Effects of roost specialization on extinction risk in bats

Understanding causes and consequences of ecological specialization is of major concern in conservation. Specialist species are particularly vulnerable to human activities. If their food or habitats are depleted or lost, they may not be able to exploit alternative resources, and population losses may result. We examined International Union for Conservation of Nature (IUCN) Red List bat data and the number of roosts used per species (accounting for phylogenetic independence) to determine whether roost specialization is correlated with extinction risk. We found a significant correlation between the IUCN Red List category and the number of roost types used. Species that use fewer roost types had a higher risk of extinction. We found that caves and similar structures were the most widely used roost types, particularly by species under some level of risk of extinction. Many critically endangered, endangered, or vulnerable species used natural roosts exclusively, whereas less threatened species used natural and human‐made roosts. Our results suggest that roost loss, particularly in species that rely on a single roost type, may be linked to extinction risk. Our focus on a single life history trait prevented us from determining how important this variable is for extinction risk relative to other variables, but we have taken a first step toward prioritizing conservation actions. Our results also suggest that roost specialization may exacerbate population declines due to other risk factors, such as hunting pressure or habitat loss, and thus that management actions to preserve species under risk of extinction should prioritize protection of roosting sites.     

Use of Basic Biological Information for Rapid Prediction of the Response of Species to Habitat Loss

Abstract:  Much research has focused on identifying traits that can act as useful indicators of how habitat loss affects the extinction risk of species, and the results are mixed. We developed 2 simple, rapid-assessment models of the susceptibility of species to habitat loss. We based both on an index of range size, but one also incorporated an index of body mass and the other an index combining habitat and dietary specialization. We applied the models to samples of birds (Accipitridae and Bucerotidae) and to the lemurs of Madagascar and compared the models' classifications of risk with the IUCN's global threat status of each species. The model derived from ecological attributes was much more robust than the one derived from body mass. Ecological attributes identified threatened birds and lemurs with an average of 80% accuracy and endangered and critically endangered species with 100% accuracy and identified some species not currently listed as threatened that almost certainly warrant conservation consideration. Appropriate analysis of even fairly crude biological information can help raise early-warning flags to the relative susceptibilities of species to habitat loss and thus provide a useful and rapid technique for highlighting potential species-level conservation issues. Advantages of this approach to classifying risk include flexibility in the specialization parameters used as well as its applicability at a range of spatial scales.     

Response of Neotropical Bat Assemblages to Human Land Use

Neotropical bats are sensitive to human‐induced habitat changes, and some authors believe bats can be used as bioindicators. In the literature, however, the results are disparate. Some results show bat diversity deceases as disturbance increases, whereas others indicate no effect. Determining the general response patterns of bats when they encounter different degrees of human‐induced disturbance across the Neotropics would help to determine their usefulness as bioindicators. In a series of meta‐analyses, we compared the occurrence frequency of bat species between well‐preserved forests and human‐use areas. We obtained data through an extensive review of published peer‐reviewed articles, theses, and reports. The overall effect size indicated that human‐use areas harbored more bat species than well‐preserved forests. Different response patterns emerged when meta‐analyses were conducted separately by family, feeding habit, vegetation stratum, and conservation status. Our results suggest that bat assemblages display strong responses to forest loss and land‐use change and that the direction and magnitude of these responses depends on the bat group under study and the type of disturbance. Our results are consistent with the idea that bats are useful for assessing the effects of habitat changes in the Neotropics. However, with our meta‐analyses we could not detect fine differences in bat feeding habits, especially within Phyllostomidae, or elucidate the effect of landscape configuration. Respuesta de Ensambles de Murciélagos Neotropicales al Uso de Suelo por Humanos     

Estimation of spatiotemporal trends in bat abundance from mortality data collected at wind turbines

Renewable energy sources, such as wind energy, are essential tools for reducing the causes of climate change, but wind turbines can pose a collision risk for bats. To date, the population-level effects of wind-related mortality have been estimated for only 1 bat species. To estimate temporal trends in bat abundance, we considered wind turbines as opportunistic sampling tools for flying bats (analogous to fishing nets), where catch per unit effort (carcass abundance per monitored turbine) is a proxy for aerial abundance of bats, after accounting for seasonal variation in activity. We used a large, standardized data set of records of bat carcasses from 594 turbines in southern Ontario, Canada, and corrected these data to account for surveyor efficiency and scavenger removal. We used Bayesian hierarchical models to estimate temporal trends in aerial abundance of bats and to explore the effect of spatial factors, including landscape features associated with bat habitat (e.g., wetlands, croplands, and forested lands), on the number of mortalities for each species. The models showed a rapid decline in the abundance of 4 species in our study area; declines in capture of carcasses over 7 years ranged from 65% (big brown bat [Eptesicus fuscus]) to 91% (silver-haired bat [Lasionycteris noctivagans]). Estimated declines were independent of the effects of mitigation (increasing wind speed at which turbines begin to generate electricity from 3.5 to 5.5 m/s), which significantly reduced but did not eliminate bat mortality. Late-summer mortality of hoary (Lasiurus cinereus), eastern red (Lasiurus borealis), and silver-haired bats was predicted by woodlot cover, and mortality of big brown bats decreased with increasing elevation. These landscape predictors of bat mortality can inform the siting of future wind energy operations. Our most important result is the apparent decline in abundance of four common species of bat in the airspace, which requires further investigation.     

Habitat Fragmentation and Species Loss across Three Interacting Trophic Levels: Effects of Life-History and Food-Web Traits

Abstract:  Not all species are likely to be equally affected by habitat fragmentation; thus, we evaluated the effects of size of forest remnants on trophically linked communities of plants, leaf-mining insects, and their parasitoids. We explored the possibility of differential vulnerability to habitat area reduction in relation to species-specific and food-web traits by comparing species–area regression slopes. Moreover, we searched for a synergistic effect of these traits and of trophic level . We collected mined leaves and recorded plant, leaf miner, and parasitoid species interactions in five 100-m² transects in 19 Chaco Serrano woodland remnants in central Argentina. Species were classified into extreme categories according to body size, natural abundance, trophic breadth, and trophic level . Species–area slopes differed between groups with extreme values of natural abundance or trophic specialization. Nevertheless, synergistic effects of life-history and food-web traits were only found for trophic level and trophic breadth: area-related species loss was highest for specialist parasitoids. It has been suggested that species position within interaction webs could determine their vulnerability to extinction. Our results provide evidence that food-web parameters, such as trophic level and trophic breadth, affect species sensitivity to habitat fragmentation .     

Effects of Artificial Roosts for Frugivorous Bats on Seed Dispersal in a Neotropical Forest Pasture Mosaic

Abstract:  In the Neotropics ongoing deforestation is producing open and heavily fragmented landscapes dominated by agriculture, mostly plantations and cattle pastures. After some time agriculture often becomes uneconomical and land is abandoned. Subsequent habitat regeneration may be slow because seed inputs are restricted by a lack of incentives—such as suitable roost sites—for seed dispersers to enter deforested areas. Increasing environmental awareness has fostered growing efforts to promote reforestation. Practical and cost-efficient methods for kick-starting forest regeneration are, however, lacking. We investigated whether artificial bat roosts for frugivorous bat species can attract these key seed dispersers to deforested areas, thereby increasing seed rain. We installed artificial bat roosts in a forest-pasture mosaic in the Costa Rican Atlantic lowlands and monitored bat colonization and seed dispersal. Colonization occurred within a few weeks of installation, and 10 species of bats occupied the artificial roosts. Five species of frugivorous or nectarivorous bats colonized artificial roosts permanently in both primary habitat and in deforested areas, in numbers similar to those found in natural roosts. Seed input around artificial roosts increased significantly. Sixty-nine different seed types, mostly of early-successional plant species, were transported by bats to artificial roosts in disturbed habitats. The installation of artificial bat roosts thus successfully attracted frugivorous bats and increased seed inputs into degraded sites. This method is likely to speed up early-vegetation succession, which in turn will attract additional seed dispersers, such as birds, and provide a microhabitat for seeds of mid- and late-successional plants. As well as supporting natural forest regeneration and bat conservation, this cost-efficient method can also increase environmental awareness among landowners.     

Ecology and Conservation of the Endangered American Burying Beetle (Nicrophorus americanus)

Field studies were conducted on the western population of the endangered American burying beetle (Nicrophorus americanus) in Oklahoma and Arkansas to determine its habitat affinities. A common cause of declining populations is some specialized adaptation that makes it difficult to respond to a rapidly changing habitat. We evaluated the hypothesis that N. americanus is a habitat specialist in its search for food, preferring mature forests with deep, humic soils. This hypothesis was rejected. Based on comparisons of niche breadth among syntopic congeners and niche overlap, N. americanus is relatively generalized in its use of a range of habitats when searching for food. It is likely that the generalist nature and the endangered status of N. americanus both derive from the fact that it is the largest member of its guild. In comparison to smaller species, N. americanus breeds on larger carcasses, which are more unpredictable in space and time. It is likely, therefore, that N. americanus must search over a larger area and greater diversity of habitats than its smaller congeners.     

Ecological Correlates of Extinction Proneness in Tropical Butterflies

Abstract:  Widespread and rapid losses of natural habitats and biodiversity have made the identification of extinction-prone species a major challenge in conservation biology. We assessed the relative importance of biologically relevant species traits (e.g., body size, ecological specialization) obtained from published records to determine the extinction probability of butterflies in a highly disturbed tropical landscape (i.e., Singapore). We also developed a taxon-specific model to estimate the extinction proneness of butterflies in Southeast Asia. Logistic regression analyses showed that adult habitat specialization, larval host plant specificity, geographical distribution, sexual dichromatism, and congenor density were significant and independent determinants of butterfly extinctions in Singapore. Among these traits, specificity of larval host plant and adult habitat specialization were the best correlates of extinction risks. We used this phenomenological extinction-regression model to estimate the relative extinction proneness of 416 butterfly species in Southeast Asia. Our results illustrate the utility of available taxon-specific data for a localized area in estimating the extinction proneness of closely related species on a regional scale. When intensive field studies are not forthcoming, especially in regions suffering from rapid biodiversity losses (e.g., Southeast Asia), similar approaches could be used to estimate extinction threats for other taxonomic groups.     

Predicting and setting conservation priorities for Bolivian mammals based on biological correlates of the risk of decline

The recognition that growing proportions of species worldwide are endangered has led to the development of comparative analyses to elucidate why some species are more prone to extinction than others. Understanding factors and patterns of species vulnerability might provide an opportunity to develop proactive conservation strategies. Such comparative analyses are of special concern at national scales because this is the scale at which most conservation initiatives take place. We applied powerful ensemble learning models to test for biological correlates of the risk of decline among the Bolivian mammals to understand species vulnerability at a national scale and to predict the population trend for poorly known species. Risk of decline was nonrandomly distributed: higher proportions of large‐sized taxa were under decline, whereas small‐sized taxa were less vulnerable. Body mass, mode of life (i.e., aquatic, terrestrial, volant), geographic range size, litter size, home range, niche specialization, and reproductive potential were strongly associated with species vulnerability. Moreover, we found interacting and nonlinear effects of key traits on the risk of decline of mammals at a national scale. Our model predicted 35 data‐deficient species in decline on the basis of their biological vulnerability, which should receive more attention in order to prevent their decline. Our results highlight the relevance of comparative analysis at relatively narrow geographical scales, reveal previously unknown factors related to species vulnerability, and offer species‐by‐species outcomes that can be used to identify targets for conservation, especially for insufficiently known species. Predección y Definición de Prioridades de Conservación para Mamíferos de Bolivia con Base en Correlaciones Biológicas del Riesgo de Declinación     

Estimating Extinction Risk with Metapopulation Models of Large‐Scale Fragmentation

Habitat loss is the principal threat to species. How much habitat remains—and how quickly it is shrinking—are implicitly included in the way the International Union for Conservation of Nature determines a species’ risk of extinction. Many endangered species have habitats that are also fragmented to different extents. Thus, ideally, fragmentation should be quantified in a standard way in risk assessments. Although mapping fragmentation from satellite imagery is easy, efficient techniques for relating maps of remaining habitat to extinction risk are few. Purely spatial metrics from landscape ecology are hard to interpret and do not address extinction directly. Spatially explicit metapopulation models link fragmentation to extinction risk, but standard models work only at small scales. Counterintuitively, these models predict that a species in a large, contiguous habitat will fare worse than one in 2 tiny patches. This occurs because although the species in the large, contiguous habitat has a low probability of extinction, recolonization cannot occur if there are no other patches to provide colonists for a rescue effect. For 4 ecologically comparable bird species of the North Central American highland forests, we devised metapopulation models with area‐weighted self‐colonization terms; this reflected repopulation of a patch from a remnant of individuals that survived an adverse event. Use of this term gives extra weight to a patch in its own rescue effect. Species assigned least risk status were comparable in long‐term extinction risk with those ranked as threatened. This finding suggests that fragmentation has had a substantial negative effect on them that is not accounted for in their Red List category. Estimación del Riesgo de Extinción Mediante Modelos Metapoblacionales de Fragmentación a Gran Escala     

Behavioral responses to echolocation calls from sympatric heterospecific bats: implications for interspecific competition

Mutual recognition is the product of species coexistence, and has direct effects on survival and reproduction of animals. Bats are able to discriminate between sympatric different heterospecifics based on their echolocation calls, which has been shown both in free-flying and captive bats. To date, however, the factors that may determine the behavioral responses of bats to echolocation calls from sympatric heterospecifics have rarely been tested, especially under well-controlled conditions in captive bats. Hence, we aimed at tackling this question by performing playback experiments (habituation–dishabituation) with three horseshoe bat species within the constant-frequency bat guild, which included big-eared horseshoe bats (Rhinolophus macrotis), Blyth’s horseshoe bats (Rhinolophus lepidus), and Chinese horseshoe bats (Rhinolophus sinicus). We studied the behavioral responses of these three species to echolocation calls of conspecifics, to other two species, and to another heterospecifics bat, Stoliczka’s trident bat (Asellisus stoliczkanus), which also belongs to this guild. We found that the three rhinolophid species displayed a series of distinct behaviors to heterospecific echolocation but few to conspecific calls after habituation, suggesting that they may have been able to discriminate sympatric heterospecific echolocation calls from those of conspecifics. Interestingly, the behavioral responses to heterospecific calls were positively correlated with the interspecific overlap index in trophic niche, whereas call design had only a minor effect. This implies that the behavioral responses of these bats to heterospecific echolocation calls may be related to the degree of interspecific food competition.     

Interactions among Frugivores and Fleshy Fruit Trees in a Philippine Submontane Rainforest

Abstract: We assessed the potential effect of frugivore extinctions on forest regeneration in the North Negros Forest Reserve, a forest fragment that is one of the last remaining wet tropical rainforest ecosystems in the biogeographic region of the central Philippine Islands. We evaluated foraging observations of 19 species of birds, fruit bats, and other mammals in three successional habitats and identified tree species that are potentially at risk because their seeds are dispersed by frugivores that are seriously endangered. The relative abundance of zoochorous trees in this forest community was exceptionally high (80%), suggesting that the process of forest regeneration will change drastically if endangered frugivores are hunted to extinction. We grouped 45 tree species as early-, mid-, or late-successional species based on their population structure and we demonstrated that early-successional tree species were visited by a wide spectrum of frugivores, whereas mid- and late-successional species were visited mostly by hornbills (Bucerotidae) and fruit pigeons (Columbidae). Late-successional tree species were most specialized with respect to dispersers and could therefore be susceptible to extinction. We recommend tree species that could be useful for assisted natural regeneration projects in the reserve because they are visited by a variety of frugivores. Of those, we recommend early-successional trees for open-field plantations and mid-successional tree species for enrichment plantings.     

Risk of Local Extinction of Odonata Freshwater Habitat Generalists and Specialists

Understanding the risk of a local extinction in a single population relative to the habitat requirements of a species is important in both theoretical and applied ecology. Local extinction risk depends on several factors, such as habitat requirements, range size of species, and habitat quality. We studied the local extinctions among 31 dragonfly and damselfly species from 1930 to 1975 and from 1995 to 2003 in Central Finland. We tested whether habitat specialists had a higher local extinction rate than generalist species. Approximately 30% of the local dragonfly and damselfly populations were extirpated during the 2 study periods. The size of the geographical range of the species was negatively related to extinction rate of the local populations. In contrast to our prediction, the specialist species had lower local extinction rates than the generalist species, probably because generalist species occurred in both low‐ and high‐quality habitat. Our results are consistent with source–sink theory. Riesgo de Extinción Local de Odonatos de Agua Dulce Generalistas y Especialistas de Hábitat     

Global Warming, Human Population Pressure, and Viability of the World's Smallest Butterfly

Abstract:  The effects of climate change and habitat destruction and their interaction are likely to be the greatest challenge to animal and plant conservation in the twenty-first century. We used the world's smallest butterfly, the Sinai baton blue ( Pseudophilotes sinaicus ), as an exemplar of how global warming and human population pressures may act together to cause species extinctions. We mapped the entire global range of this butterfly and obtained extensive data on the intensity of livestock grazing. As with an increasing number of species, it is confined to a network of small habitat patches and is threatened both by indirect human-induced factors (global warming) and by the direct activities of humans (in this case, livestock grazing and collection of medicinal plants). In the absence of global warming, grazing, and plant collection, our model suggested that the butterfly will persist for at least 200 years. Above a threshold intensity of global warming, the chance of extinction accelerated rapidly, implying that there may be an annual average temperature, specific to each endangered species, above which extinction becomes very much more likely. By contrast, there was no such threshold of grazing pressure—the chance of extinction increased steadily with increasing grazing. The impact of grazing, however, decreased with higher levels of year-to-year variation in habitat quality. The effect of global warming did not depend on the future level of grazing, suggesting that the impacts of global warming and grazing are additive. If the areas of habitat patches individually fall below certain prescribed levels, the butterfly is likely to go extinct. Two patches were very important for persistence: if either were lost the species would probably go extinct. Our results have implications for the conservation management of all species whose habitats are at risk because of the direct activities of humans and in the longer term because of climate change.     

Modified Cave Entrances: Thermal Effect on Body Mass and Resulting Decline of Endangered Indiana Bats (Myotis sodalis)

Entrances to many caves occupied by the endangered Indiana bat ( Myotis sodalis ) have been modified to control human access. We show that modifying cave entrances can degrade the bats' winter habitat, we demonstrate one mechanism by which this damage occurs, and we document a restoration experiment. We compared a large bar population in an unmodified cave with a small, reduced bat population in a cave with warm winter temperatures resulting from an entrance wall that impeded air exchange. In the modified cave, mean winter temperature at the hibernation site was 5.0° C higher than in the unmodified cave, bats entered hibernation at a 5% higher body mass, bats lost 42% more mass and the frequency distribution of late-winter mass was truncated, with no bats weighing less than 5.4 g. The results describe unacceptable extremes for hibernation: subfreezing temperatures and warm temperatures causing mass-loss rates of more than 0.009 g/day. Over a decade following removal of the entrance-constricting wall, the population increased from 2,000 to 13,000 bats. Previous recommendations, based on common-sense observation, to open blocked cave entrances are confirmed by this study. The similar case of Coach Cave, Kentucky, offers the potential for recovery of 100,000 Indiana bats.     

Echolocation behavior of the bat <Emphasis Type="Italic">Vespertilio murinus</Emphasis> reveals the border between the habitat types “edge” and “open space”

We test the hypothesis that echolocation behavior can be used to find the border between bat habitats. Assuming that bats react to background targets in “edge space” but not in “open space”, we determined the border between these two habitat types for commuting individuals of the parti-colored bat Vespertilio murinus. We recorded sequences of bats’ echolocation signals while they flew parallel to the walls of large buildings and to the ground and determined the signals’ average bandwidth, duration, and pulse interval. These parameters varied systematically with the estimated horizontal and vertical distances between the bats and the background. A distinct effect of horizontal distance to the background on echolocation behavior was found for horizontal distances of less than 6 m, thus indicating the border between edge and open space. Only a few bats flew at vertical distances below 5 m. However, enough passages at vertical distances of 5 m and above indicated that the vertical border is somewhere below a distance of 5 m. Within edge space, V. murinus reacted to the background by reducing signal duration, increasing bandwidth at closer distances, and often emitting one signal per wing beat. In open space, signal parameters did not vary as a function of distance to the background. There, V. murinus emitted the longest signals with the narrowest bandwidth and often made one or two wing beats without emitting a pulse. With our data we support with statistical methods the hypothesis that echolocation behavior reveals the border between the habitat types “edge” and “open space”.     

The Normative Dimension and Legal Meaning of Endangered and Recovery in the U.S. Endangered Species Act

Abstract:  The ethical, legal, and social significance of the U.S. Endangered Species Act of 1973 (ESA) is widely appreciated. Much of the significance of the act arises from the legal definitions that the act provides for the terms threatened species and endangered species. The meanings of these terms are important because they give legal meaning to the concept of a recovered species. Unfortunately, the meanings of these terms are often misapprehended and rarely subjected to formal analysis. We analyzed the legal meaning of recovered species and illustrate key points with details from "recovery" efforts for the gray wolf ( Canis lupus ). We focused on interpreting the phrase "significant portion of its range," which is part of the legal definition of endangered species. We argue that recovery and endangerment entail a fundamentally normative dimension (i.e., specifying conditions of endangerment) and a fundamentally scientific dimension (i.e., determining whether a species meets the conditions of endangerment). Specifying conditions for endangerment is largely normative because it judges risks of extinction to be either acceptable or unacceptable. Like many other laws that specify what is unacceptable, the ESA largely specifies the conditions that constitute unacceptable extinction risk. The ESA specifies unacceptable risks of extinction by defining endangered species in terms of the portion of a species' range over which a species is "in danger of extinction." Our analysis indicated that (1) legal recovery entails much more than the scientific notion of population viability, (2) most efforts to recover endangered species are grossly inadequate, and (3) many unlisted species meet the legal definition of an endangered or threatened species.     

Global Patterns of Mammalian Diversity, Endemism, and Endangerment

To assess the conservation status of the world's land mammals, we compiled data on the number of total species, endemic species, recently extinct species, and currently endangered species for 155 countries. Total species richness was significantly correlated with territorial land area, whereas number of endemic species was only weakly correlated with both area and total number of species. The large amount of variation left unexplained by species-area regressions reflects the influence of other factors, such as latitude, topographic and habitat heterogeneity, and historical biogeography, on species richness and especially on patterns of endemism. Countries of particular conservation concern, because they have rich mammalian faunas containing many endemic species, are the large islands of Australia, Madagascar, Indonesia, and the Philippines, as well as continental Mexico. Patterns of recent extinctions and the current endangered status of species were difficult to interpret, largely because of inadequate and inconsistent data. The majority of officially listed endangered species are large, well known, and popular mammals, such as primates, ungulates, and carnivores, whereas the majority of species known to have gone recently extinct and likely to be currently threatened are small and inconspicuous, such as rodents and bats. Our work not only illustrates the role of ecological, evolutionary, and biogeographic processes in the origin and maintenance of land mammal diversity, it also presents the information at the level of biogeographic regions and political units where management and policy must be applied in order to slow the loss of this diversity.     

Predicting the Risk of Extinction through Hybridization

Abstract: Natural hybridization threatens a substantial number of plant and animal species with extinction, but extinction risk has been difficult to evaluate in the absence of a quantitative assessment of risk factors. We investigated a number of ecological parameters likely to affect extinction risk, through an individual-based model simulating the life cycle of two hybridizing annual plant species. All parameters tested, ranging from population size to variance in pollen-tube growth rates, affected extinction risk. The sensitivity of each parameter varied dramatically across parameter sets, but, overall, the competitive ability, initial frequency, and selfing rate of the native taxon had the strongest effect on extinction. In addition, prezygotic reproductive barriers had a stronger influence on extinction rates than did postzygotic barriers. A stable hybrid zone was possible only when habitat differentiation was included in the model. When there was no habitat differentiation, either one of the parental species or the hybrids eventually displaced the other two taxa. The simulations demonstrated that hybridization is perhaps the most rapidly acting genetic threat to endangered species, with extinction often taking place in less than five generations. The simulation model was also applied to naturally hybridizing species pairs for which considerable genetic and ecological information is available. The predictions from these "worked examples" are in close agreement with observed outcomes and further suggest that an endemic cordgrass species is threatened by hybridization. These simulations provide guidance concerning the kinds of data required to evaluate extinction risk and possible conservation strategies.