Life history predicts risk of species decline in a stochastic world

Understanding what traits determine the extinction risk of species has been a long-standing challenge. Natural populations increasingly experience reductions in habitat and population size concurrent with increasing novel environmental variation owing to anthropogenic disturbance and climate change. Recent studies show that a species risk of decline towards extinction is often non-random across species with different life histories. We propose that species with life histories in which all stage-specific vital rates are more evenly important to population growth rate may be less likely to decline towards extinction under these pressures. To test our prediction, we modelled declines in population growth rates under simulated stochastic disturbance to the vital rates of 105 species taken from the literature. Populations with more equally important vital rates, determined using elasticity analysis, declined more slowly across a gradient of increasing simulated environmental variation. Furthermore, higher evenness of elasticity was significantly correlated with a reduced chance of listing as Threatened on the International Union for Conservation of Nature Red List. The relative importance of life-history traits of diverse species can help us infer how natural assemblages will be affected by novel anthropogenic and climatic disturbances.     

Is tuna critically endangered? Extinction risk of a large and overexploited population

In 1994, (the World Conservation Union (IUCN) made new quantitative criteria for Red List Categories. Among these, criterion A is based on the reduction rate of population size and is not linked to absolute population size. This is because for most unexploited threatened species absolute population size is completely uncertain. Criterion E is directly concerned with the extinction probability within a specified period. Criterion A is applied to marine fish species, including tuna, which are exploited by commercial fishing. However, for many fish that are commercially exploited, the absolute number of mature individuals and the variance in its yearly reduction rate are often known. In addition, extinction probability depends on absolute population size. There is an inconsistency between criterion A and E when population size is large enough. This is the case for tuna. In this paper, we propose a new criterion for threatened species based on the average reduction rate and the current population size. Criterion A is consistent with criterion E as long as the population size is very small. We also propose a method for estimating the extinction risk of tuna based on the variance of the reduction rate. We investigated the sensitivity in the uncertain parameters involved in the models and concluded that tuna is unlikely to be listed as critically endangered but that southern bluefin tuna may be listed as vulnerable.     

How is diversity related to species turnover through time?

Empirical studies across a wide range of taxa show that the slopes of species–time relationships often decline as average species richness increases, indicating that more diverse communities have greater temporal stability in species composition. I explored potential explanations for this observation using two simple model formulations for species temporal dynamics. In the Abiotic model, species turnover is governed by the degree of heterogeneity in the environment and the range of species' tolerances. In this case, more variable conditions lead to lower species richness and higher turnover, but only if the distribution of species' niche widths and the size of the species pool are independent of the degree of environmental variability. The Biotic model represents direct effects of diversity on turnover through positive or negative feedbacks between diversity and species' colonization and extinction rates. Declining turnover with increasing richness occurred when higher diversity either facilitated colonization by new species or reduced extinction rates of extant species. Both models could produce the observed pattern of declining turnover at higher diversity under some circumstances, however the conditions for this outcome in the Abiotic model were restrictive and potentially unrealistic. The models provide a process-based framework for understanding the connection between diversity and species turnover through time.     

Phylogenetic distributions of British birds of conservation concern

Recent studies suggest that species' life histories and ecology can be used to forecast future extinction risk. Threatened species often share similar traits such that if a trait predisposing a species to decline or extinction is evolutionarily conserved, then close relatives of threatened species are themselves likely to be at risk. The phylogenetic distribution of current threat has been argued to provide insight into the species that could be threatened in the future when trait data are not available. Conservation criteria are typically based on multiple indices that capture different symptoms of threat including population trends and range contraction. However, there is no reason to assume consistent phylogenetic distributions of different symptoms. I construct a molecular phylogeny of 249 species of British birds (more than 93% of the breeding and wintering species) and use this to show that the species that are threatened due to population declines are phylogenetically more closely related than expected by chance alone. However, species that are listed for other reasons, including range contraction, are distributed randomly with respect to phylogeny. I suggest that while phylogeny can be informative with respect to identifying clades that are susceptible to some measures of extinction risk, such patterns are likely to be idiosyncratic with respect to symptom and taxa.     

Scaling the extinction vortex: Body size as a predictor of population dynamics close to extinction events

1. Mutual reinforcement between abiotic and biotic factors can drive small populations into a catastrophic downward spiral to extinction—a process known as the “extinction vortex.” However, empirical studies investigating extinction dynamics in relation to species'' traits have been lacking.
2. We assembled a database of 35 vertebrate populations monitored to extirpation over a period of at least ten years, represented by 32 different species, including 25 birds, five mammals, and two reptiles. We supplemented these population time series with species‐specific mean adult body size to investigate whether this key intrinsic trait affects the dynamics of populations declining toward extinction.
3. We performed three analyses to quantify the effects of adult body size on three characteristics of population dynamics: time to extinction, population growth rate, and residual variability in population growth rate.
4. Our results provide support for the existence of extinction vortex dynamics in extirpated populations. We show that populations typically decline nonlinearly to extinction, while both the rate of population decline and variability in population growth rate increase as extinction is approached. Our results also suggest that smaller‐bodied species are particularly prone to the extinction vortex, with larger increases in rates of population decline and population growth rate variability when compared to larger‐bodied species.
5. Our results reaffirm and extend our understanding of extinction dynamics in real‐life extirpated populations. In particular, we suggest that smaller‐bodied species may be at greater risk of rapid collapse to extinction than larger‐bodied species, and thus, management of smaller‐bodied species should focus on maintaining higher population abundances as a priority.

     

On assessment of the conservation effectiveness of Red Data insect species in the territories of a nature reserve and a nature sanctuary within the same reservation area (by the example of Voronezh Biosphere Nature Reservation)

A category scale of the status of Red Data insect species occurring in the territories of Voronezh Biosphere Nature Reservation and appropriate numerical values (from 0 to 4) of the state index (SI) of insect species are developed. This scale is compatible with the rarity categories used in the Red Data Book of the Russian Federation (2001) and in the regional Red Data Book of Voronezh Province (2011) and Red Data Book of Lipetsk Province (2014). Based on long-term field data and collection material, the status and SI are characterized for 14 insect species listed in the Red Data Book of the Russian Federation and the regional Red Data books and occurring in the territories of the Nature Reserve (shared between Voronezh and Lipetsk provinces) and Nature Sanctuary within Voronezh Biosphere Reservation. The Red Data species showing a positive difference between the SI value in the territory of the Reserve or Sanctuary and the SI listed in the Red Data Book of the Russian Federation (or a regional Red Data book) are considered to be efficiently protected in the Reserve or Sanctuary, respectively. Six Red Data insect species were found to be efficiently protected in the Nature Reserve, and only four species in the Sanctuary.     

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.     

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.     

Application of the IUCN Red Listing system to setting species targets for conservation planning purposes

Biodiversity targets, or estimates of the quantities of biodiversity features that should be conserved in a region, are fundamental to systematic conservation planning. We propose that targets for species should be based on the quantitative thresholds developed for the Vulnerable category of the IUCN Red List system, thereby avoiding future listings of species in an IUCN Red List threat category or an increase in the extinction risk, or ultimate extinction, of species already listed as threatened. Examples of this approach are presented for case studies from South Africa, including threatened taxa listed under the IUCN Red List criteria of A to D, a species listed as Near Threatened, a species of conservation concern due to its rarity, and one species in need of recovery. The method gives rise to multiple representation targets, an improvement on the often used single representation targets that are inadequate for long term maintenance of biodiversity or the arbitrary multiple representation and percentage targets that are sometimes adopted. Through the implementation of the resulting conservation plan, these targets will ensure that the conservation status of threatened species do not worsen over time by qualifying for higher categories of threat and may actually improve their conservation status by eliminating the threat of habitat loss and stabilizing population declines. The positive attributes ascribed to the IUCN Red List system, and therefore to the species targets arising from this approach, are important when justifying decisions that limit land uses known to be detrimental to biodiversity.     

Supertree analyses of the roles of viviparity and habitat in the evolution of atherinomorph fishes

Using supertree phylogenetic reconstructions, we investigate how livebearing and freshwater adaptations may have shaped evolutionary patterns in the Atherinomorpha, a large clade (approximately 1500 extant species) of ray-finned fishes. Based on maximum parsimony reconstructions, livebearing appears to have evolved at least four times independently in this group, and no reversions to the ancestral state of oviparity were evident. With respect to habitat, at least five evolutionary transitions apparently occurred from freshwater to marine environments, at least two transitions in the opposite direction, and no clear ancestral state was identifiable. All viviparous clades exhibited more extant species than their oviparous sister taxa, suggesting that transitions to viviparity may be associated with cladogenetic diversification. Transitions to freshwater were usually, but not invariably associated with increased species richness, but the trend was, overall, not significant among sister clades. Additionally, we investigated whether livebearing and freshwater adaptations are currently associated with elevated risks of extinction as implied by species' presence on the 2004 IUCN Red List. Despite being correlated with decreased brood size, livebearing has not significantly increased extinction risk in the Atherinomorpha. However, freshwater species were significantly more likely than marine species to be listed as endangered.     

Population Fluctuations and Synchrony of Grassland Butterflies in Relation to Species Traits

Population fluctuations and synchrony influence population persistence; species with larger fluctuations and more synchronised population fluctuations face higher extinction risks. Here, we analyse the effect of diet specialisation, mobility, length of the flight period, and distance to the northern edge of the species’ distribution in relation to between-year population fluctuations and synchrony of butterfly species. All butterfly species associated with grasslands were surveyed over five successive years at 19 grassland sites in a forest-dominated landscape (50 km²) in southern Sweden. At both the local and regional level, we found larger population fluctuations in species with longer flight periods. Population fluctuations were more synchronous among localities in diet specialists. Species with a long flight period might move more to track nectar resources compared to species with shorter flight period, and if nectar sources vary widely between years and localities it may explain that population fluctuations increase with increasing flight length. Diet generalists can use different resources (in this case host plants) at different localities and this can explain the lower synchrony in population fluctuations among generalist species. Higher degree of synchrony is one possible explanation for the higher extinction risks that have been observed for more specialised species. Therefore, diet specialists are more often threatened and require more conservation efforts than generalists.     

How is extinction risk related to population-size variability over time? A family of models for species with repeated extinction and immigration

It is well known that for an isolated population, the probability of extinction is positively related to population size variation: more variation is associated with more extinction. What, then, is the relation of extinction to population size variation for a population embedded in a metapopulation and subjected to repeated extinction and recolonization? In this case, the extinction risk can be measured by the extinction rate, the frequency at which local extinction occurs. Using several population dynamics models with immigration, we find, in general, a negative correlation between extinction and variation. More precisely, with increasing length of the time series, an initially negative regression coefficient first becomes more negative, then becomes less negative, and eventually attains positive values before decreasing again to 0. This pattern holds under substantial variation in values of parameters representing species and environmental properties. It is also rather robust to census interval length and the fraction of missed individuals but fails to hold for high thresholds (population size values below which extinction is deemed to occur) when quasi extinction rather than true extinction is represented. The few departures from the initial negative correlation correspond to populations at risk: low growth rate or frequent catastrophes.     

Using Mark-recapture to provide population census data for use in Red Listing of invertebrates: the rare terrestrial snail Prestonella bowkeri as a case study

Invertebrates in general, and terrestrial molluscs in particular, are greatly affected by the current biodiversity extinction crisis, and accurate assessment of these organisms for inclusion in Red Lists is essential for the conservation of these taxa. However, obtaining accurate population counts of molluscs for this purpose can be challenging. Using Prestonella bowkeri, a terrestrial snail up to 23 mm in length and 14 mm in width found in mesic rocky cliff face habitats on the Great Escarpment of southern Africa as an example, we show that the use of Mark-recapture techniques to obtain population census data is appropriate to terrestrial molluscs of this size and larger. While currently listed as vulnerable, our results indicate that there are as many as 4,108 individuals of this species in one population, which suggests that the population size (sensu the IUCN definition) is probably >20,000, and the species could be down-listed and classified as near threatened. However, when considering the problems associated with applying the IUCN Red List criteria to invertebrates, and the very small number of populations and hence area of occupancy of this species, down-listing would be premature.     

Testing a biological mechanism of the insurance hypothesis in experimental aquatic communities

1.  The insurance hypothesis predicts a stabilizing effect of increasing species richness on community and ecosystem properties. Difference among species' responses to environmental fluctuations provides a general mechanism for the hypothesis. Previous experimental investigations of the insurance hypothesis have not examined this mechanism directly.
2.  First, responses to temperature of four protist species were measured in laboratory microcosms. For each species, we measured the response of intrinsic rate of increase ( r ) and carrying capacity ( K ) to temperature.
3.  Next, communities containing pairs of species were exposed to temperature fluctuations. Community biomass varied less when correlation in K between species (but not r ) was more negative, and this resulted from more negative covariances in population sizes, as predicted. Results were contingent on species identity, with findings differing between analyses including or not including communities containing one particular species.
4.  These findings provide the clearest support to date for this mechanism of the insurance hypothesis. Biodiversity, in terms of differences in species' responses to environmental fluctuations (i.e. functional response diversity) stabilizes community dynamics.     

Neither protogynous nor obligatory out-crossed: pollination biology and breeding system of the European Red List Fritillaria meleagris L. (Liliaceae)

For 4 years we studied pollination biology and breeding system of the critically endangered, Red List plant Fritillaria meleagris L. (Liliaceae), in the larger of the two remaining populations of the plant in SE Poland. Our observations indicated that, contrary to literature data, the species is not dichogamous nor is it obligatorily out-crossing. Selfing, although rare in natural populations, results in fully developed seeds. Flowers are visited by several insect species, mostly social and solitary bees. In spite of extremely low visitation rates to this early spring-flowering plant, the species is not pollen limited. Although the largest pollen loads are transferred by solitary bees, the key pollinators are bumblebees (mostly the most common species, Bombus terrestris and B. lapidarius) due to their seasonal and floral constancy, and tolerance of bad weather conditions. The current decline of the studied population seems not to be related to the species' pollination or breeding systems but to plant habitat loss. It is suggested, however, that in smaller populations, the species' dependence on generally rare pollinators and largely out-crossed breeding system may accelerate local extinction.     

Caught in the middle: Asymmetric competition causes high variance in intermediate trait abundances

In asymmetric competition between two individuals of the same or different species, one individual has a distinct advantage over the other due to a particular beneficial trait. An important trait that induces asymmetric competition is size (body size in animals, height in plants). There is usually a trade-off between fecundity and the trait that leads to competitive superiority (e.g. seed number vs seed size), enabling coexistence of populations with different trait values. These predictions on coexistence are based on classic deterministic models. Here, we explore the behaviour of a stochastic model of asymmetric competition where stochasticity is assumed to be demographic. We derive approximations for the temporal variance and covariance of the population sizes of the coexisting species. The derivations highlight that the variability of the population size of a species strongly depends on the stochastic fluctuations of species with higher trait values, while they are less influenced by species with lower trait values. Particularly, species with intermediate trait values are strongly affected resulting in relatively high variability. As a result these species have a relative high probability of extinction even though they have a larger population size than species with high trait values. We confirm these approximations with individual-based simulations. Thus, our analysis can explain gaps in size distributions as an emergent property of systems with a fecundity–competition trade-off.     

Palm economic and traditional uses,evolutionary history and the IUCN Red List

The growing demand for natural resources to sustain human population has increased the loss and modification of natural habitats, enhancing the number of species threatened with extinction. Commonly tools such as Red Lists guide conservation actions and policies. However, Red Lists are based in population parameters, and important aspects of biodiversity such as phylogenetic diversity are not considered. Here we evaluated the amount of economic and traditional uses and evolutionary history of palms captured by the global IUCN Red List and the national Red Lists of Colombia and Madagascar. We estimated palms plant use diversity (PUD) and phylogenetic diversity (PD) for all species in the IUCN Red List and for each threat category at global and national scale. We also investigated if the number of uses, PUD and PD predict palm threat level. Species covered by IUCN Red List have lower PUD and PD than expected by chance. At global scale, palms with higher extinction risk have lower number of uses, PUD and PD. However, whereas in Colombia least concern species had lower PUD and PD, in Madagascar only Data Deficient species had lower PUD than expected by chance. Our findings highlight the need of palm specialists to expand the list of palms they have assessed and submit them for inclusion in Red Lists, enabling Red Lists to capture a more random sample of palm evolutionary history and economic uses. That would improve the success of biodiversity conservation actions by taking into account other aspects of biodiversity rather than taxonomic identity.     

Extinctions in competitive communities forced by coloured environmental variation

Understanding the relationships between environmental fluctuations, population dynamics and species interactions in natural communities is of vital theoretical and practical importance. This knowledge is essential in assessing extinction risks in communities that are, for example, pressed by changing environmental conditions and increasing exploitation. We developed a model of density dependent population renewal, in a Lotka–Volterra competitive community context, to explore the significance of interspecific interactions, demographic stochasticity, population growth rate and species abundance on extinction risk in populations under various autocorrelation (colour) regimes of environmental forcing. These factors were evaluated in two cases, where either a single species or the whole community was affected by the external forcing. Species' susceptibility to environmental noise with different autocorrelation structure depended markedly on population dynamics, species' position in the abundance hierarchy and how similarly community members responded to external forcing. We also found interactions between demographic stochasticity and environmental noise leading to a reversal in extinction probabilities from under- to overcompensatory dynamics. We compare our results with studies of single species populations and contrast possible mechanisms leading to extinctions. Our findings indicate that abundance rank, the form of population dynamics, and the colour of environmental variation interact in affecting species extinction risk. These interactions are further modified by interspecific interactions within competitive communities as the interactions filter and modulate the environmental noise.     

General relationships between species diversity and stability in competitive systems

Investigating the effect of biodiversity on the stability of ecological communities is complicated by the numerous ways in which models of community interactions can be formulated. This has led to differences in conclusions and interpretations of how the number of species in a community affects its stability. Here, we derive a simple, general relationship between the coefficient of variation (CV) of combined species densities and the environmentally driven variability in species' per capita population growth rates. For a given level of environmentally driven variability in per capita population growth rates, increasing the number of species in a community decreases the CV of combined species densities, provided that species do not respond to environmental fluctuations in a perfectly correlated way. Thus, a community with more species of competitors will be more stable (have lower CV in combined species densities for a given level of environmental variability) than a species-poor community, provided that the species in both communities show equal variability in per capita population growth rates and provided that species within each community do not show strongly correlated responses to environmental fluctuations. This conclusion also applies to "noninteractive" models in which there is no competition between species.     

Warning times for species extinctions due to climate change

Climate change is likely to become an increasingly major obstacle to slowing the rate of species extinctions. Several new assessment approaches have been proposed for identifying climate‐vulnerable species, based on the assumption that established systems such as the IUCN Red List need revising or replacing because they were not developed to explicitly consider climate change. However, no assessment approach has been tested to determine its ability to provide advanced warning time for conservation action for species that might go extinct due to climate change. To test the performance of the Red List system in this capacity, we used linked niche‐demographic models with habitat dynamics driven by a ‘business‐as‐usual’ climate change scenario. We generated replicate 100‐year trajectories for range‐restricted reptiles and amphibians endemic to the United States. For each replicate, we categorized the simulated species according to IUCN Red List criteria at annual, 5‐year, and 10‐year intervals (the latter representing current practice). For replicates that went extinct, we calculated warning time as the number of years the simulated species was continuously listed in a threatened category prior to extinction. To simulate data limitations, we repeated the analysis using a single criterion at a time (disregarding other listing criteria). Results show that when all criteria can be used, the Red List system would provide several decades of warning time (median = 62 years; >20 years for 99% of replicates), but suggest that conservation actions should begin as soon as a species is listed as Vulnerable, because 50% of replicates went extinct within 20 years of becoming uplisted to Critically Endangered. When only one criterion was used, warning times were substantially shorter, but more frequent assessments increased the warning time by about a decade. Overall, we found that the Red List criteria reliably provide a sensitive and precautionary way to assess extinction risk under climate change.