No apparent genetic bottleneck in the demographically declining European eel using molecular genetics and forward-time simulations

The stock of the European eel is considered to be outside safe biological limits, following a dramatic demographic decline in recent decades (90–99% drop) that involves a large number of factors including overfishing, contaminants and environmental fluctuations. The aim of the present study is to estimate the effective population size of the European eel and the possible existence of a genetic bottleneck, which is expected during or after a severe demographic crash. Using a panel of 22 EST-derived microsatellite loci, we found no evidence for a genetic bottleneck in the European eel as our data showed moderate to high levels of genetic diversity, no loss of allele size range or rare alleles, and a stationary population with growth values not statistically different from zero, which is confirmed by finding comparable value of short-term and long-term effective population size. Our results suggest that the observed demographic decline in the European eel did not entail a genetic decline of the same magnitude. Forward-time simulations confirmed that large exploited marine fish populations can undergo genetic bottleneck episodes and experience a loss of genetic variability. Simulations indicated that the failure to pick up the signal of a genetic bottleneck in the European eel is not due to lack of power. Although anthropogenic factors lowered the continental stock biomass, the observation of a stable genetic effective population size suggests that the eel crash was not due to a reduction in spawning stock abundance. Alternatively, we propose that overfishing, pollution and/or parasites might have affected individual fitness and fecundity, leading to an impoverished spawning stock that may fail to produce enough good quality eggs. A reduced reproduction success due to poor quality of the spawners may be exacerbated by oceanic processes inducing changes in primary production in the Sargasso Sea and/or pathway of transport across the Atlantic Ocean leading to a higher larval mortality.     

Comparing the seasonal survival of resident and migratory oystercatchers: carry‐over effects of habitat quality and weather conditions

Events happening in one season can affect life‐history traits at (the) subsequent season(s) by carry‐over effects. Wintering conditions are known to affect breeding success, but few studies have investigated carry‐over effects on survival. The Eurasian oystercatcher Haematopus ostralegus is a coastal wader with sedentary populations at temperate sites and migratory populations in northern breeding grounds of Europe. We pooled continental European ringing‐recovery datasets from 1975 to 2000 to estimate winter and summer survival rates of migrant and resident populations and to investigate long‐term effects of winter habitat changes. During mild climatic periods, adults of both migratory and resident populations exhibited survival rates 2% lower in summer than in winter. Severe winters reduced survival rates (down to 25% reduction) and were often followed by a decline in survival during the following summer, via short‐term carry‐over effects. Habitat changes in the Dutch wintering grounds caused a reduction in food stocks, leading to reduced survival rates, particularly in young birds. Therefore, wintering habitat changes resulted in long‐term (>10 years) 8.7 and 9.4% decrease in adult annual survival of migrant and resident populations respectively. Studying the impact of carry‐over effects is crucial for understanding the life history of migratory birds and the development of conservation measures.     

Density-dependent and inter-specific interactions affecting European eel settlement in freshwater habitats

Identifying the factors influencing the settlement of European eel (Anguilla anguilla) juveniles in continental habitats is crucial to designing effective management and conservation measures for this endangered species. A long-term data series (1993–2008) of European eel and European catfish (Silurus glanis) abundance in a freshwater canal of the Camargue water system (southern France), along with parallel data on water salinity and glass eel abundance in the adjacent Vaccarès lagoon, was analysed to identify the possible causes of decline in eel abundance observed in the canal during the last two decades. A model including glass eel recruitment and catfish abundance as covariates explained 78% of the observed variation in eel settlement success. Results suggest that (1) salinity does not play a significant role in determining the fraction of eels moving from the brackish lagoon to the canal; (2) density dependence affects settlement success, possibly through a reduction of juvenile survival in the adjacent lagoon; and (3) catfish abundance is negatively correlated with eel settlement. We discuss this latter point in terms of possible predation of catfish upon eels and/or inter-specific competition between the two species.     

Conservation insights from changing associations between habitat,territory distribution and mating system of Corn Buntings Emberiza calandra over a 20‐year population decline

Associations between habitat and animal distributions are widely used to make conservation recommendations. However, short‐term studies do not allow investigation of temporal variation in associations as habitats change or populations decline. Here we quantify changes in the habitat attributes and distribution of breeding territories in a multiple‐brooded, crop‐nesting farmland bird, the Corn Bunting Emberiza calandra, over a 20‐year period during which the study population declined by 91%. Corn Buntings were positively associated with weedy fields, overhead wires, spring cereals and, in early summer, with winter barley and forage grass. Territory associations with wires (positive) and fallow (positive in early summer, negative in late summer) were stronger in later years when the population was smaller. Trends in the proportions of males holding territories into late summer (decline), and mated polygynously or not at all (increases), suggested that habitat quality declined and became more spatially variable in later years. Field size increased and weed abundance within fields declined, reducing the availability of field‐boundary song‐posts, invertebrate‐rich foraging habitats and physical cover for nests within crops. Conservation recommendations are for weed‐rich or under‐sown spring cereals and winter barley combined with late‐cut hay and fallow, especially when offered close to song‐posts such as overhead wires. We also demonstrate the value of long‐term studies by comparing our 20‐year analysis with 3‐year periods at the start, middle and end of this period, and expose some risks of conservation recommendations derived from short studies.     

Distribution of genetic variation in farmed and natural stocks of european eel

European eel ( Anguilla anguilla ; Teleostei) is a valuable commercial species. However, over the past 25 years, the population of European eel has been declining to such a degree that major concerns have been raised for its long‐term conservation. Since little information is available on the life‐cycle and genetic structure of European eel, it has been difficult to evaluate the existence of any population substructuring. Molecular genetic methods contribute to a better knowledge of the demography and population structure in marine fish. In addition, management strategies and conservation goals must consider information on genetic substructuring as well as on life history patterns.
The aim of the study is to provide more detailed knowledge on the genetic variability, demography and population substructuring of European eel by analysing and comparing natural and farmed individuals. Natural eel samples have been obtained in two geographical sites (Netherlands, France) including temporal samples in a short‐scale (within years) and a long‐scale (between years). Simultaneously, farmed glass eels have been grown in two separate batches during one year. Batches have been monitored and genetic samples have been obtained during the year.
A combination of selection‐sensitive (allozymes) and selection‐neutral markers (microsatellites) has been used in the study since selection seems to play an important role in the determination of the quality of future eel spawners. Results suggest a positive correlation between growth and genetic variability since individuals attaining a large length and mass present significant higher heterozygosities.     

A review of glass eel migratory behaviour,sampling techniques and abundance estimates in estuaries: implications for assessing recruitment,local production and exploitation

Recruitment of the three northern hemisphere eel species (European eel Anguilla anguilla, American eel Anguilla rostrata and Japanese eel Anguilla japonica) has reduced significantly over the past thirty-five years. The stock of the European eel is described as being outside safe biological limits, with urgent action required by European Union Member States to assist recovery of the panmictic stock. Stock recruitment models and estimates of silver eel output from a river catchment are strongly influenced by the degree of certainty in estimating key population parameters of each life history stage. Therefore, management decisions aimed at enhancing eel populations rely on sound scientific evidence, based upon a fundamental understanding of the complex anguillid eel life cycle. This review paper focuses on the estuarine entry phase of the eel life cycle and synthesises the current scientific knowledge with regard to glass eel migratory behaviour, sampling methods and abundance estimates within estuaries. Although the behavioural and environmental processes modulating glass eel migration patterns are reasonably well understood, site specific factors play a significant role in determining fine scale distribution patterns at an individual estuary level. Given the large resource commitment required to adequately sample this key life history stage, behavioural studies of migration patterns on a local scale are crucially important to aid the design of robust sampling programmes aimed at quantifying seasonal abundance and annual recruitment.     

The changing times of Europe's largest remaining commercially harvested population of eel Anguilla anguilla L.

This study quantifies the processes involved in regulating the European eel population of Lough Neagh, a lake in Northern Ireland. The relationship between glass eel input and silver eel output for the 1923–1997 cohorts was best described by a Beverton–Holt stock recruitment model. Glass eel input time series was not complete and was thus derived from the relationship between catches elsewhere in Europe and Lough Neagh, together with the addition of stocked glass eel. Silver eel output was the sum of silver eel escapement, catch and yellow eel catch converted to silver eel equivalents. Natural mortality increased with glass eel density, ranging from 0.017 to 0.142 year⁻¹. The mean carrying capacity increased from ≈3.25 M silver eels (≈26 kg ha⁻¹) for the 1923–1943 cohorts to ≈5.0 M (≈40 kg ha⁻¹) for the 1948–1971 cohorts before regressing back to ≈3.25 M. The total silver eel output was highest during the late 1970s/early 1980s at 35–45 kg ha⁻¹ year⁻¹ and lowest during the early years of the 20th century and is currently at 10–15 kg ha⁻¹ year⁻¹. The findings are discussed in relation to (a) the ecological changes that have occurred within the lough, associated with eutrophication and the introduction of roach (Rutilus rutilus L.), and (b) the decline of the wider European eel stock across its distribution range. The findings from this study have relevance for the wider management of the European eel stock.     

Matching effort to threat: Strategies to increase the scale and effectiveness of revegetation in southern Australia

The past 30 years of restoration activities in Australia has been mere cautious fiddling in the face of continental‐wide native habitat loss, fragmentation and degradation. A fundamental principle of conservation is to address threats at the scale of the threatening processes. This is still not happening for two reasons: we do not know how to effectively restore at scale, and if we did, there is no demand because it does not pay. The first problem of developing the technologies needed for large‐scale revegetation will largely be solved if we collectively demand revegetation at scale. Such a scale of demand by Australian governments (taxpayers) is only likely if a permanent Natural Heritage Trust is created for long‐term funding complemented by a price on carbon pollution. That will take a lot of political will. The other big opportunity is to create demand for large‐scale revegetation cofunded by farmers to improve their farm's long‐term productivity, resilience and economic viability. This requires sustained R&D supported by novel partnerships with the massive Australian agricultural market. Native vegetation must move from the margins to the mainstream if scale is to be achieved.     

All roads lead to home: panmixia of European eel in the Sargasso Sea

European eels (Anguilla anguilla) spawn in the remote Sargasso Sea in partial sympatry with American eels (Anguilla rostrata), and juveniles are transported more than 5000 km back to the European and North African coasts. The two species have been regarded as classic textbook examples of panmixia, each comprising a single, randomly mating population. However, several recent studies based on continental samples have found subtle, but significant, genetic differentiation, interpreted as geographical or temporal heterogeneity between samples. Moreover, European and American eels can hybridize, but hybrids have been observed almost exclusively in Iceland, suggesting hybridization in a specific region of the Sargasso Sea and subsequent nonrandom dispersal of larvae. Here, we report the first molecular population genetics study based on analysis of 21 microsatellite loci in larvae of both Atlantic eel species sampled directly in the spawning area, supplemented by analysis of European glass eel samples. Despite a clear East-West gradient in the overlapping distribution of the two species in the Sargasso Sea, we only observed a single putative hybrid, providing evidence against the hypothesis of a wide marine hybrid zone. Analyses of genetic differentiation, isolation by distance, isolation by time and assignment tests provided strong evidence for panmixia in both the Sargasso Sea and across all continental samples of European eel after accounting for the presence of sibs among newly hatched larvae. European eel has declined catastrophically, and our findings call for management of the species as a single unit, necessitating coordinated international conservation efforts.     

Effects of long‐term grazing management on sand dune vegetation of high conservation interest

Question: Can long‐term grazing management maintain and restore species‐rich sand dune plant communities within a sand dune site of high conservation interest? Location: Newborough Warren, North Wales, UK. Methods: Vegetation changes that occurred between 1987 and 2003, subsequent to grazing by domestic livestock being introduced to the site after decades with little or no stock grazing, were analysed using data collected from permanent monitoring quadrats over a 16‐year period. Results: At the plant community level, grazing brought about a shift from a tall‐grass dominated, species‐poor community to a more species‐rich community in the dry dunes, but did not change community type in dune slacks. However, at the species level, grazing enhanced the abundance of some desired perennial, annual and biennial species, graminoids and bryophytes in both habitat types. The increased frequency of positive indicator species for habitat condition suggests that grazing was beneficial for species of conservation interest. Ellenberg nitrogen (N) values decreased after grazing in dry habitats but showed no long‐term change independent of grazing, suggesting no increase in site fertility over the study period. Surprisingly, light (L) values also decreased in the dry dunes after grazing. Conclusions: Long‐term grazing management can play an important role for the conservation of dune communities and associated species. Because of its positive effects on species diversity, plant communities and habitat condition in sand dunes, livestock grazing is recommended for conservation management.     

Decline of North Atlantic eels: a fatal synergy?

Panmictic species pose particular problems for conservation because their welfare can be addressed effectively only on a global scale. We recently documented by means of microsatellite analysis that the European eel (Anguilla anguilla) is not panmictic but instead shows genetic isolation by distance. In this study, we extended the analysis to the American eel (A. rostrata) by applying identical analytical procedures and statistical power. Results obtained for the American eel were in sharp contrast with those obtained for the European eel: the null hypothesis of panmixia could not be rejected, and no isolation by distance was detected. This implies that the species must be managed as a single population. Using Bayesian statistics, we also found that the effective population sizes for both species were surprisingly low and that the populations had undergone severe contractions, most probably during the Wisconsinan glaciation. The apparent sensitivity of eels to climatic changes affecting the strength and position of the Gulf Stream 20,000 years ago is particularly worrying, given the effects of the ongoing global warming on the North Atlantic climate. Moreover, additional short-term stresses such as surging glass eel prizes, overfishing and lethal parasitic infections negatively affect eel population size. The fascinating transatlantic migration and life cycle of Atlantic eels is also their Achilles' heel as these negative short- and long-term effects will probably culminate in a fatal synergy if drastic conservation measures are not implemented to protect these international biological resources.     

A synthesis of the ecological processes influencing variation in life history and movement patterns of American eel: towards a global assessment

American eel, Anguilla rostrata, is a catadromous fish that spawns in the Sargasso Sea and migrates to coastal waters and freshwater systems ranging from Greenland down the Atlantic coast to South America and has been regarded as comprising a panmictic population. American eel is in decline across much of its range. Research and management is primarily conducted at local to regional scales, yielding inconsistent research results and management recommendations that may be inhibited by large-scale processes. We review the research on American eel ecology demonstrating that its variable life history and movement patterns can be explained based on: (1) latitudinal productivity gradients; (2) ideal free habitat selection; (3) conditional evolutionarily stable life history strategies; (4) size at arrival to the coast (correlated with distance from the spawning grounds); and, (5) temperature variance and annual degree-day effects on somatic growth. Using these ecological processes, we outline how local and large-scale effects on American eel dynamics can be integrated in a panmictic (or quasi-panmictic) modelling framework to enable defensible predictions of population responses to anthropogenic and oceanic phenomena. Due to its widespread distribution and existing knowledge gaps, the conservation and management of American eel will require international cooperation.     

Assessing Extinction Risk in Small Metapopulations of Golden‐headed Lion Tamarins (Leontopithecus chrysomelas) in Bahia State,Brazil

Golden‐headed lion tamarins (GHLTs; Leontopithecus chrysomelas) are endangered primates endemic to the Brazilian Atlantic Forest, where loss of forest and its connectivity threaten species survival. Understanding the role of habitat availability and configuration on population declines is critical for guiding proactive conservation for this, and other, endangered species. We conducted population viability analysis to assess vulnerability of ten GHLT metapopulations to habitat loss and small population size. Seven metapopulations had a low risk of extirpation (or local extinction) over the next 100 years assuming no further forest loss, and even small populations could persist with immediate protection. Three metapopulations had a moderate/high risk of extirpation, suggesting extinction debt may be evident in parts of the species’ range. When deforestation was assumed to continue at current rates, extirpation risk significantly increased while abundance and genetic diversity decreased for all metapopulations. Extirpation risk was significantly negatively correlated with the size of the largest patch available to metapopulations, underscoring the importance of large habitat patches for species persistence. Finally, we conducted sensitivity analysis using logistic regression, and our results showed that local extinction risk was sensitive to percentage of females breeding, adult female mortality, and dispersal rate and survival; conservation or research programs that target these aspects of the species’ biology/ecology could have a disproportionately important impact on species survival. We stress that efforts to protect populations and tracts of habitat of sufficient size throughout the species’ distribution will be important in the near‐term to protect the species from continuing decline and extinction.     

Can intrinsic factors explain population declines in North American breeding shorebirds? A comparative analysis

Many shorebirds that breed in North America are declining. These trends reflect global patterns in shorebird populations. Here we ask what factors make some shorebird species more prone to decline than others. Specifically, we test the influence of migratory behaviour (route and distance), biogeography (population size and range), life history (body size, clutch size) and sexual selection (social mating system and testis size) on population trends in North American breeding shorebirds. Using phylogenetic comparative methods, we show that species that migrate across continental North America are more prone to decline than species that do not. Our finding that continental migrants are associated with population decline indicates that intrinsic factors may play an important role in predisposing a species to decline. Previous studies within the class Aves have failed to identify migration route as a correlate of decline or extinction risk. Two other intrinsic factors (oceanic migrants and threats on the non-breeding grounds) were also important in our overall models, although neither was significant alone. The moderate explanatory power of our variables indicates that other factors are also important for explaining shorebird declines. We suggest that contemporary threats, most notably habitat loss and degradation at migratory stopover sites, are likely to be important.     

Effects of climate warming on polar bears: a review of the evidence

Climate warming is causing unidirectional changes to annual patterns of sea ice distribution, structure, and freeze‐up. We summarize evidence that documents how loss of sea ice, the primary habitat of polar bears (Ursus maritimus), negatively affects their long‐term survival. To maintain viable subpopulations, polar bears depend on sea ice as a platform from which to hunt seals for long enough each year to accumulate sufficient energy (fat) to survive periods when seals are unavailable. Less time to access to prey, because of progressively earlier breakup in spring, when newly weaned ringed seal (Pusa hispida) young are available, results in longer periods of fasting, lower body condition, decreased access to denning areas, fewer and smaller cubs, lower survival of cubs as well as bears of other age classes and, finally, subpopulation decline toward eventual extirpation. The chronology of climate‐driven changes will vary between subpopulations, with quantifiable negative effects being documented first in the more southerly subpopulations, such as those in Hudson Bay or the southern Beaufort Sea. As the bears' body condition declines, more seek alternate food resources so the frequency of conflicts between bears and humans increases. In the most northerly areas, thick multiyear ice, through which little light penetrates to stimulate biological growth on the underside, will be replaced by annual ice, which facilitates greater productivity and may create habitat more favorable to polar bears over continental shelf areas in the short term. If the climate continues to warm and eliminate sea ice as predicted, polar bears will largely disappear from the southern portions of their range by mid‐century. They may persist in the northern Canadian Arctic Islands and northern Greenland for the foreseeable future, but their long‐term viability, with a much reduced global population size in a remnant of their former range, is uncertain.     

Context‐dependent conservation of the cavity‐nesting European Roller

To maximize the effectiveness of conservation interventions, it is crucial to have an understanding of how intraspecific variation determines the relative importance of potential limiting factors. For bird populations, limiting factors include nest‐site availability and foraging resources, with the former often addressed through the provision of artificial nestboxes. However, the effectiveness of artificial nestboxes depends on the relative importance of nest‐site vs. foraging resource limitations. Here, we investigate factors driving variation in breeding density, nestbox occupation and productivity in two contrasting study populations of the European Roller Coracias garrulus, an obligate cavity‐nesting insectivorous bird. Breeding density was more than four times higher at the French study site than at the Latvian site, and there was a positive correlation between breeding density (at the 1‐km² scale) and nest‐site availability in France, whereas there was a positive correlation between breeding density and foraging resource availability in Latvia. Similarly, the probability of a nestbox being occupied increased with predicted foraging resource availability in Latvia but not in France. We detected no positive effect of foraging resource availability on productivity at either site, with most variation in breeding success driven by temporal effects: a seasonal decline in France and strong interannual fluctuations in Latvia. Our results indicate that the factors limiting local breeding density can vary across a species' range, resulting in different conservation priorities. Nestbox provisioning is a sufficient short‐term conservation solution at our French study site, where foraging resources are typically abundant, but in Latvia the restoration of foraging habitat may be more important.     

Long‐term decline despite conservation efforts questions Eurasian Stone‐curlew population viability in intensive farmlands

Agricultural intensification over the past decades has led to a generalized decline in farmland biodiversity. Farmland birds are particularly exposed to rapid changes in habitat and reduced food resources or availability. Understanding how farmland specialists can be preserved and their populations enhanced are major challenges for this century. Based on a long‐term (19‐year) study of a Eurasian Stone‐curlew Burhinus oedicnemus population, we estimated the demographic parameters, including clutch size, egg volume, hatching success, survival rate and apparent population size. Demographic rates found for this French population were, on average, comparable to those found elsewhere in Europe. However, all demographic parameters showed negative trends, including a dramatic decline in the local population (26% decline over 14 years) and a 10% decline in adult survival rate over 11 years. Such a long‐term decline, despite on‐going conservation efforts, calls into question the overall sustainability of arable Stone‐curlew populations. We infer some of the possible causes of this decline, in particular food shortage, and discuss how this pattern could be reversed through conservation measures applicable at very large spatial scales.     

The global decline of freshwater megafauna

Freshwater ecosystems are among the most diverse and dynamic ecosystems on Earth. At the same time, they are among the most threatened ecosystems but remain underrepresented in biodiversity research and conservation efforts. The rate of decline of vertebrate populations is much higher in freshwaters than in terrestrial or marine realms. Freshwater megafauna (i.e., freshwater animals that can reach a body mass ≥30 kg) are intrinsically prone to extinction due to their large body size, complex habitat requirements and slow life‐history strategies such as long life span and late maturity. However, population trends and distribution changes of freshwater megafauna, at continental or global scales, remain unclear. In the present study, we compiled population data of 126 freshwater megafauna species globally from the Living Planet Database and available literature, and distribution data of 44 species inhabiting Europe and the United States from literature and databases of the International Union for Conservation of Nature and NatureServe. We quantified changes in population abundance and distribution range of freshwater megafauna species. Globally, freshwater megafauna populations declined by 88% from 1970 to 2012, with the highest declines in the Indomalaya and Palearctic realms (?99% and ?97%, respectively). Among taxonomic groups, mega‐fishes exhibited the greatest global decline (?94%). In addition, freshwater megafauna experienced major range contractions. For example, distribution ranges of 42% of all freshwater megafauna species in Europe contracted by more than 40% of historical areas. We highlight the various sources of uncertainty in tracking changes in populations and distributions of freshwater megafauna, such as the lack of monitoring data and taxonomic and spatial biases. The detected trends emphasize the critical plight of freshwater megafauna globally and highlight the broader need for concerted, targeted and timely conservation of freshwater biodiversity.     

Contrasting patterns of sexually selected traits in Mediterranean and continental populations of European mouflon

The expression of sexually selected traits in highly dimorphic ungulates may be influenced by environmental quality. Variations in habitat conditions can impose different constraints on the allocation of energy resources to male life‐history traits, and possibly alter the female preferences for specific features. Here, we compared the horn growth patterns in male European mouflon Ovis aries musimon living in different habitats (Mediterranean vs. continental) but sharing a common genetic origin. We hypothesized that the expression of sexually selected traits such as horn development should be promoted in more favorable habitat conditions (i.e., Mediterranean). Using linear mixed models on data retrieved from individuals harvested under the same hunting regime, we found longer horns and greater individual variance in horn segment length in the Mediterranean population than in the continental one. Furthermore, Mediterranean rams showed no evidence of compensatory horn growth, as opposed to the continental rams. Unexpectedly, horn base circumference was greater in the continental habitat than in the Mediterranean one. The overall results suggest different patterns of investment in horns in the two populations, with seemingly stronger pressure and consequences of sexual selection on mouflon rams living in more favorable environments. Although the role of hunters' selectivity cannot be excluded a priori, our data suggest that the differences in the expression of sexually selected traits in our study populations may be influenced by environmental conditions. Because sexual selection can impose substantial fitness costs on individuals, further investigations on the trade‐offs between reproduction and survival would improve our understanding of the dynamics of mouflon populations living in different environmental conditions.