Extrinsic versus intrinsic factors in the decline and extinction of Australian marsupials

Recent attempts to explain the susceptibility of vertebrates to declines worldwide have largely focused on intrinsic factors such as body size, reproductive potential, ecological specialization, geographical range and phylogenetic longevity. Here, we use a database of 145 Australian marsupial species to test the effects of both intrinsic and extrinsic factors in a multivariate comparative approach. We model five intrinsic (body size, habitat specialization, diet, reproductive rate and range size) and four extrinsic (climate and range overlap with introduced foxes, sheep and rabbits) factors. We use quantitative measures of geographical range contraction as indices of decline. We also develop a new modelling approach of phylogenetically independent contrasts combined with imputation of missing values to deal simultaneously with phylogenetic structuring and missing data. One extrinsic variable-geographical range overlap with sheep-was the only consistent predictor of declines. Habitat specialization was independently but less consistently associated with declines. This suggests that extrinsic factors largely determine interspecific variation in extinction risk among Australian marsupials, and that the intrinsic factors that are consistently associated with extinction risk in other vertebrates are less important in this group. We conclude that recent anthropogenic changes have been profound enough to affect species on a continent-wide scale, regardless of their intrinsic biology.     

Predicting extinction risk in declining species

What biological attributes predispose species to the risk of extinction? There are many hypotheses but so far there has been no systematic analysis for discriminating between them. Using complete phylogenies of contemporary carnivores and primates, we present, to our knowledge, the first comparative test showing that high trophic level, low population density slow life history and, in particular, small geographical range size are all significantly and independently associated with a high extinction risk in declining species. These traits together explain nearly 50% of the total between-species variation in extinction risk. Much of the remaining variation can be accounted for by external anthropogenic factors that affect species irrespective of their biology.     

Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics

Whereas previous studies have investigated correlates of extinction risk either at global or regional scales, our study explicitly models regional effects of anthropogenic threats and biological traits across the globe. Using phylogenetic comparative methods with a newly-updated supertree of 5020 extant mammals, we investigate the impact of species traits on extinction risk within each WWF ecoregion. Our analyses reveal strong geographical variation in the influence of traits on risk: notably, larger species are at higher risk only in tropical regions. We then relate these patterns to current and recent-historical human impacts across ecoregions using spatial modelling. The body–mass results apparently reflect historical declines of large species outside the tropics due to large-scale land conversion. Narrow-ranged and rare species tend to be at high risk in areas of high current human impacts. The interactions we describe between biological traits and anthropogenic threats increase understanding of the processes determining extinction risk.     

Ecological and socio-economic factors affecting extinction risk in parrots

Parrots (Psittaciformes) are among the most threatened bird orders with 28 % (111 of 398) of extant species classified as threatened under IUCN criteria. We confirmed that parrots have a lower Red List Index (higher aggregate extinction risk) than other comparable bird groups, and modeled the factors associated with extinction risk. Our analyses included intrinsic biological, life history and ecological attributes, external anthropogenic threats, and socio-economic variables associated with the countries where the parrot species occur, while we controlled for phylogenetic dependence among species. We found that the likelihood of parrot species being classified as threatened was less for species with larger historical distribution size, but was greater for species with high forest dependency, large body size, long generation time, and greater proportion of the human population living in urban areas in the countries encompassing the parrots’ home ranges. The severity of extinction risk (from vulnerable to critically endangered) was positively related to the per capita gross domestic product (GDP) of the countries of occurrence, endemism to a single country, and lower for species used as pets. A disproportionate number of 16 extinct parrot species were endemic to islands and single countries, and were large bodied, habitat specialists. Agriculture, hunting, trapping, and logging are the most frequent threats to parrots worldwide, with variation in importance among regions. We use multiple methods to rank countries with disproportionately high numbers of threatened parrot species. Our results promote understanding of global and regional factors associated with endangerment in this highly threatened taxonomic group, and will enhance the prioritization of conservation actions.     

Phylogenetic correlates of extinction risk in mammals: species in older lineages are not at greater risk

Phylogenetic information is becoming a recognized basis for evaluating conservation priorities, but associations between extinction risk and properties of a phylogeny such as diversification rates and phylogenetic lineage ages remain unclear. Limited taxon-specific analyses suggest that species in older lineages are at greater risk. We calculate quantitative properties of the mammalian phylogeny and model extinction risk as an ordinal index based on International Union for Conservation of Nature Red List categories. We test for associations between lineage age, clade size, evolutionary distinctiveness and extinction risk for 3308 species of terrestrial mammals. We show no significant global or regional associations, and three significant relationships within taxonomic groups. Extinction risk increases for evolutionarily distinctive primates and decreases with lineage age when lemurs are excluded. Lagomorph species (rabbits, hares and pikas) that have more close relatives are less threatened. We examine the relationship between net diversification rates and extinction risk for 173 genera and find no pattern. We conclude that despite being under-represented in the frequency distribution of lineage ages, species in older, slower evolving and distinct lineages are not more threatened or extinction-prone. Their extinction, however, would represent a disproportionate loss of unique evolutionary history.     

Human impacts and the global distribution of extinction risk

Understanding the global geographical distribution of extinction risk is a key challenge in conservation biology. It remains controversial, however, to what extent areas become threat hotspots simply because of high human impacts or due to predisposing ecological conditions. Limits to the taxonomic and geographical extent, resolution and quality of previously available data have precluded a full global assessment of the relative roles of these factors. Here, we use a new global database on the geographical distributions of birds on continents and continental islands to show that, after controlling for species richness, the best predictors of the global pattern of extinction risk are measures of human impact. Ecological gradients are of secondary importance at a global scale. The converse is true for individual biogeographic realms, within which variation in human impact is reduced and its influence on extinction risk globally is therefore underestimated. These results underline the importance of a global perspective on the mechanisms driving spatial patterns of extinction risk, and the key role of anthropogenic factors in driving the current extinction crisis.     

Anthropogenic, ecological and genetic factors in extinction and conservation

Anthropogenic factors constitute the primary deterministic causes of species declines, endangerment and extinction: land development, overexploitation, species translocations and introductions, and pollution. The primary anthropogenic factors produce ecological and genetic effects contributing to extinction risk. Ecological factors include environmental stochasticity, random catastrophes, and metapopulation dynamics (local extinction and colonization) that are intensified by habitat destruction and fragmentation. Genetic factors include hybridization with nonadapted gene pools, and selective breeding and harvesting. In small populations stochastic factors are especially important, including the ecological factors of Allee effect, edge effects, and demographic stochasticity, and the genetic factors of inbreeding depression, loss of genetic variability, and fixation of new deleterious mutations. All factors affecting extinction risk are expressed, and can be evaluated, through their operation on population dynamics.     

Behavioral Correlates of Primates Conservation Status: Intrinsic Vulnerability to Anthropogenic Threats

Behavioral traits are likely to influence species vulnerability to anthropogenic threats and in consequence, their risk of extinction. Several studies have addressed this question and have highlighted a correlation between reproductive strategies and different viability proxies, such as introduction success and local extinction risk. Yet, very few studies have investigated the effective impact of social behaviour, and evidence regarding global extinction risk remains scant. Here we examined the effects of three main behavioral factors: the group size, the social and reproductive system, and the strength of sexual selection on global extinction risk. Using Primates as biological model, we performed comparative analysis on 93 species. The conservation status as described by the IUCN Red List was considered as a proxy for extinction risk. In addition, we added previously identified intrinsic factors of vulnerability to extinction, and a measure of the strength of the human impact for each species, described by the human footprint. Our analysis highlighted a significant effect of two of the three studied behavioral traits, group size and social and reproductive system. Extinction risk is negatively correlated with mean group size, which may be due to an Allee effect resulting from the difficulties for solitary and monogamous species to find a partner at low densities. Our results also indicate that species with a flexible mating system are less vulnerable. Taking into account these behavioral variables is thus of high importance when establishing conservation plans, particularly when assessing species relative vulnerability.     

Reproductive failure: a new paradigm for extinction

Extinction was recognized as a scientific fact 200 years ago, although no adequate paradigm has emerged to explain the process. Prevailing theory has focused on ‘cause(s)’ of extinction but has neglected ‘effect’ and ‘mechanism’. These omissions preclude the formulation of a functional paradigm necessary for remedial action in response to the impending anthropogenic mediated, worldwide extinction crisis. The new paradigm is defined as the multi‐generational, attritional loss of reproductive fitness. Stabilizing selection continuously adapts species to specific ecosystems, which often results in highly evolved species prone to extinction when environments shift. Some species survive by tracking the declining palaeoclimates in which they presumably evolved, often becoming relicts prior to extinction. Compelling new evidence shows that even mass extinctions are largely a result of environmental change leading to widespread, attritional reproductive decline, rather than a result of instantaneous global catastrophes.     

How humans drive speciation as well as extinction

A central topic for conservation science is evaluating how human activities influence global species diversity. Humanity exacerbates extinction rates. But by what mechanisms does humanity drive the emergence of new species? We review human-mediated speciation, compare speciation and known extinctions, and discuss the challenges of using net species diversity as a conservation objective. Humans drive rapid evolution through relocation, domestication, hunting and novel ecosystem creation—and emerging technologies could eventually provide additional mechanisms. The number of species relocated, domesticated and hunted during the Holocene is of comparable magnitude to the number of observed extinctions. While instances of human-mediated speciation are known, the overall effect these mechanisms have upon speciation rates has not yet been quantified. We also explore the importance of anthropogenic influence upon divergence in microorganisms. Even if human activities resulted in no net loss of species diversity by balancing speciation and extinction rates, this would probably be deemed unacceptable. We discuss why, based upon ‘no net loss’ conservation literature—considering phylogenetic diversity and other metrics, risk aversion, taboo trade-offs and spatial heterogeneity. We conclude that evaluating speciation alongside extinction could result in more nuanced understanding of biosphere trends, clarifying what it is we actually value about biodiversity.     

Diversity,extinction, and threat status in Lagomorphs

A quarter of all lagomorphs (pikas, rabbits, hares and jackrabbits) are threatened with extinction, including several genera that contain only one species. The number of species in a genus correlates with extinction risk in lagomorphs, but not in other mammal groups, and this is concerning because the non‐random extinction of small clades disproportionately threatens genetic diversity and phylogenetic history. Here, we use phylogenetic analyses to explore the properties of the lagomorph phylogeny and test if variation in evolution, biogeography and ecology between taxa explains current patterns of diversity and extinction risk. Threat status was not related to body size (and, by inference, its biological correlates), and there was no phylogenetic signal in extinction risk. We show that the lagomorph phylogeny has a similar clade‐size distribution to other mammals, and found that genus size was unrelated to present climate, topography, or geographic range size. Extinction risk was greater in areas of higher human population density and negatively correlated with anthropogenically modified habitat. Consistent with this, habitat generalists were less likely to be threatened. Our models did not predict threat status accurately for taxa that experience region‐specific threats. We suggest that pressure from human populations is so severe and widespread that it overrides ecological, biological, and geographic variation in extant lagomorphs.     

Biological correlates of extinction risk in bats

We investigated patterns and processes of extinction and threat in bats using a multivariate phylogenetic comparative approach. Of nearly 1,000 species worldwide, 239 are considered threatened by the International Union for Conservation of Nature and Natural Resources (IUCN) and 12 are extinct. Small geographic ranges and low wing aspect ratios are independently found to predict extinction risk in bats, which explains 48% of the total variance in IUCN assessments of threat. The pattern and correlates of extinction risk in the two bat suborders are significantly different. A higher proportion (4%) of megachiropteran species have gone extinct in the last 500 years than microchiropteran bats (0.3%), and a higher proportion is currently at risk of extinction (Megachiroptera: 34%; Microchiroptera: 22%). While correlates of microchiropteran extinction risk are the same as in the order as a whole, megachiropteran extinction is correlated more with reproductive rate and less with wing morphology. Bat extinction risk is not randomly distributed phylogenetically: closely related species have more similar levels of threat than would be expected if extinction risk were random. Given the unbalanced nature of the evolutionary diversification of bats, it is probable that the amount of phylogenetic diversity lost if currently threatened taxa disappear may be greater than in other clades with numerically more threatened species.     

The cost of being valuable: predictors of extinction risk in marine invertebrates exploited as luxury seafood

Extinction risk has been linked to biological and anthropogenic variables. Prediction of extinction risk in valuable fauna may not follow mainstream drivers when species are exploited for international markets. We use results from an International Union for Conservation of Nature Red List assessment of extinction risk in all 377 known species of sea cucumber within the order Aspidochirotida, many of which are exploited worldwide as luxury seafood for Asian markets. Extinction risk was primarily driven by high market value, compounded by accessibility and familiarity (well known) in the marketplace. Extinction risk in marine animals often relates closely to body size and small geographical range but our study shows a clear exception. Conservation must not lose sight of common species, especially those of high value. Greater human population density and poorer economies in the geographical ranges of endangered species illustrate that anthropogenic variables can also predict extinction risks in marine animals. Local-level regulatory measures must prevent opportunistic exploitation of high-value species. Trade agreements, for example CITES, may aid conservation but will depend on international technical support to low-income tropical countries. The high proportion of data deficient species also stresses a need for research on the ecology and population demographics of unglamorous invertebrates.     

How species respond to multiple extinction threats

It is well established that different species vary in their vulnerability to extinction risk and that species biology can underpin much of this variation. By contrast, very little is known about how the same species responds to different threat processes. The purpose of this paper is therefore twofold: to examine the extent to which a species' vulnerability to different types of threat might covary and to explore the biological traits that are associated with threat-specific responses. We use an objective and quantitative measure of local extinction risk to show that vulnerability to local population decline in primates varies substantially among species and between threat types. Our results show that a species' response to one threat type does not predict its response to others. Multivariate analyses also suggest that different mechanisms of decline are associated with each type of threat, since different biological traits are correlated with each threat-specific response. Primate species at risk from forestry tend to exhibit low ecological flexibility, while those species vulnerable to agriculture tend to live in the canopy and eat low-fruit diets; in further contrast, primates at risk from hunting tend to exhibit large body size. Our analyses therefore indicate that a species' vulnerability to local extinction can be highly variable and is likely to depend on both threat type and biology.     

Global distribution and drivers of language extinction risk

Many of the world''s languages face serious risk of extinction. Efforts to prevent this cultural loss are severely constrained by a poor understanding of the geographical patterns and drivers of extinction risk. We quantify the global distribution of language extinction risk—represented by small range and speaker population sizes and rapid declines in the number of speakers—and identify the underlying environmental and socioeconomic drivers. We show that both small range and speaker population sizes are associated with rapid declines in speaker numbers, causing 25% of existing languages to be threatened based on criteria used for species. Language range and population sizes are small in tropical and arctic regions, particularly in areas with high rainfall, high topographic heterogeneity and/or rapidly growing human populations. By contrast, recent speaker declines have mainly occurred at high latitudes and are strongly linked to high economic growth. Threatened languages are numerous in the tropics, the Himalayas and northwestern North America. These results indicate that small-population languages remaining in economically developed regions are seriously threatened by continued speaker declines. However, risks of future language losses are especially high in the tropics and in the Himalayas, as these regions harbour many small-population languages and are undergoing rapid economic growth.     

Life history correlates and extinction risk of capital-breeding fishes

We consider a distinction for fishes, often made for birds and reptiles, between capital-breeding and income-breeding species. Species that follow a capital-breeding strategy tend to evolve longer intervals between reproductive events and tend to have characteristics that we associate with higher extinction risk. To examine whether these ideas are relevant for fishes, we assembled life history data for fish species, including an index of extinction risk, the interval between spawning events, the degree of parental care, and whether or not the species migrates to spawn. These data were used to evaluate two hypotheses: (1) fish species with a major accessory activity to spawning (migration or parental care) spawn less often and (2) fish species that spawn less often are at greater risk of extinction. We tested these hypotheses by applying two alternative statistical methods that account for phylogenetic correlation in cross-taxon comparisons. The two methods predicted average intervals between spawning events 0.13–0.20 years longer for fishes with a major accessory activity. Both accessories, above-average parental care and spawning migration, were individually associated with longer average spawning intervals. We conclude that the capital-breeding paradigm is relevant for fishes. We also confirmed the second hypothesis, that species in higher IUCN extinction risk categories had longer average spawning intervals. Further research is needed to understand the relationship between extinction risk and spawning interval, within the broader context of life history traits and aquatic habitats. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest editors: S. Dufour, E. Prévost, E. Rochard & P. Williot Fish and diadromy in Europe (ecology, management, conservation)     

Habitat loss, resource specialization, and extinction on coral reefs

Coral reefs worldwide are being degraded because of global warming (coral bleaching) and coastal development (sedimentation and eutrophication). Predicting the risk of species extinctions from this type of habitat degradation is one of the most challenging and urgent tasks facing ecologists. Habitat specialists are thought to be more prone to extinction than generalists; however, specialists may be more susceptible to extinction because (1) they are specialists per se, (2) they are less abundant than generalists, or (3) both. Here, I show that declines in coral abundance lead to corresponding declines in the abundance of coral‐dwelling fishes, but with proportionally greater losses to specialists than generalists. In addition, specialists have smaller initial population sizes than generalists. Consequently, specialists face a dual risk of extinction because their already small populations decline more rapidly than those of generalists. Corresponding with this increased extinction risk, I describe the local extinction of one specialist species and the near‐global extinction of another species. I conclude that habitat specialists will be the first species lost from coral reefs because their small populations suffer the most from human‐induced disturbances.     

Predicting how populations decline to extinction

Global species extinction typically represents the endpoint in a long sequence of population declines and local extinctions. In comparative studies of extinction risk of contemporary mammalian species, there appear to be some universal traits that may predispose taxa to an elevated risk of extinction. In local population-level studies, there are limited insights into the process of population decline and extinction. Moreover, there is still little appreciation of how local processes scale up to global patterns. Advancing the understanding of factors which predispose populations to rapid declines will benefit proactive conservation and may allow us to target at-risk populations as well as at-risk species. Here, we take mammalian population trend data from the largest repository of population abundance trends, and combine it with the PanTHERIA database on mammal traits to answer the question: what factors can be used to predict decline in mammalian abundance? We find in general that environmental variables are better determinants of cross-species population-level decline than intrinsic biological traits. For effective conservation, we must not only describe which species are at risk and why, but also prescribe ways to counteract this.     

The mechanism of background extinction

Following publication of On the Origin of Species, biologists concentrated on and resolved the mechanisms of adaptation and speciation, but largely ignored extinction. Thus, extinction remained essentially a discipline of palaeontology. Adequate language is not available to describe extinction phenomena because they must be discussed in the passive voice, wherein populations simply ‘go extinct’ without reference to process, specifics, effects, or causality. Extinction is also described typically in terms of its dynamics (including rate or risk), and although correlative variables enhance our ability to predict extinction, they do not necessarily enable an understanding of process. Yet background extinction, like evolution, is a process requiring a functional explanation, without which it is impossible to formulate mechanisms. We define the mechanism of background extinction as a typically long‐term, multi‐generational loss of reproductive fitness. This simple concept has received little credence because of a perception that excess generation of progeny ensures population sustainability, and perhaps the misconception that the loss of reproductive fitness somehow constitutes selection against reproduction itself. During environmental shifts, reproductive fitness is compromised when biotic or abiotic extremes consistently exceed existing norms of reaction. Subsequent selection will now favour individual survival over reproductive fitness, initiating long‐term negative selection pressure and population decline. Background extinction consists typically of two intergrading phases: habitat attenuation and habitat dissolution. These processes generate the relict populations that characterize many species undergoing background extinction. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 255–268.     

Specialisation and extinction: Cope's law revisited

Some lineages, specific and supraspecific, tend to be extinction‐prone, others extinction‐resistant in the face of environmental change. Recent attention to the theoretical causes of extinction has focused almost entirely on physical (exogenous) factors. In most higher taxa, species appearing first are commonly characterised by having small to average size, and relatively generalised morphology. Species appearing later in many groups frequently include forms characterised by significant morphologic departures from the early‐appearing, but persistent norm. Such specialised features may include excessive ornamentation such as spinosity, and large, even giant size. Generalists within a genus occupy a considerable spectrum of environments (and communities), but specialists in the same genus tend to occur in a single environment and a single community. Particularly in the benthos, specialists tend to be biogeographically endemic and generalists cosmopolitan, unless the spectrum of environments is extensive and there are no barriers to reproductive communication. Not all forms becoming extinct show morphologic, ecologic or biogeographic evidence of specialisation; this is not surprising since specialisations are not restricted to the skeletal system alone, nor to ecologic and biogeographic characteristics. Specialised community types (e.g. the reef complex of communities, varied pelmatozoan and bryozoan thickets, and sponge forests) are far more extinction‐prone than their more generalised level bottom antecedents. Such biological specialisations ‐ connected with endogenous factors and characteristics of some species ‐ may sometimes be recognised in the palaeontologic record.