High variability in patterns of population decline: the importance of local processes in species extinctions

A fundamental goal of conservation science is to improve conservation practice. Understanding species extinction patterns has been a central approach towards this objective. However, uncertainty remains about the extent to which species-level patterns reliably indicate population phenomena at the scale of local sites, where conservation ultimately takes place. Here, we explore the importance of both species- and site-specific components of variation in local population declines following habitat disturbance, and test a suite of hypotheses about their intrinsic and extrinsic drivers. To achieve these goals, we analyse an unusually detailed global dataset for species responses to habitat disturbance, namely primates in timber extraction systems, using cross-classified generalized linear mixed models. We show that while there are consistent differences in the severity of local population decline between species, an equal amount of variation also occurs between sites. The tests of our hypotheses further indicate that a combination of biological traits at the species level, and environmental factors at the site level, can help to explain these patterns. Specifically, primate populations show a more marked decline when the species is characterized by slow reproduction, high ecological requirements, low ecological flexibility and small body size; and when the local environment has had less time for recovery following disturbance. Our results demonstrate that individual species show a highly heterogeneous, yet explicable, pattern of decline. The increased recognition and elucidation of local-scale processes in species declines will improve our ability to conserve biodiversity in the future.     

The uncertain blitzkrieg of Pleistocene megafauna

We investigated, using meta‐analysis of empirical data and population modelling, plausible scenarios for the cause of late Pleistocene global mammal extinctions. We also considered the rate at which these extinctions may have occurred, providing a test of the so‐called ‘blitzkrieg’ hypothesis, which postulates a rapid, anthropogenically driven, extinction event. The empirical foundation for this work was a comprehensive data base of estimated body masses of mammals, comprising 198 extinct and 433 surviving species > 5 kg, which we compiled through an extensive literature search. We used mechanistic population modelling to simulate the role of human hunting efficiency, meat off‐take, relative naivety of prey to invading humans, variation in reproductive fitness of prey and deterioration of habitat quality (due to either anthropogenic landscape burning or climate change), and explored the capacity of different modelling scenarios to recover the observed empirical relationship between body mass and extinction proneness. For the best‐fitting scenarios, we calculated the rate at which the extinction event would have occurred. All of the modelling was based on sampling randomly from a plausible range of parameters (and their interactions), which affect human and animal population demographics. Our analyses of the empirical data base revealed that the relationship between body mass and extinction risk relationship increases continuously from small‐ to large‐sized animals, with no clear ‘megafaunal’ threshold. A logistic ancova model incorporating body mass and geography (continent) explains 92% of the variation in the observed extinctions. Population modelling demonstrates that there were many plausible mechanistic scenarios capable of reproducing the empirical body mass–extinction risk relationship, such as specific targeting of large animals by humans, or various combinations of habitat change and opportunistic hunting. Yet, given the current imperfect knowledge base, it is equally impossible to use modelling to isolate definitively any single scenario to explain the observed extinctions. However, one universal prediction, which applied in all scenarios in which the empirical distribution was correctly predicted, was for the extinctions to be rapid following human arrival and for surviving fauna to be suppressed below their pre‐‘blitzkrieg’ densities. In sum, human colonization in the late Pleistocene almost certainly triggered a ‘blitzkrieg’ of the ‘megafauna’, but the operational details remain elusive.     

Multiple drivers of decline in the global status of freshwater crayfish (Decapoda: Astacidea)

Rates of biodiversity loss are higher in freshwater ecosystems than in most terrestrial or marine ecosystems, making freshwater conservation a priority. However, prioritization methods are impeded by insufficient knowledge on the distribution and conservation status of freshwater taxa, particularly invertebrates. We evaluated the extinction risk of the world''s 590 freshwater crayfish species using the IUCN Categories and Criteria and found 32% of all species are threatened with extinction. The level of extinction risk differed between families, with proportionally more threatened species in the Parastacidae and Astacidae than in the Cambaridae. Four described species were Extinct and 21% were assessed as Data Deficient. There was geographical variation in the dominant threats affecting the main centres of crayfish diversity. The majority of threatened US and Mexican species face threats associated with urban development, pollution, damming and water management. Conversely, the majority of Australian threatened species are affected by climate change, harvesting, agriculture and invasive species. Only a small proportion of crayfish are found within the boundaries of protected areas, suggesting that alternative means of long-term protection will be required. Our study highlights many of the significant challenges yet to come for freshwater biodiversity unless conservation planning shifts from a reactive to proactive approach.     

Evolutionary age and risk of extinction in the global avifauna

Species at high risk of extinction are not distributed at random among higher taxa. Here we demonstrate that there is a positive relationship between the proportion of species in a taxon which are considered to be threatened and the evolutionary age of that taxon, both for the global avifauna and the avifauna of the New World. The potential mechanisms and consequences of the relationship are examined.     

Common pattern of population decline for freshwater cetacean species in deteriorating habitats

1. Freshwater cetacean species, including the baiji (Lipotes vexillifer), Amazon River dolphin (Inia geoffrensis), Ganges/Indus River dolphins (Platanista spp.) and Yangtze finless porpoise (Neophocaena asiaeorientalis asiaeorientalis), apex predators in megariver ecosystems, face serious challenges owing to the deterioration of habitat quality. 2. We simulated population change of four freshwater cetacean species under increasing habitat deterioration. Carrying capacity (K) was used to represent the habitat quality, and a logistic model was used to describe the rate of habitat deterioration (dK). 3. An individual‐based Leslie matrix model showed that population declines and extinctions in freshwater cetaceans under increasing habitat deterioration exhibit a consistent pattern irrespective of the initial level of K or population size. When dK is low, population abundance fluctuates stochastically around initial K, but a rapid increase in dK is accompanied by a sharp population decline, with a residual population ultimately declining continuously to extinction. 4. Simulations show that traditional census survey techniques used in cetacean species are unlikely to detect early signs of population decline before a critical level is reached. 5. Empirical data of the likely extinction of baiji strongly agree with our simulation exercise, implying that extinction of other freshwater cetacean species may occur sooner than previously considered. Hence, precautionary approaches for habitat restoration and landscape management should be implemented before freshwater cetacean population declines are detected, and ideally, before habitat quality begins to deteriorate.     

Population and geographic range dynamics: implications for conservation planning

Continuing downward trends in the population sizes of many species, in the conservation status of threatened species, and in the quality, extent and connectedness of habitats are of increasing concern. Identifying the attributes of declining populations will help predict how biodiversity will be impacted and guide conservation actions. However, the drivers of biodiversity declines have changed over time and average trends in abundance or distributional change hide significant variation among species. While some populations are declining rapidly, the majority remain relatively stable and others are increasing. Here we dissect out some of the changing drivers of population and geographic range change, and identify biological and geographical correlates of winners and losers in two large datasets covering local population sizes of vertebrates since 1970 and the distributions of Galliform birds over the last two centuries. We find weak evidence for ecological and biological traits being predictors of local decline in range or abundance, but stronger evidence for the role of local anthropogenic threats and environmental change. An improved understanding of the dynamics of threat processes and how they may affect different species will help to guide better conservation planning in a continuously changing world.     

Freshwater megafauna diversity: Patterns,status and threats

Aim

Freshwater megafauna remain underrepresented in research and conservation, despite a disproportionately high risk of extinction due to multiple human threats. Therefore, our aims are threefold; (i) identify global patterns of freshwater megafauna richness and endemism, (ii) assess the conservation status of freshwater megafauna and (iii) demonstrate spatial and temporal patterns of human pressure throughout their distribution ranges.

Location

Global.

Methods

We identified 207 extant freshwater megafauna species, based on a 30 kg weight threshold, and mapped their distributions using HydroBASINS subcatchments (level 8). Information on conservation status and population trends for each species was extracted from the IUCN Red List website. We investigated human impacts on freshwater megafauna in space and time by examining spatial congruence between their distributions and human pressures, described by the Incident Biodiversity Threat Index and Temporal Human Pressure Index.

Results

Freshwater megafauna occur in 76% of the world’s main river basins (level 3 HydroBASINS), with species richness peaking in the Amazon, Congo, Orinoco, Mekong and Ganges‐Brahmaputra basins. Freshwater megafauna are more threatened than their smaller counterparts within the specific taxonomic groups (i.e., fishes, mammals, reptiles and amphibians). Out of the 93 freshwater megafauna species with known population trends, 71% are in decline. Meanwhile, IUCN Red List assessments reported insufficient or outdated data for 43% of all freshwater megafauna species. Since the early 1990s, human pressure has increased throughout 63% of their distribution ranges, with particularly intense impacts occurring in the Mekong and Ganges‐Brahmaputra basins.

Main conclusions

Freshwater megafauna species are threatened globally, with intense and increasing human pressures occurring in many of their biodiversity hotspots. We call for research and conservation actions for freshwater megafauna, as they are highly sensitive to present and future pressures including a massive boom in hydropower dam construction in their biodiversity hotspots.

     

Doomed to die? Predicting extinction risk in the true hawks Accipitridae

One of the most important tasks in conservation biology is identifying species at risk from extinction and establishing the most likely factors influencing this risk. Here, we consider an ecologically well-defined, monophyletic group of organisms, the true hawks of the family Accipitridae, which are not only among the most studied, but also contain some of the rarest bird species in the world. We investigate which intrinsic and extrinsic factors, covering morphology, life history and ecology, covary with International Union for the Conservation of Nature and Natural Resources threat status, as well as global population size and geographic range size. By decomposing threat status into population size and range size, we test whether any factors are generally important: we found that species with less habitat specialization, a larger clutch size and more plumage polymorphism were associated with lower extinction risk and larger population and range sizes. Species with special habitat requirements might be less capable of dealing with habitat transformation and fragmentation, while species with small clutch sizes might not be able to reverse population declines. Plumage polymorphism might indicate the size of the species' gene pool and could be a good marker of extinction risk. The analyses also emphasized that no single factor is likely to be sufficient when predicting the threat of extinction.     

A method for the estimation of the global population sizes of plant species – the Area-abundance-index

The aim of this study is to establish a practical index that considers both the size of the global range, and the mean relative abundance of species within their range. Detailed general distribution maps provide the basis for a classification of ranges into nine size categories. The abundance data are arranged into five categories, ranging from very rare to very common. These categories are derived directly from floristic literature. The Area-abundance-index is calculated using an empirical formula, i.e. by the addition of the mean relative global abundance and the range size category number. Values of the index range from 2 (very rare and range ≤10 km²) to 13 (very common throughout and range > 10⁷ km²). The main advantage of the index is that species become comparable in terms of their global population sizes. Frequently, regional Red Lists contain species that are common elsewhere and occupy wide areas, or may not include locally abundant species that occupy only very small geographical ranges. The application of the Area-abundance-index for the prioritizing of species within Red List categories and, hence, a varying assignment of conservational efforts, is discussed. Furthermore, the application of the index on a local scale, and the regional responsibility for species conservation or monitoring are discussed.     

The Eclipse of Species Ranges

This paper distinguishes four recognisably different geographical processes in principle causing species to die out. One of these processes, the one we dub “range eclipse”, holds that one range expands at the expense of another one, thereby usurping it. Channell and Lomolino (2000a, Journal of Biogeography 27: 169–179; 2000b, Nature 403: 84–87; see also Lomolino and Channell, 1995, Journal of Mammalogy 76: 335–347) measured the course of this process in terms of the proportion of the total range remaining in its original centre, thereby essentially assuming a homogeneous distribution of animals over the range. However, part of their measure seems mistaken. By giving a general, analytical formulation of eclipsing ranges, we estimate the exact course of this process. Also, our formulation does not partition a range into two spatially equal parts, its core and its edge, but it assumes continuity. For applying this model to data on the time evolution of species, individual time series should be available for each of them. For practical purposes we give an alternative way of plotting and interpreting such time series. Our approach, being more sensitive than Channell and Lomolino’s, gives a less optimistic indication of range eclipses than theirs once these have started.     

Analysis of factors implicated in the recent decline of Australia's mammal fauna

Aim To assess whether eight factors thought to be involved in the extinction process can explain the pattern of recent decline in Australia's mammal fauna. Location Australia. Methods We compiled the first comprehensive lists of mammal species extant at the time of European settlement in each of Australia's 76 mainland regions, and assigned a current conservation status to each species in each region to derive an index of faunal attrition. We then sought to explain the observed region‐to‐region variation in attrition (the dependent variable) by building a series of models using variables representing the eight factors. Results A strong geographically based pattern of attrition emerged, with faunal losses being greatest in arid regions and least in areas of high rainfall. The Akaike information criterion showed support for one model that explained 93% of the region‐to‐region variation in attrition. Its six variables all made independent contributions towards explaining the observed variation. Two were environmental variables, namely mean annual rainfall (a surrogate for regional productivity) and environmental change (a measure of post‐European disturbance). The other four were faunal variables, namely phylogenetic similarity, body‐weight distribution, area (as a surrogate for extent of occurrence), and proportion of species that usually shelter on the ground (rather than in rock piles, burrows or trees). Main conclusions In combination with historical evidence, the analysis provides an explicit basis for setting priorities among regions and species. It also shows that the long‐term recovery of populations of many species of Australian mammals will require introduced predator suppression as well as extensive habitat management that includes controlling feral herbivores. Specifically, habitat management should restore aspects of productivity relevant to the types of species at risk and ensure the continual availability of suitable refuges from physiological stressors.     

Projected range contractions of montane biodiversity under global warming

Mountains, especially in the tropics, harbour a unique and large portion of the world''s biodiversity. Their geographical isolation, limited range size and unique environmental adaptations make montane species potentially the most threatened under impeding climate change. Here, we provide a global baseline assessment of geographical range contractions and extinction risk of high-elevation specialists in a future warmer world. We consider three dispersal scenarios for simulated species and for the world''s 1009 montane bird species. Under constrained vertical dispersal (VD), species with narrow vertical distributions are strongly impacted; at least a third of montane bird diversity is severely threatened. In a scenario of unconstrained VD, the location and structure of mountain systems emerge as a strong driver of extinction risk. Even unconstrained lateral movements offer little improvement to the fate of montane species in the Afrotropics, Australasia and Nearctic. Our results demonstrate the particular roles that the geography of species richness, the spatial structure of lateral and particularly vertical range extents and the specific geography of mountain systems have in determining the vulnerability of montane biodiversity to climate change. Our findings confirm the outstanding levels of biotic perturbation and extinction risk that mountain systems are likely to experience under global warming and highlight the need for additional knowledge on species'' vertical distributions, dispersal and adaptive capacities.     

Comparison of methods for detecting bottlenecks from microsatellite loci

This paper describes simulation tests to compare methods for detecting recent bottlenecks using microsatellite data. This study considers both type I error (detecting a bottleneck when there wasn’t one) and type II error (failing to detect a bottleneck when there was one) under a variety of scenarios. The two most promising methods were the range in allele size conditioned on the number of alleles, M _k , and heterozygosity given the number of alleles, H _k , under a two-phase mutation model; in most of the simulations one of these two methods had the lowest type I and type II error relative to other methods. M _k was the method most likely to correctly identify a bottleneck when a bottleneck lasted several generations, the population had made a demographic recovery, and mutation rates were high or pre-bottleneck population sizes were large. On the other hand H _k was most likely to correctly identify a bottleneck when a bottleneck was more recent and less severe and when mutation rates were low or pre-bottleneck population sizes were small. Both methods were prone to type I errors when assumptions of the model were violated, but it may be easier to design a conservative heterozygosity test than a conservative ratio test.     

Biogeographical basis of recent phenotypic divergence among birds: a global study of subspecies richness

Theory predicts that biogeographic factors should play a central role in promoting population divergence and speciation. Previous empirical studies into biogeography and diversification have been relatively restricted in terms of the geographical area, phylogenetic scope, and the range of biogeographic factors considered. Here we present a global analysis of allopatric phenotypic divergence (measured as subspecies richness) across more than 9600 bird species. The main aim of this study was to examine the extent to which biogeographical factors can explain patterns of phenotypic divergence. Analysis of the taxonomic distribution of subspecies among species suggests that subspecies formation and extinction have occurred at a considerably faster rate than has species formation. However, the observed distribution departs from the expectation under a random birth-death model of diversification. Across 19 phylogenetic trees, we find no significant linear relationship between species age and subspecies richness, implying that species age is a poor predictor of subspecies richness. Both subspecies richness and subspecies diversification rate are found to exhibit low phylogenetic signal, meaning that closely related species do not tend to possess similar numbers of subspecies. As predicted by theory, high subspecies richness was associated with large breeding range size, island dwelling, inhabitation of montane regions, habitat heterogeneity, and low latitude. Of these factors, breeding range size was the variable that explained the most variation. Unravelling whether species that have invaded previously glacial areas have more or fewer subspecies than expected proves to be complicated due to a covariation between the postglacial colonization, latitude, geographic range size, and subspecies richness. However, the effect of postglacial colonization on subspecies richness appears to be small. Mapping the distribution of species' subspecies richness globally reveals geographical patterns that correspond to many of the predictions of the statistical models, but may also reflect geographical variation in taxonomic practice. Overall, we demonstrate that biogeographic models can explain about 30% of the global variation in subspecies richness in birds.     

Explaining the global pattern of protected area coverage: relative importance of vertebrate biodiversity, human activities and agricultural suitability

Aim Twelve per cent of the Earth’s terrestrial surface is covered by protected areas, but neither these areas nor the biodiversity they contain are evenly distributed spatially. To guide future establishment of protected areas, it is important to understand the factors that have shaped the spatial arrangement of the current protected area system. We used an information‐theoretic approach to assess the ability of vertebrate biodiversity measures, resource consumption and agricultural potential to explain the global coverage pattern of protected areas. Location Global. Methods For each of 762 World Wildlife Fund terrestrial ecoregions of the world, we measured protected area coverage, resource consumption, terrestrial vertebrate species richness, number of endemic species, number of threatened species, net primary production, elevation and topographic heterogeneity. We combined these variables into 39 a priori models to describe protected area coverage at the global scale, and for six biogeographical realms. Using the Akaike information criterion and Akaike weights, we identified the relative importance and influence of each variable in describing protected area coverage. Results Globally, the number of endemic species was the best variable describing protected area coverage, followed by the number of threatened species. Species richness and resource consumption were of moderate importance and agricultural potential had weak support for describing protected area coverage at a global scale. Yet, the relative importance of these factors varied among biogeographical realms. Measures of vertebrate biodiversity (species richness, endemism and threatened species) were among the most important variables in all realms, except the Indo‐Malayan, but had a wide range of relative importance and influence. Resource consumption was inversely related to protected area coverage across all but one realm (the Palearctic), most strongly in the Nearctic realm. Agricultural potential, despite having little support in describing protected area coverage globally, was strongly and positively related to protection in the Palearctic and Neotropical realms, as well as in the Indo‐Malayan realm. The Afrotropical, Indo‐Malayan and Australasian realms showed no clear, strong relationships between protected area coverage and the independent variables. Main conclusions Globally, the existing protected area network is more strongly related to biodiversity measures than to patterns of resource consumption or agricultural potential. However, the relative importance of these factors varies widely among the world’s biogeographical realms. Understanding the biases of the current protected area system may help to correct for them as future protected areas are added to the global network.     

The key elements of a comprehensive global mammal conservation strategy

A global strategy is necessary to achieve the level of coordination, synergy and therefore optimization of resources to achieve the broad goal of conserving mammals worldwide. Key elements for the development of such a strategy include: an institutional subject that owns the strategy; broad conservation goals, quantitative targets derived from them and appropriate indicators; data on the distribution of species, their threats, the cost-effectiveness of conservation actions; and a set of methods for the identification of conservation priorities. Previous global mammal research investigated phylogeny, extinction risk, and the species and areas that should be regarded as global conservation priorities. This theme issue presents new key elements: an updated Red List Index, a new list of evolutionarily distinct and globally endangered species, new high-resolution mammal distribution models, a global connectivity analysis and scenarios of future mammal distribution based on climate and land-cover change. Area prioritization schemes account for mammalian phylogeny, governance and cost-benefit of measures to abate habitat loss. Three discussion papers lay the foundations for the development of a global unifying mammal conservation strategy, which should not be further deterred by the knowledge gaps still existing.     

Quantifying the extinction vortex

We developed a database of 10 wild vertebrate populations whose declines to extinction were monitored over at least 12 years. We quantitatively characterized the final declines of these well-monitored populations and tested key theoretical predictions about the process of extinction, obtaining two primary results. First, we found evidence of logarithmic scaling of time-to-extinction as a function of population size for each of the 10 populations. Second, two lines of evidence suggested that these extinction-bound populations collectively exhibited dynamics akin to those theoretically proposed to occur in extinction vortices. Specifically, retrospective analyses suggested that a population size of n individuals within a decade of extinction was somehow less valuable to persistence than the same population size was earlier. Likewise, both year-to-year rates of decline and year-to-year variability increased as the time-to-extinction decreased. Together, these results provide key empirical insights into extinction dynamics, an important topic that has received extensive theoretical attention.