of Hawaii results in a cyclical pattern of habitat destruction and fragmentation by lava, followed by habitat regeneration on newly formed substrates. While this pattern has been hypothesized to promote the diversification of Hawaiian lineages, there have been few attempts to link geological processes to measurable changes in population structure. We investigated the genetic structure of three species of Hawaiian spiders in forests fragmented by a 150-year-old lava flow on Mauna Loa Volcano, island of Hawaii: Tetragnatha quasimodo (forest and lava flow generalist), T. anuenue and T. brevignatha (forest specialists). To estimate fragmentation effects on population subdivision in each species, we examined variation in mitochondrial and nuclear genomes (DNA sequences and allozymes, respectively). Population subdivision was higher for forest specialists than for the generalist in fragments separated by lava. Patterns of mtDNA sequence evolution also revealed that forest specialists have undergone rapid expansion, while the generalist has experienced more gradual population growth. Results confirm that patterns of neutral genetic variation reflect patterns of volcanic activity in some Tetragnatha species. Our study further suggests that population subdivision and expansion can occur across small spatial and temporal scales, which may facilitate the rapid spread of new character states, leading to speciation as hypothesized by H. L. Carson 30 years ago.