Integrating species life-history traits and patterns of deforestation in amphibian conservation planning

Aim  To identify priority areas for amphibian conservation in southeastern Brazil, by integrating species life-history traits and patterns of deforestation.
Location  State of São Paulo, Brazil.
Methods  We used the software M arxan to evaluate different scenarios of amphibian conservation planning. Our approach differs from previous methods by explicitly including two different landscape metrics; habitat split for species with aquatic larvae, and habitat loss for species with terrestrial development. We evaluated the effect of habitat requirements by classifying species breeding habitats in five categories (flowing water, still water permanent, still water temporary, bromeliad or bamboo, and terrestrial). We performed analyses using two scales, grid cells and watersheds and also considered nature preserves as protected areas.
Results  We found contrasting patterns of deforestation between coastal and inland regions. Seventy-six grid cells and 14 watersheds are capable of representing each species at least once. When accounting for grid cells already protected in state and national parks and considering species habitat requirements we found 16 high-priority grid cells for species with one or two reproductive habitats, and only one cell representing species with four habitat requirements. Key areas for the conservation of species breeding in flowing and permanent still waters are concentrated in southern state, while those for amphibians breeding in temporary ponds are concentrated in central to eastern zones. Eastern highland zones are key areas for preserving species breeding terrestrially by direct or indirect development. Species breeding in bromeliads and bamboos are already well represented in protected areas.
Main conclusions  Our results emphasize the need to integrate information on landscape configuration and species life-history traits to produce more ecologically relevant conservation strategies.     

Global amphibian declines: sorting the hypotheses

Abstract. Reports of malformed amphibians and global amphibian declines have led to public concern, particularly because amphibians are thought to be indicator species of overall environmental health. The topic also draws scientific attention because there is no obvious, simple answer to the question of what is causing amphibian declines? Complex interactions of several anthropogenic factors are probably at work, and understanding amphibian declines may thus serve as a model for understanding species declines in general. While we have fewer answers than we would like, there are six leading hypotheses that we sort into two classes. For class I hypotheses, alien species, over‐exploitation and land use change, we have a good understanding of the ecological mechanisms underlying declines; these causes have affected amphibian populations negatively for more than a century. However, the question remains as to whether the magnitude of these negative effects increased in the 1980s, as scientists began to notice a global decline of amphibians. Further, remedies for these problems are not simple. For class II hypotheses, global change (including UV radiation and global climate change), contaminants and emerging infectious diseases we have a poor, but improving understanding of how each might cause declines. Class II factors involve complex and subtle mechanistic underpinnings, with probable interactions among multiple ecological and evolutionary variables. They may also interact with class I hypotheses. Suspected mechanisms associated with class II hypotheses are relatively recent, dating from at least the middle of the 20th century. Did these causes act independently or in concert with pre‐existing negative forces of class I hypotheses to increase the rate of amphibian declines to a level that drew global attention? We need more studies that connect the suspected mechanisms underlying both classes of hypotheses with quantitative changes in amphibian population sizes and species numbers. An important step forward in this task is clarifying the hypotheses and conditions under which the various causes operate alone or together.     

Gene-flow in the clouds: landscape genetics of a viviparous,montane grassland toad in the tropics

Anthropogenic habitat alteration often increases fragmentation and isolation, which decreases population sizes and increases extinction risk for species. Extrinsic threats may be buffered or enhanced by intrinsic factors. Within amphibians, the influence of different environmental and intrinsic factors on the population structure is not yet fully understood. Four factors were found to be important for population connectivity: life history traits, recent (anthropogenic) land use history, habitat, and topography, but the direction of their influence differed between studies. Here, we examine the genetic population structure and interpopulation connectivity within the complete distribution of Nimba toads (Nimbaphrynoides occidentalis), a toad from montane tropical West Africa. The Nimba toad is the only known viviparous, matrotrophic (foetuses are nourished during the gestation by their mothers) anuran on Earth. It occurs in three regions, the smallest is situated in disturbed, the largest population in partly disturbed habitat and the third was not yet impacted. We found small, but significant population differentiation, no indication of a recent bottleneck in the smallest population, but an indication of a reduction in population sizes in the more distant past in all three populations and no sex-biased dispersal. Correlations with landscape classifications indicate that high elevations, due to their high humidity levels, are the most important landscape characteristic facilitating dispersal. This underscores desiccation risk as an important landscape characteristic for amphibian population connectivity. We found indication that life-history traits (viviparity), land use history (mining-related activity) and topography (elevation) have an influence on Nimba toad population differentiation and gene-flow.     

Evaluating multiple causes of amphibian declines of Ecuador using geographical quantitative analyses

Amphibians are declining at alarming rates worldwide; however, the causes of these declines remain somewhat elusive. Here we evaluated three major threats implicated in declines of populations and disappearance of Ecuadorian amphibians: chytridiomicosis, climate change, and habitat loss. We assessed spatial patterns of these key threats to Ecuadorian amphibians using a multi‐species database of endemic frogs along with information on the pathogen's distribution and environmental requirements, species sensitivity to climate change (indirectly based on species geographical distribution and ecological properties) and habitat loss. Our results show that amphibians display a non‐random pattern of extinction risk, both geographically and taxonomically. Further, climate change, chytridiomicosis, and their synergetic effects, are likely currently exerting the greatest impact on amphibians in Ecuador, while habitat loss does not seem to be causing precipitous declines. The most threatened species under the IUCN extinction risk categories are exactly those that appear to be the most affected by these threats. By examining multiple potential causes of amphibian threat level in a spatially explicit framework our study provides new insights about what combination of factors are most important in amphibian declines in a tropical diversity hotspot. Further, our approach and conclusions are useful for studying declines in other regions of the world.     

A comparison of understanding of the amphibian crisis by zoo visitors across three countries

Despite the global declines in the rate of amphibians, evaluation of public understanding of the crisis has not yet been carried out. We surveyed visitors (n = 1,293) at 15 zoos in Brazil, New Zealand, and the United Kingdom, using a certainty‐based assessment method to compare visitor knowledge of the global amphibian crisis. We further analyzed zoo educational material about amphibians to explore its potential to raise awareness through amphibian‐focused environmental education. Visitors in the three countries had relatively little understanding of amphibians and the global amphibian crisis. When the degree of confidence in answering the questions (high, medium, and low) is accounted for, correct answers varied between 28% and 39%. This compared to scores of between 58% and 73% when the degree of confidence in responding was not accounted for. However, specific areas of knowledge (e.g., biology, conservation, biogeography, and conceptual ideas) varied significantly across the countries. Visitors had a weaker grasp of biogeographical and conservation issues than general amphibian biology. Zoo visitors in Brazil knew less about amphibian conservation than those in New Zealand or the United Kingdom. There was less amphibian‐focused content in educational materials in zoos in Brazil than there was in the United Kingdom. Improving information about the global amphibian crisis may increase support for future conservation actions. Outreach education is one of the most important approaches in any strategic planning for conservation of species. Amphibian‐focused environmental education at institutions such as zoos and aquaria can be a crucial intervention to support amphibian conservation worldwide.     

Larval Environment Alters Amphibian Immune Defenses Differentially across Life Stages and Populations

Recent global declines, extirpations and extinctions of wildlife caused by newly emergent diseases highlight the need to improve our knowledge of common environmental factors that affect the strength of immune defense traits. To achieve this goal, we examined the influence of acidification and shading of the larval environment on amphibian skin-associated innate immune defense traits, pre and post-metamorphosis, across two populations of American Bullfrogs (Rana catesbeiana), a species known for its wide-ranging environmental tolerance and introduced global distribution. We assessed treatment effects on 1) skin-associated microbial communities and 2) post-metamorphic antimicrobial peptide (AMP) production and 3) AMP bioactivity against the fungal pathogen Batrachochytrium dendrobatidis (Bd). While habitat acidification did not affect survival, time to metamorphosis or juvenile mass, we found that a change in average pH from 7 to 6 caused a significant shift in the larval skin microbial community, an effect which disappeared after metamorphosis. Additionally, we found shifts in skin-associated microbial communities across life stages suggesting they are affected by the physiological or ecological changes associated with amphibian metamorphosis. Moreover, we found that post-metamorphic AMP production and bioactivity were significantly affected by the interactions between pH and shade treatments and interactive effects differed across populations. In contrast, there were no significant interactions between treatments on post-metamorphic microbial community structure suggesting that variation in AMPs did not affect microbial community structure within our study. Our findings indicate that commonly encountered variation in the larval environment (i.e. pond pH and degree of shading) can have both immediate and long-term effects on the amphibian innate immune defense traits. Our work suggests that the susceptibility of amphibians to emerging diseases could be related to variability in the larval environment and calls for research into the relative influence of potentially less benign anthropogenic environmental changes on innate immune defense traits.     

Amphibian diversity increases in an heterogeneous agricultural landscape

As a group amphibians are the vertebrates most affected by anthropic activity, particularly by agriculture. The rapid advance of the agricultural frontier makes it important to identify the role of agroecosystems as habitat supply for amphibians. We analyzed the differences in amphibian assemblages and populations between habitats with different plant covers and different degrees of human intervention in northwestern Argentina. For three years we conducted 114 high frequency trap samplings to quantify abundance, specific composition and species richness of amphibian assemblages in three habitat types (lemon and sugarcane crops and secondary forest) of a piedmont agroecosystem of Tucumán province. Crops hosted more species and individuals than secondary forests, but the specific composition of forest was different from that of crops suggesting that they could be complementary. Although the assemblage abundance of every observation responded to climate, the strong effect of sampling year was not related to climatic factors suggesting that there might be long term fluctuations that were not analyzed. We also found that responses to agricultural practices were species specific, so no generalizations about these practices should be done. Our study shows that cultivated areas are not hostile environments for amphibians since they can lodge huge amphibian populations and that the occurrence of disturbances associated to agricultural practices is not necessarily reflected in a decrease in the abundance and richness of amphibians in the short term. However, our results also show that forested lands are necessary to lodge some specialist species which are very rare in the croplands. This suggests that environmental heterogeneity generated by the combination of natural and cultivated patches can increase biodiversity at landscape scale because this allows the coexistence of species related to either kind of environment.     

Environmental stress as an indicator of anthropogenic impact across the African Albertine Rift: a case study using museum specimens

We examined fluctuating asymmetry (FA) and body condition (BC) as two measures of environmental stress using museum specimens of Lophuromys aquilus, a rodent species complex wide-spread across the African Albertine Rift. We related FA and BC to a spatially-derived index of anthropogenic impact using a principal components analysis (PCA). We found no relationship between the four PCA scores and mean FA or BC, but did find that FA variance was higher in areas with lower anthropogenic impact. There was also a negative, albeit non-significant, trend for PC3, suggesting that populations with higher than average BC were in areas with higher anthropogenic impact. Overall, our case study does not support FA and BC as effective predictors of environmental stress with low to moderate habitat disturbance. In fact, L. aquilus, as a habitat generalist, may be positively affected by some aspects of anthropogenic change. Studies relating environmental stress to anthropogenic impact should examine sites with a wide range of habitat qualities and human impact and utilize multiple measures of environmental stress to characterize the health of one or more populations.     

Habitat amount drives the functional diversity and nestedness of anuran communities in an Atlantic Forest fragmented landscape

Natural environments disturbed by human activities can suffer from species extinctions, but some can still harbor high taxonomic diversity. However, disturbances may have impacts beyond the species level, if the species lost represent unique functions in the ecosystem. In this study, we evaluated to what extent the amount of habitat can determine the functional diversity and nestedness of amphibian communities in an Atlantic Forest fragmented landscape in Brazil, and if there is a threshold of habitat amount beyond which there is severe loss of functional diversity. As species responses may depend on their habitat type, we performed the analyses for three different sets of species: all species, forest‐dependent species, and generalist species. We also evaluated the relative importance of turnover and nestedness components to total functional dissimilarity among sites. Habitat amount affected functional diversity of frogs, especially for forest‐dependent species where a linear reduction was detected. The functional dissimilarity among sites was mostly explained by the nestedness component. The reduction of functional diversity was mediated by an ordered loss of traits, leading to a functionally nested metacommunity. These sensitive traits were closely related to habits and reproductive modes that depend on rivers and streams. The maintenance of functional diversity of frogs in fragmented landscapes must rely on the conservation of both terrestrial and aquatic environments, as some species and their traits can disappear from remnants of native vegetation lacking some specific habitats (e.g. streams). Abstract in Portuguese is available with online material.     

Movement ecology of Afrotropical birds: Functional traits provide complementary insights to species identity

Effects of anthropogenic activities on habitats and species communities and populations are complex and vary across species depending on their ecological traits. Movement ecology may provide important insights into species’ responses to habitat structures and quality. We investigated how movement behavior across a human‐modified landscape depends on species identity and species traits, with particular focus on habitat specialization, feeding guilds, and dispersal behavior. We tracked 34 individuals of nine Afrotropical bird species during three years in an anthropogenic riparian landscape of East Africa. We investigated whether species’ functional traits predicted their habitat use and movement behavior better than species’ identities. Our results indicate that habitat specialists mainly occur in dense riparian thickets, while habitat generalists do occur in agricultural land. Home‐ranges of omnivorous habitat generalists are larger than of frugivorous and insectivorous generalists and omnivorous and insectivorous specialists. Movement speed was highest in settlement areas for all species, with activity peaks during morning and afternoon for habitat specialists. Our results reveal that functional traits and species identity provide complementary insights into responses of organisms to habitat structures and habitat quality.     

Interaction between breeding habitat and elevation affects prevalence but not infection intensity of Batrachochytrium dendrobatidis in Brazilian anuran assemblages

Chytridiomycosis, an infectious disease of amphibians, is caused by the fungus Batrachochytrium dendrobatidis (Bd) and has been linked to declining amphibian populations worldwide. The susceptibility of amphibians to chytridiomycosis-induced population declines is potentially influenced by many factors, including environmental characteristics, differences among host species and the growth of the pathogen itself. We investigated the effects of elevation and breeding habitat on Bd prevalence and individual infection intensity (zoospore loads) in 3 anuran assemblages of the Atlantic Coastal Forest of Brazil. Bd infection intensity was strongly influenced by elevation and breeding habitat, but we found no evidence of an interaction between those 2 variables in explaining the number of zoospores sampled from individual frogs. In contrast, Bd infection odds were predicted by elevation and by an interaction between elevation and breeding habitat, such that frogs had a higher probability of Bd infection in lotic habitats at low elevations. Our results indicate that Bd persists across a wide variety of habitats and elevations in the Atlantic Coastal Forest. Prevalence and infection intensity of Bd are highest at high elevations where overall environmental conditions for Bd are most favorable. In addition, at low elevations amphibian host habitat choice is also an important determinant of infection. Our study highlights the need to investigate interacting variables of host ecology and the environment simultaneously.     

Evolutionarily distinct amphibians are disproportionately lost from human‐modified ecosystems

Humans continue to alter terrestrial ecosystems, but our understanding of how biodiversity responds is still limited. Anthropogenic habitat conversion has been associated with the loss of evolutionarily distinct bird species at local scales, but whether this evolutionary pattern holds across other clades is unknown. We collate a global dataset on amphibian assemblages in intact forests and nearby human‐modified sites to assess whether evolutionary history influences susceptibility to land conversion. We found that evolutionarily distinct amphibian species are disproportionately lost when forested habitats are converted to alternative land‐uses. We tested the hypothesis that grassland‐associated amphibian lineages have both higher diversification and are pre‐adapted to human landscapes, but found only weak evidence supporting this. The loss of evolutionarily distinct amphibians with land conversion suggests that preserving remnant forests will be vital if we aim to preserve the amphibian tree of life in the face of mounting anthropogenic pressures.     

Measuring the meltdown: drivers of global amphibian extinction and decline

Habitat loss, climate change, over-exploitation, disease and other factors have been hypothesised in the global decline of amphibian biodiversity. However, the relative importance of and synergies among different drivers are still poorly understood. We present the largest global analysis of roughly 45% of known amphibians (2,583 species) to quantify the influences of life history, climate, human density and habitat loss on declines and extinction risk. Multi-model Bayesian inference reveals that large amphibian species with small geographic range and pronounced seasonality in temperature and precipitation are most likely to be Red-Listed by IUCN. Elevated habitat loss and human densities are also correlated with high threat risk. Range size, habitat loss and more extreme seasonality in precipitation contributed to decline risk in the 2,454 species that declined between 1980 and 2004, compared to species that were stable (n = 1,545) or had increased (n = 28). These empirical results show that amphibian species with restricted ranges should be urgently targeted for conservation.     

Global stressors and the global decline of amphibians: tipping the stress immunocompetency axis

There is a widespread consensus that the earth is experiencing a mass extinction event and at the forefront are amphibians, the most threatened of all vertebrate taxa. A recent assessment found that nearly one-third (32%, 1,856 species) of the world’s amphibian species are threatened. Amphibians have existed on the earth for over 300 million years, yet in just the last two decades there have been an alarming number of extinctions, nearly 168 species are believed to have gone extinct and at least 2,469 (43%) more have populations that are declining. Infectious diseases have been recognized as one major cause of worldwide amphibian population declines. This could be the result of the appearance of novel pathogens, or it could be that exposure to environmental stressors is increasing the susceptibility of amphibians to opportunistic pathogens. Here I review the potential effects of stressors on disease susceptibility in amphibians and relate this to disease emergence in human and other wildlife populations. I will present a series of case studies that illustrate the role of stress in disease outbreaks that have resulted in amphibian declines. First, I will examine how elevated sea-surface temperatures in the tropical Pacific since the mid-1970s have affected climate over much of the world and could be setting the stage for pathogen-mediated amphibian declines in many regions. Finally, I will discuss how the apparently rapid increase in the prevalence of amphibian limb deformities is linked to the synergistic effects of trematode infection and exposure to chemical contaminants.     

A small increase in UV-B increases the susceptibility of tadpoles to predation

Increased ultraviolet-B (UV-B) radiation as a consequence of ozone depletion is one of the many potential drivers of ongoing global amphibian declines. Both alone and in combination with other environmental stressors, UV-B is known to have detrimental effects on the early life stages of amphibians, but our understanding of the fitness consequences of these effects remains superficial. We examined the independent and interactive effects of UV-B and predatory chemical cues (PCC) on a suite of traits of Limnodynastes peronii embryos and tadpoles, and assessed tadpole survival time in a predator environment to evaluate the potential fitness consequences. Exposure to a 3 to 6 per cent increase in UV-B, which is comparable to changes in terrestrial UV-B associated with ozone depletion, had no effect on any of the traits measured, except survival time in a predator environment, which was reduced by 22 to 28 per cent. Exposure to PCC caused tadpoles to hatch earlier, have reduced hatching success, have improved locomotor performance and survive for longer in a predator environment, but had no effect on tadpole survival, behaviour or morphology. Simultaneous exposure to UV-B and PCC resulted in no interactive effects. These findings demonstrate that increased UV-B has the potential to reduce tadpole fitness, while exposure to PCCs improves their fitness.     

Pond-Breeding Amphibian Species Richness and Habitat Selection in a Beaver-Modified Landscape

ABSTRACT Beaver (Castor canadensis) activity creates wetland habitats with varying hydroperiods important in maintaining habitat diversity for pond-breeding amphibians with significantly different breeding habitat requirements. We documented pond-breeding amphibian assemblages in 71 freshwater wetlands in Acadia National Park, Maine, USA. Using 15 variables describing local pond conditions and wetland landscape characteristics, we developed a priori models to predict sites with high amphibian species richness and used model selection with Akaike's Information Criterion to judge the strength of evidence supporting each model. We developed single-species models to predict wood frog (Rana sylvatica), bullfrog (R. catesbeiana), and pickerel frog (R. palustris) breeding site selection. Sites with high species richness were best predicted by 1) connectivity of wetlands in the landscape through stream corridors and 2) wetland modification by beaver. Wood frog breeding habitat was best predicted by temporary hydroperiod, lack of fish, and absence of current beaver activity. Wood frog breeding was present in abandoned beaver wetlands nearly as often as in nonbeaver wetlands. Bullfrog breeding was limited to active beaver wetlands with fish and permanent water. Pickerel frog breeding sites were best predicted by connectivity through stream corridors within the landscape. As beavers have recolonized areas of their former range in North America, they have increased the number and diversity of available breeding sites in the landscape for pond-breeding amphibians. The resulting mosaic of active and abandoned beaver wetlands both supports rich amphibian assemblages and provides suitable breeding habitat for species with differing habitat requirements. Land managers should consider the potential benefits of minimal management of beavers in promoting and conserving amphibian and wetland diversity at a landscape scale.     

Chytridiomycosis, Amphibian Extinctions, and Lessons for the Prevention of Future Panzootics

The human-mediated transport of infected amphibians is the most plausible driver for the intercontinental spread of chytridiomycosis, a recently emerged infectious disease responsible for amphibian population declines and extinctions on multiple continents. Chytridiomycosis is now globally ubiquitous, and it cannot be eradicated from affected sites. Its rapid spread both within and between continents provides a valuable lesson on preventing future panzootics and subsequent erosion of biodiversity, not only of amphibians, but of a wide array of taxa: the continued inter-continental trade and transport of animals will inevitably lead to the spread of novel pathogens, followed by numerous extinctions. Herein, we define and discuss three levels of amphibian disease management: (1) post-exposure prophylactic measures that are curative in nature and applicable only in a small number of situations; (2) pre-exposure prophylactic measures that reduce disease threat in the short-term; and (3) preventive measures that remove the threat altogether. Preventive measures include a virtually complete ban on all unnecessary long-distance trade and transport of amphibians, and are the only method of protecting amphibians from disease-induced declines and extinctions over the long-term. Legislation to prevent the emergence of new diseases is urgently required to protect global amphibian biodiversity.     

Ecological consequences of amphibian larvae and their native and alien predators on the community structure of temporary ponds

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Effects of nutrient supplementation on host‐pathogen dynamics of the amphibian chytrid fungus: a community approach

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Amphibians as models for studying environmental change

The use of amphibians as models in ecological research has a rich history. From an early foundation in studies of amphibian natural history sprang generations of scientists who used amphibians as models to address fundamental questions in population and community ecology. More recently, in the wake of an environment that human disturbances rapidly altered, ecologists have adopted amphibians as models for studying applied ecological issues such as habitat loss, pollution, disease, and global climate change. Some of the characteristics of amphibians that make them useful models for studying these environmental problems are highlighted, including their trophic importance, environmental sensitivity, research tractability, and impending extinction. The article provides specific examples from the recent literature to illustrate how studies on amphibians have been instrumental in guiding scientific thought on a broad scale. Included are examples of how amphibian research has transformed scientific disciplines, generated new theories about global health, called into question widely accepted scientific paradigms, and raised awareness in the general public that our daily actions may have widespread repercussions. In addition, studies on amphibian declines have provided insight into the complexity in which multiple independent factors may interact with one another to produce catastrophic and sometimes unpredictable effects. Because of the complexity of these problems, amphibian ecologists have been among the strongest advocates for interdisciplinary research. Future studies of amphibians will be important not only for their conservation but also for the conservation of other species, critical habitats, and entire ecosystems.