Life-history characters and phylogeny are correlated with extinction risk in the Australian angiosperms

Aim To determine whether life‐history characters that affect population persistence (e.g. habit and life span) and those that influence reproductive success (e.g. sexual system and fruit type) are non‐randomly correlated with extinction risk (i.e. threat category) in the Australian flora (c. 19,000 species, of which c. 14% is threatened). To identify patterns that present useful conservation directions. To understand patterns of extinction risk in the Australian flora at a broad scale. Location Continental Australia. Methods A country‐wide exploration of four life‐history characters in the Australian flora (n = 18,822 species) was undertaken using reference texts, expert opinion, herbarium records and field work. For each character and threat‐category combination, a G‐test (using a log‐linear model) was performed to test the null hypothesis that the two factors were independent in their effects on count. A generalized linear model (GLM) with a logit link and binomial error distribution was constructed with the proportion of taxa in each extinction risk category as the response variable and the habit, sex and fruit‐type characters as explanatory terms. In a separate approach, we investigated patterns across the threat categories of non‐endangered extant, endangered, and extinct using a multinomial model. We examined whether or not species‐poor genera were more likely to contain threatened or extinct species than species‐rich genera. A GLM with a binomial error distribution and logit link function was constructed to obtain a weighted regression on the proportion of species listed as extinct or endangered within a genus versus the log of the size of the genus. We also used a supertree analysis and character tracing to investigate the role of phylogeny on extinction risk. Results We found that the Australian flora is primarily composed of bisexual shrubs with dry‐dehiscent fruits. Dioecious breeding systems (separate female and male flowers on separate plants) in many floras are the predominant unisexual system, but in Australia there are unexpectedly high levels of monoecy (separate female and male flowers on the same plant). Within the extinct data set of 31 species we detected a significant departure from that expected for habit but not for life span, sexual system or fruit type. There are significantly fewer trees on the extinct list than expected. This may reflect the greater resilience of trees than of other growth habits to extinction processes as well as the observation time‐frame. Within the endangered data set of 450 species we found significant differences in the representation of the observed characters from that expected within sex systems and fruit types. We show that, depending on the life form, unisexual breeding systems can be significantly and positively associated with endangered species compared with non‐threatened species. For example, there are more monoecious species than expected by chance among the tree species listed as endangered but fewer among the herbaceous life forms. Threat category was found to be non‐randomly clustered in some clades. Main conclusions Life‐history characters in certain combinations are predictive of extinction risk. Phylogeny is also an important component of extinction risk. We suggest that specific life‐history characters could be used for conservation planning and as an early warning sign for detecting vulnerability in lists of species.     

Are psyllids affiliated with the threatened plants Acacia ausfeldii,A. dangarensis and A. gordonii at risk of co‐extinction?

Secondary extinctions of dependent affiliate species may exceed the numbers of species directly extirpated with habitat loss. We investigated the host specificity, and hence the co‐extinction risk, of multiple psyllid species (Hemiptera: Psylloidea) on the threatened plants Acacia ausfeldii, A. dangarensis and A. gordonii by sampling from these and other sympatric common plants across multiple sites, years and plant phenologies. We found one specialist psyllid species (Psyllidae: Acizzia sp.) on each of the plants A. ausfeldii and A. gordonii but no specialists on A. dangarensis. The A. gordonii specialist only occurred when its host was in flower. Specialist psyllids considered at risk of extinction represented 10% of all psyllid species observed on the three threatened acacias. Potential risks to co‐endangered affiliates need to be considered when implementing threatened plant recovery actions. Conservation of plant populations and plant species diversity is also necessary to maintain high insect diversity.     

Do human activities raise species richness? Contrasting patterns in United States plants and fishes

In a given area, human activities usually cause the extinction of native species and the establishment of non‐native species. A key conservation issue is whether non‐native establishment tends to outpace native species extinction to produce a net gain in species richness. To determine this, empirical data must be accumulated at various scales. I show that, within the United States, the number of established non‐native plant species per state does tend to outpace the number of extinct and threatened species per state. The net gain in plant species is strongly and positively correlated with human population density. Continuation of this trend predicts substantial gains in net plant species richness for all states in the United States as human population grows. This contrasts with freshwater fishes, where most states show a net loss of species diversity as extinct and threatened species exceed established non‐native species. Changes in fish diversity do not correlate strongly with human population or non‐native species but are largely driven by the decline of native fish species.     

Present day risk of extinction may exacerbate the lower species richness of dioecious clades

Dioecious clades have been observed to have lower species richness than their non‐dioecious sister groups indicating that dioecious species experience higher extinction rates and (or) lower speciation rates. To determine whether current threats to biodiversity may exacerbate this pattern, we examined the threat to exclusively dioecious families of angiosperms among the 13,013 species of threatened plants included in the IUCN Red List of Threatened Species. When examined phylogenetically, dioecious families had proportionally more species listed than their sister groups. We then examined whether ecological traits correlated with dioecy, namely tropical distribution, woody growth form, and fleshy fruits, are associated with having higher proportions of threatened species. Ignoring breeding system, woody growth form was the only trait that was associated with a greater than expected proportion of threatened species per family. Red‐Listed dioecious families were more likely to have a woody growth form than non‐dioecious families. Woody growth habit is likely contributing to the higher incidence of dioecious species being at risk of extinction but is not solely responsible for the pattern because higher risk within dioecious groups was also apparent in a comparison of exclusively woody sister‐group pairs. Our results indicate that dioecious plants may warrant special attention in conservation practices.     

Do threatened hosts have fewer parasites? A comparative study in primates

1. Parasites and infectious diseases have become a major concern in conservation biology, in part because they can trigger or accelerate species or population declines. Focusing on primates as a well-studied host clade, we tested whether the species richness and prevalence of parasites differed between threatened and non-threatened host species. 2. We collated data on 386 species of parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect wild populations of 36 threatened and 81 non-threatened primate species. Analyses controlled for uneven sampling effort and host phylogeny. 3. Results showed that total parasite species richness was lower among threatened primates, supporting the prediction that small, isolated host populations harbour fewer parasite species. This trend was consistent across three major parasite groups found in primates (helminths, protozoa and viruses). Counter to our predictions, patterns of parasite species richness were independent of parasite transmission mode and the degree of host specificity. 4. We also examined the prevalence of selected parasite genera among primate sister-taxa that differed in their ranked threat categories, but found no significant differences in prevalence between threatened and non-threatened hosts. 5. This study is the first to demonstrate differences in parasite richness relative to host threat status. Results indicate that human activities and host characteristics that increase the extinction risk of wild animal species may lead simultaneously to the loss of parasites. Lower average parasite richness in threatened host taxa also points to the need for a better understanding of the cascading effects of host biodiversity loss for affiliated parasite species.     

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.     

Resistance,tolerance and environmental transmission dynamics determine host extinction risk in a load‐dependent amphibian disease

While disease‐induced extinction is generally considered rare, a number of recently emerging infectious diseases with load‐dependent pathology have led to extinction in wildlife populations. Transmission is a critical factor affecting disease‐induced extinction, but the relative importance of transmission compared to load‐dependent host resistance and tolerance is currently unknown. Using a combination of models and experiments on an amphibian species suffering extirpations from the fungal pathogen Batrachochytrium dendrobatidis (Bd), we show that while transmission from an environmental Bd reservoir increased the ability of Bd to invade an amphibian population and the extinction risk of that population, Bd‐induced extinction dynamics were far more sensitive to host resistance and tolerance than to Bd transmission. We demonstrate that this is a general result for load‐dependent pathogens, where non‐linear resistance and tolerance functions can interact such that small changes in these functions lead to drastic changes in extinction dynamics.     

Phylogenetic Patterns of Extinction Risk in the Eastern Arc Ecosystems,an African Biodiversity Hotspot

There is an urgent need to reduce drastically the rate at which biodiversity is declining worldwide. Phylogenetic methods are increasingly being recognised as providing a useful framework for predicting future losses, and guiding efforts for pre-emptive conservation actions. In this study, we used a reconstructed phylogenetic tree of angiosperm species of the Eastern Arc Mountains – an important African biodiversity hotspot – and described the distribution of extinction risk across taxonomic ranks and phylogeny. We provide evidence for both taxonomic and phylogenetic selectivity in extinction risk. However, we found that selectivity varies with IUCN extinction risk category. Vulnerable species are more closely related than expected by chance, whereas endangered and critically endangered species are not significantly clustered on the phylogeny. We suggest that the general observation for taxonomic and phylogenetic selectivity (i.e. phylogenetic signal, the tendency of closely related species to share similar traits) in extinction risks is therefore largely driven by vulnerable species, and not necessarily the most highly threatened. We also used information on altitudinal distribution and climate to generate a predictive model of at-risk species richness, and found that greater threatened species richness is found at higher altitude, allowing for more informed conservation decision making. Our results indicate that evolutionary history can help predict plant susceptibility to extinction threats in the hyper-diverse but woefully-understudied Eastern Arc Mountains, and illustrate the contribution of phylogenetic approaches in conserving African floristic biodiversity where detailed ecological and evolutionary data are often lacking.     

Integrating biogeography,threat and evolutionary data to explore extinction crisis in the taxonomic group of cycads

Will the ongoing extinction crisis cause a severe loss of evolutionary information accumulated over millions of years on the tree of life? This question has been largely explored, particularly for vertebrates and angiosperms. However, no equivalent effort has been devoted to gymnosperms. Here, we address this question focusing on cycads, the gymnosperm group exhibiting the highest proportion of threatened species in the plant kingdom. We assembled the first complete phylogeny of cycads and assessed how species loss under three scenarios would impact the cycad tree of life. These scenarios are as follows: (1) All top 50% of evolutionarily distinct (ED ) species are lost; (2) all threatened species are lost; and (3) only all threatened species in each IUCN category are lost. Finally, we analyzed the biogeographical pattern of cycad diversity hotspots and tested for gaps in the current global conservation network. First, we showed that threatened species are not significantly clustered on the cycad tree of life. Second, we showed that the loss of all vulnerable or endangered species does not depart significantly from random loss. In contrast, the loss of all top 50% ED , all threatened or all critically endangered species, would result in a greater loss of PD (Phylogenetic Diversity) than expected. To inform conservation decisions, we defined five hotpots of diversity, and depending on the diversity metric used, these hotspots are located in Southern Africa, Australia, Indo‐Pacific, and Mexico and all are found within protected areas. We conclude that the phylogenetic diversity accumulated over millions of years in the cycad tree of life would not survive the current extinction crisis. As such, prioritizing efforts based on ED and concentrating efforts on critically endangered species particularly in southern Africa, Australia, Indo‐Pacific, and Mexico are required to safeguarding the evolutionary diversity in the cycad tree of life.     

Better common than rare? Effects of low reproductive success,scarce pollinator visits and interspecific gene flow in threatened and common species of Tibouchina (Melastomataceae)

The reasons for plant rarity have been the focus of many studies, especially because rare species are more prone to extinction than common species. Under the same habitat conditions, rare plants are expected to attract fewer flower visitors and to show some limitation in their reproductive success. Here, using one of the most emblematic Neotropical plant genus (Tibouchina) we tested whether narrow endemic and threatened species in Ecuador have a lower reproductive success or are visited by fewer pollinators than common species, in 13 populations monitored from 2011 to 2013. We also assessed whether interspecific gene flow could be considered a threat to the rare species. However, contrary to expectations, we found that few pollinators visited the flowers, independently of species rarity. Natural outcross pollinations were always very low in all small‐size populations, leading to high levels of pollen limitation. Interspecific crossing experiments also revealed weak reproductive barriers in some species. This study reveals that both narrow and common species of Tibouchina have similar reproductive and pollinator patterns in Ecuador and, therefore, other causes of the rarity of these species should be considered.     

Guiding the prioritization of the most endangered and evolutionary distinct birds for new zoo conservation programs

Zoos have played a pivotal role in the successful reinforcement and reintroduction of species threatened with extinction, but prioritization is required in the face of increasing need and limited capacity. One means of prioritizing between species of equal threat status when establishing new breeding programs is the consideration of evolutionary distinctness (ED). More distinct species have fewer close relatives such that their extinction would result in a greater overall loss to the Tree of Life. Considering global ex situ holdings of birds (a group with a complete and well‐detailed evolutionary tree), we investigate the representation of at‐risk and highly evolutionarily distinct species in global zoo holdings. We identified a total of 2,236 bird species indicated by the Zoological Information Management System as being held in zoological institutions worldwide. As previously reported, imperiled species (defined as those possessing endangered or critically endangered threat status) in this database are less likely to be held in zoos than non‐imperiled species. However, we find that species possessing ED scores within the top 10% of all bird species are more likely to be held in zoos than other species, possibly because they possess unique characteristics that have historically made them popular exhibits. To assist with the selection of high priority ED species for future zoo conservation programs, we provide a list of imperiled species currently not held in zoos, ranked by ED. This list highlights species representing particular priorities for ex situ conservation planners, and represents a practical tool for improving the conservation value of zoological collections.     

Variation of butterfly diet breadth in relation to host-plant predictability: results from two faunas

Host‐plant data for North American and Australian butterflies were used to test the hypothesis that larval diet breadth increases with decreasing resource predictability (where the latter was estimated by host‐plant growth‐form/duration). For each region in turn we compared the diet breadths of butterflies which utilise herbaceous host‐plants with those of species having woody hosts. For North America alone we also compared the diet breadths of species having annual hosts with those utilising perennial hosts, and the diets of species having herbaceous‐annual hosts with those using woody‐perennial hosts. Studies of diet breadth may be biased by the host taxonomic level which contributes most to the diet index used. For example, the results of analyses which employ indices based on numbers of families of hosts utilised may differ from those using indices based on counts of host species or genera. To investigate this potential problem we performed cross‐species analyses where diet breadth was defined in turn as the number of host species, genera, or families eaten. We found that using different taxonomic levels did give inconsistent results. To avoid this we employed phylogenetic diet breadth indices in comparative analyses of Independent Contrasts. The former incorporate information from the whole of the host‐plant phylogeny, whilst the comparative method eliminates any confounding effects of butterfly phylogeny. The results indicated that there is a phylogenetic component to butterfly diet breadth. They also largely differed from those of the cross‐species investigations, although there were similarities (i.e. results differed between regions and varied according to whether the whole fauna or just endemics were investigated). Our results suggested that in both regions, non‐endemics which feed on herbaceous plants have wider diet breadths than non‐endemics which utilise woody hosts. However, we found no consistent evidence that the diet breadths of endemics increase with decreasing resource predictability (as estimated here).     

Maintaining historic disturbance regimes increases species' resilience to catastrophic hurricanes

As habitat loss and fragmentation, urbanization, and global climate change accelerate, conservation of rare ecosystems increasingly relies on human intervention. However, any conservation strategy is vulnerable to unpredictable, catastrophic events. Whether active management increases or decreases a system's resilience to these events remains unknown. Following Hurricane Irma's landfall in our habitat restoration study sites, we found that rare ecosystems with active, human‐imposed management suffered less damage in a hurricane's path than unmanaged systems. At the center of Irma's landfall, we found Croton linearis' (a locally rare plant that is the sole host for two endangered butterfly species) survival and population growth rates in the year of the hurricane were higher in previously managed plots than in un‐managed controls. In the periphery of Irma's circulation, the effect of prior management was stronger than that of the hurricane. Maintaining the historical disturbance regime thus increased the resilience of the population to major hurricane disturbance. As climate change increases the probability and intensity of severe hurricanes, human management of disturbance‐adapted landscapes will become increasingly important for maintaining populations of threatened species in a storm's path. Doing nothing will accelerate extinction.     

The potential role of arbuscular mycorrhizal fungi in protecting endangered plants and habitats

Ecosystems worldwide are threatened with the extinction of plants and, at the same time, invasion by new species. Plant invasiveness and loss of species can be caused by similar but opposing pressures on the community structures. Arbuscular mycorrhizal fungi (AMF) can have multiple positive effects on plant growth, productivity, health, and stress relief. Many endangered species live in symbiosis with AMF. However, the list of the International Union for Conservation of Nature and Natural Resources (IUCN Red List of Threatened Species) indicates that the mycorrhizal status of most of the threatened species has not been assessed. Rare plants often occur in specialized and also endangered habitats and might utilize specialized or unique AMF. The specificity of any endangered plant to its AMF population has not been investigated. Because most of the current AMF isolates that are available colonize a broad range of plant species, selected inocula could be used to promote growth of endangered plants before the proper and more effective indigenous AMF are characterized. Application of AMF in field sites to protect endangered plants is hardly feasible due to the complexity of plant community structures and the large amount of fungal inocula needed. Endangered plants could, however, be grown as greenhouse cultures together with appropriate fungi, and, at the relevant developmental stage, they could be re-planted into native sites to prevent extinction and to preserve plant community ecology.     

Small edge populations at risk: genetic diversity of the green lizard (<Emphasis Type="Italic">Lacerta viridis viridis</Emphasis>) in Germany and implications for conservation management

Edge and central populations can show great differences regarding their genetic variation and thereby also in their probability of extinction. This fact might be of great importance for the conservation strategies of endangered species. In this study we examine the level of microsatellite variability within three threatened edge populations of the green lizard subspecies Lacerta viridis viridis (Laur.) in Brandenburg (Germany) and compare the observed variation to other edge and central populations within the northern species range. We demonstrate that the northernmost edge populations contain less genetic variation in comparison to the central population. However, there were no observable significant differences to the other edge population included in this study. Surprisingly, we observed a high genetic differentiation in a small geographical range between the three endangered populations in Brandenburg, which can be explained by processes like fragmentation, isolation, genetic drift and small individual numbers within these populations. We also detected unique genetic variants (alleles), which only occurred in these populations, despite a low overall genetic variation. This study demonstrates the potential of fast evolving markers assessing the genetic status of endangered populations with a high resolution. It also illustrates the need for a comparative analysis of different regions within the species range, achieving a more exact interpretation of the genetic variation in endangered populations. This will aid future management decisions in the conservation of genetic diversity in threatened species.     

Do virus‐resistant plants pose a threat to non‐target ecosystems? I. Evidence from an Australian pathosystem based on glasshouse challenge experiments

One key environmental risk associated with the release of novel disease‐resistant plants is the potential for non‐target host populations to acquire resistance genes and undergo enemy release, leading to damage to associated native plant populations in high conservation‐value ecosystems. Unfortunately, the dynamics of most natural pathosystems are poorly understood, and risk assessment of disease‐resistant plants remains a challenge. Here we describe the first stage of a multi‐tiered risk assessment strategy aimed at quantifying potential ecological release in a model pathosystem (the weedy pasture species Trifolium repens infected with Clover yellow vein virus; ClYVV) in order to assess the level of risk posed by genetically modified and conventionally bred disease‐resistant host genotypes to non‐target plant communities in south‐eastern Australia. Glasshouse inoculation and growth experiments using 14 ClYVV isolates and 20 wild T. repens lines collected from high conservation‐value montane grassland and woodland communities show that viral infection reduces the survival and growth of host plants by on average 10–50%. However, T. repens lines exhibited variable levels of resistance and tolerance to virus infection and ClYVV isolates differed in infectivity and aggressiveness, with grassland isolates having a greater pathogenic effect on associated host plants than woodland isolates. We conclude that ClYVV potentially plays an important role in limiting the size of T. repens populations in some at‐risk non‐target ecosystems and that second‐tier field experiments are required to adequately quantify the risk associated with the commercial release of V‐R T. repens genotypes in Australia.     

Effects of environmental variation on extinction and establishment

Theoretical models predict that increasing environmental variation increases the probability of extinction, decreases the probability of establishment, and influences the distribution of times to extinction or establishment. We conducted an experiment with 281 independent populations of Daphnia magna under controlled laboratory conditions to test these predictions. Consistent with the theory, the fraction of populations going extinct increased and the fraction of populations establishing self‐sustaining populations decreased under higher levels of environmental variation compared with controls. Time to extinction decreased under higher levels of environmental variation, but we found no effect on time to establishment. These results are consistent with theoretical predictions from models of extinction. They therefore support the use of stochastic population models to predict the fates of introductions of non‐indigenous species or native endangered species based on historic fluctuations and/or expected future conditions.     

Roads to isolation: Similar genomic history patterns in two species of freshwater crabs with contrasting environmental tolerances and range sizes

Freshwater species often show high levels of endemism and risk of extinction owing to their limited dispersal abilities. This is exemplified by the stenotopic freshwater crab, Johora singaporensis which is one of the world's 100 most threatened species, and currently inhabits less than 0.01 km² of five low order hill streams within the highly urbanized island city‐state of Singapore. We compared populations of J. singaporensis with that of the non‐threatened, widespread, abundant, and eurytopic freshwater crab, Parathelphusa maculata, and found surprisingly high congruence between their population genomic histories. Based on 2,617 and 2,470 genome‐wide SNPs mined via the double‐digest restriction‐associated DNA sequencing method for ~90 individuals of J. singaporensis and P. maculata, respectively, the populations are strongly isolated (F_ST = 0.146–0.371), have low genetic diversity for both species (also for COI), and show signatures of recent genetic bottlenecks. The most genetically isolated populations for both species are separated from other populations by one of the oldest roads in Singapore. These results suggest that anthropogenic developments may have impacted stream‐dependent species in a uniform manner, regardless of ubiquity, habitat preference, or dispersal modes of the species. While signs of inbreeding were not detected for the critically endangered species, the genetic distinctiveness and low diversity of the populations call for genetic rescue and connecting corridors between the remaining fragments of the natural habitat.     

Disease ecology in the Galápagos Hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies

An increased susceptibility to disease is one hypothesis explaining how inbreeding hastens extinction in island endemics and threatened species. Experimental studies show that disease resistance declines as inbreeding increases, but data from in situ wildlife systems are scarce. Genetic diversity increases with island size across the entire range of an extremely inbred Galápagos endemic bird, providing the context for a natural experiment examining the effects of inbreeding on disease susceptibility. Extremely inbred populations of Galápagos hawks had higher parasite abundances than relatively outbred populations. We found a significant island effect on constitutively produced natural antibody (NAb) levels and inbred populations generally harboured lower average and less variable NAb levels than relatively outbred populations. Furthermore, NAb levels explained abundance of amblyceran lice, which encounter the host immune system. This is the first study linking inbreeding, innate immunity and parasite load in an endemic, in situ wildlife population and provides a clear framework for assessment of disease risk in a Galápagos endemic.     

Niche width impacts vertebrate diversification

Aim The size of the climatic niche of a species is a major factor determining its distribution and evolution. In particular, it has been proposed that niche width should be associated with the rate of species diversification. Here, we test whether species niche width affects the speciation and extinction rates of three main clades of vertebrates: amphibians, mammals and birds. Location Global. Methods We obtained the time‐calibrated phylogenies, IUCN conservation status, species distribution maps and climatic data for 2340 species of amphibians, 4563 species of mammals and 9823 species of birds. We computed the niche width for each species as the mean annual temperature across the species range. We estimated speciation, extinction and transition rates associated with lineages with either narrow (specialist) or wide (generalist) niches using phylogeny‐based birth–death models. We also tested if current conservation status was correlated with the niche width of species. Results We found higher net diversification rates in specialist species than in generalist species. This result was explained by both higher speciation rates (for the three taxonomic groups) and lower extinction rates (for mammals and birds only) in specialist than in generalist species. In contrast, current specialist species tended to be more threatened than generalist species. Main conclusions Our diversification analysis shows that the width of the climatic niche is strongly associated with diversification rates and may thus be a crucial factor for understanding the emergence of diversity patterns in vertebrates. The striking difference between our diversification results and current conservation status suggests that the current extinction process may be different from extinction rates estimated from the whole history of the group.