Synergistic effects of the invasive Chinese tallow (Triadica sebifera) and climate change on aquatic amphibian survival

Changes in climate and the introduction of invasive species are two major stressors to amphibians, although little is known about the interaction between these two factors with regard to impacts on amphibians. We focused our study on an invasive tree species, the Chinese tallow (Triadica sebifera), that annually sheds its leaves and produces leaf litter that is known to negatively impact aquatic amphibian survival. The purpose of our research was to determine whether the timing of leaf fall from Chinese tallow and the timing of amphibian breeding (determined by weather) influence survival of amphibian larvae. We simulated a range of winter weather scenarios, ranging from cold to warm, by altering the relative timing of when leaf litter and amphibian larvae were introduced into aquatic mesocosms. Our results indicate that amphibian larvae survival was greatly affected by the length of time Chinese tallow leaf litter decomposes in water prior to the introduction of the larvae. Larvae in treatments simulating warm winters (early amphibian breeding) were introduced to the mesocosms early in the aquatic decomposition process of the leaf litter and had significantly lower survival compared with cold winters (late amphibian breeding), likely due to significantly lower dissolved oxygen levels. Shifts to earlier breeding phenology, linked to warming climate, have already been observed in many amphibian taxa, and with most climate models predicting a significant warming trend over the next century, the trend toward earlier breeding should continue if not increase. Our results strongly suggest that a warming climate can interact with the effects of invasive plant species, in ways we have not previously considered, to reduce the survival of an already declining group of organisms.     

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.     

The frog filter: amphibian introduction bias driven by taxonomy,body size and biogeography

Aim Invasive species often exhibit a highly non‐random suite of traits relative to non‐invasive taxa, and these biases reflect strong selection at a series of steps along the invasion pathway. Here we investigate traits that are favoured in the first of these steps: the introduction of species outside their native geographic range. We use the global introduction of amphibians as our case study. Location Global. Methods We examined whether taxonomy, body size and attributes of the native geographic range predict the likelihood of an introduction event in amphibians. We then determined whether these characteristics differed between amphibian species that have been introduced intentionally and those that have been introduced unintentionally (i.e. stowaways). Results Comparisons of introduced and non‐introduced amphibians reveal significant biases with respect to taxonomic position (c. 50% of all introduced species originate from only 5% of all families), and characteristics of the native geographic range (most introduced species originate from the Northern Hemisphere, occupy a wide geographic range and are sympatric with high densities of humans). Many of these biases presumably reflect the ease and likelihood of capturing and transporting such animals. Additionally, intentionally introduced species are of larger than average body size, occupy higher elevations in their native ranges, and are more likely to originate from the Northern Hemisphere than unintentionally introduced species. Main conclusions Introduced amphibian species are not a random subset of the global amphibian fauna with respect to taxonomic affiliation and biogeography, and this restricts our ability to make robust generalizations regarding the ecological determinants of introduction success. Nevertheless, many of our findings are similar to those revealed by previous analyses of vertebrate and invertebrate introductions. Thus, our study suggests that biases in the anthropogenic mechanisms involved in transporting species around the globe are surprisingly consistent across broadly divergent taxa.     

An examination of amphibian sensitivity to environmental contaminants: are amphibians poor canaries?

Nearly two decades ago, the global biodiversity crisis was catapulted to the front pages of newspapers with the recognition of worldwide amphibian declines. Amphibians earned their appellation, 'canaries in a coal mine', because of apparent high sensitivity to human-mediated environmental change. The most frequently cited causes for high susceptibility include permeable skin, a dual aquatic-terrestrial life cycle and a relatively rudimentary immune system. While some researchers have questioned the basis for the canary assertion, there has been no systematic evaluation of amphibian sensitivity to environmental challenges relative to other taxa. Here, we apply a database representing thousands of toxicity tests to compare the responses of amphibians relative to that of other taxonomic groups. The use of standardized methods combined with large numbers of identical challenges enables a particularly powerful test of relative effect size. Overall, we found that amphibians only exhibit moderate relative responses to water-borne toxins. Our findings imply that, as far as chemical contaminants are concerned, amphibians are not particularly sensitive and might more aptly be described as 'miners in a coal mine'. To the extent that amphibian declines have been mediated by chemical contaminants, our findings suggest that population losses and extinctions may have already occurred in a variety of taxa much more sensitive than amphibians.
Ecology Letters (2010) 13: 60–67     

A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians

The extant amphibians are one of the most diverse radiations of terrestrial vertebrates (>6800 species). Despite much recent focus on their conservation, diversification, and systematics, no previous phylogeny for the group has contained more than 522 species. However, numerous studies with limited taxon sampling have generated large amounts of partially overlapping sequence data for many species. Here, we combine these data and produce a novel estimate of extant amphibian phylogeny, containing 2871 species (∼40% of the known extant species) from 432 genera (∼85% of the ∼500 currently recognized extant genera). Each sampled species contains up to 12,712 bp from 12 genes (three mitochondrial, nine nuclear), with an average of 2563 bp per species. This data set provides strong support for many groups recognized in previous studies, but it also suggests non-monophyly for several currently recognized families, particularly in hyloid frogs (e.g., Ceratophryidae, Cycloramphidae, Leptodactylidae, Strabomantidae). To correct these and other problems, we provide a revised classification of extant amphibians for taxa traditionally delimited at the family and subfamily levels. This new taxonomy includes several families not recognized in current classifications (e.g., Alsodidae, Batrachylidae, Rhinodermatidae, Odontophrynidae, Telmatobiidae), but which are strongly supported and important for avoiding non-monophyly of current families. Finally, this study provides further evidence that the supermatrix approach provides an effective strategy for inferring large-scale phylogenies using the combined results of previous studies, despite many taxa having extensive missing data.     

Amphibians in Eurasian otter Lutra lutra diet: osteological identification unveils hidden prey richness and male‐biased predation on anurans

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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.     

Current status of the threatened amphibians and reptiles of Japan

This article compares amphibian and reptile components of the original and revised versions of the Red List of Japan, and analyzes geographic patterns of, and major threats to, species and subspecies now assigned to the threatened categories. The numbers of both amphibians and reptiles categorized as threatened in the Red List of Japan have increased greatly through its revision as a result of recent progress in the taxonomy of these groups in Japan, the introduction of new criteria for risk assessment, and unexpectedly rapid declines in the status of several taxa. Threatened taxa of amphibians and reptiles in the revised list tend to be concentrated in the Ryukyu Archipelago, where deforestation seems to be the major ultimate cause of declines. Reduction in the quality and quantity of inland water environments seems to be the major cause of declines in several endemic amphibians from the main islands of Japan. The importance of conservation was emphasized in the revised list by progress in taxonomy, by new insights and data on the estimation of temporal dynamics of population density or habitat size for threatened taxa, and by the impacts of and need to prevent further deforestation in the Ryukyus and of the ongoing destruction of inland water habitats on the main islands of Japan. Received: May 6, 1999 / Accepted: October 26, 1999     

Population differentiation of temperate amphibians in unpredictable environments

Amphibians are a globally distributed and diverse lineage, but much of our current understanding of their population genetic structure comes from studies in mesic temperate habitats. We characterize the population genetic structure of two sympatric explosive breeding amphibians in the southwestern deserts of the United States: the Great Plains toad ( Anaxyrus cognatus ) and Couch's spadefoot toad ( Scaphiopus couchii ). For both species, we find limited genetic differentiation even between populations in adjacent valleys separated by dispersal barriers such as mountainous habitats. To understand how population genetic patterns in these two arid-adapted species compare to taxa in more mesic environments, we computed a standardized measure of population differentiation for A. cognatus , S. couchii , and for pond-breeding amphibians that inhabit mesic temperate environments. Our results indicate that the arid-adapted species have lower population genetic structure at fine and moderate scales than most other amphibian species we surveyed. We hypothesize that stochasticity in the availability of appropriate breeding sites as well as landscape homogeneity may result in increased population connectivity in desert-adapted frogs. Future work examining fine-scale population structure in amphibians from a diversity of habitats will test the generality of our findings. Intraspecific comparisons among localities with varied seasonality and habitats will be particularly useful for investigating the interaction between species-typical population dynamics and environmental characteristics as determinants of population connectivity in pond-breeding amphibians.     

Strong correlation between cross-amplification success and genetic distance across all members of 'True Salamanders' (Amphibia: Salamandridae) revealed by Salamandra salamandra-specific microsatellite loci

The unpredictable and low cross-amplification success of microsatellite loci tested for congeneric amphibian species has mainly been explained by the size and complexity of amphibian genomes, but also by taxonomy that is inconsistent with phylogenetic relationships among taxa. Here, we tested whether the cross-amplification success of nine new and 11 published microsatellite loci cloned for an amphibian source species, the fire salamander (Salamandra salamandra), correlated with the genetic distance across all members of True Salamanders (genera Chioglossa, Lyciasalamandra, Mertensiella and Salamandra that form a monophyletic clade within the family of Salamandridae) serving as target species. Cross-amplification success varied strongly among the species and showed a highly significant negative relationship with genetic distance and amplification success. Even though lineages of S. salamandra and Lyciasalamndra have separated more than 30 Ma, a within genus amplification success rate of 65% was achieved for species of Lyciasalamandra thus demonstrating that an efficient cross-species amplification of microsatellite loci in amphibians is feasible even across large evolutionary distances. A decrease in genome size, on the other hand, paralleled also a decrease in amplified loci and therefore contradicted previous results and expectations that amplification success should increase with a decrease in genome size. However, in line with other studies, our comprehensive dataset clearly shows that cross-amplification success of microsatellite loci is well explained by phylogenetic divergence between species. As taxonomic classifications on the species and genus level do not necessarily mirror phylogenetic divergence between species, the pure belonging of species to the same taxonomic units (i.e. species or genus) might be less useful to predict cross-amplification success of microsatellite loci between such species.     

Genetic comparison of water molds from embryos of amphibians Rana cascadae, Bufo boreas and Pseudacris regilla

Water molds that cause the disease saprolegniasis have been implicated in widespread mortality of amphibian embryos. However, because of the limitations of traditional identification methods, water mold species involved in die-offs or utilized in ecological studies often remain unidentified or identified only as Saprolegnia ferax. Furthermore, water mold taxonomy requires revision, so very distinct organisms may all be called S. ferax. Recent DNA-based studies indicate that the diversity of water molds infecting amphibian embryos is significantly higher than what was previously known, but these studies rely on culture methods, which may be biased towards taxa that grow best under laboratory conditions. In this study, total embryo-associated DNA was extracted from 3 amphibian species in a pond in central Washington, USA. The internal transcribed spacer (ITS) region of DNA was amplified with primers capable of amplifying a broad array of eukaryotic microorgansisms, and was used to construct clone libraries. Individual clones were sequenced and relationships among newly recovered sequences and previously studied taxa were analyzed using phylogenetics. These methods recovered several new taxa in association with amphibian embryos. Samples grouped into 11 distinct phylotypes with ITS sequence differences ranging from 4 to 28%. The water mold communities recovered differed among Rana cascadae, Bufo boreas, and Pseudacris regilla egg masses. Furthermore, the diversity of water molds increased as egg masses aged, and members comprising this diversity changed over time.     

Amphibians do not follow Bergmann's rule

The tendency for organisms to be larger in cooler climates (Bergmann's rule) is widely observed in endotherms, and has been reputed to apply to some ectotherms including amphibians. However, recent reports provide conflicting support for the pattern, questioning whether Bergmann's clines are generally present in amphibians. In this study, we measured 96,996 adult Plethodon from 3974 populations to test for the presence of Bergmann's clines in these salamanders. Only three Plethodon species exhibited a significant negative correlation between body size and temperature consistent with Bergmann's rule, whereas 37 of 40 species did not display a pattern consistent with this prediction. Further, a phylogenetic comparative analysis found no relationship between body size and temperature among species. A meta-analysis combining our data with the available data for other amphibian species revealed no support for Bergmann's rule at the genus (Plethodon), order (Caudata), or class (Amphibia) levels. Our findings strongly suggest that negative thermal body size clines are not common in amphibians, and we conclude that Bergmann's rule is not generally applicable to these taxa. Thus, evolutionary explanations of Bergmann's clines in other tetrapods need not account for unique life-history attributes of amphibians.     

The Lower Mekong: an insurmountable barrier to amphibians in southern Indochina?

Geographical information system (GIS)‐based cluster analyses and comparative ecological approaches were applied to unravel the hitherto controversially discussed role of the Mekong River as a biogeographical barrier to the amphibian fauna in Indochina. Referring to the unique and independent history of the Lower Mekong, south of the Lao–Cambodian border, this approach focused on the amphibians of southern Indochina and adjacent parts of eastern Thailand. To date, 131 amphibian species have been recorded from this region. In concordance with previous studies, our GIS‐based analyses revealed that the amphibian fauna of the Cardamom Mountains, west of the Mekong, possessed no closer affinity to the herpetofauna of the Southern Annamites. In addition, a statistical comparison of ecological characters showed an occurrence of ecological differentiation among amphibians across the Lower Mekong. Our results suggest that the Lower Mekong serves as, or at least coincides with, a biogeographical barrier in southern Indochina. Here, we discuss this hypothesis, together with selected species spatial distribution patterns, their species‐specific ecological traits and the palaeogeographical background of the region. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 905–914.     

Models of climate associations and distributions of amphibians in Italy

Analyzing the relationships between the distribution of animal species and climatic variables is not only important for understanding which factors govern species distribution but also for improving our ability to predict future ecological responses to climate change. In the context of global climate change, amphibians are of particular interest because of their extreme sensitivity to the variation of temperature and precipitation regimes. We analyzed species–climate relationships for 17 amphibian species occurring in Italy using species distribution data at the 10 × 10 km resolution. A machine learning method, Random Forests, was used to model the distribution of amphibians in relation to a set of 18 climatic variables. The results showed that the variables which had the highest importance were those related to precipitation, indicating that precipitation is an important factor in determining amphibian distribution. Future projections showed a complex response of species distributions, emphasizing the potential severity of climate change on the distributions of amphibians in Italy. The species that will decrease the most are those occurring in mountainous and Mediterranean areas. Our results provide some preliminary information that could be useful for amphibian conservation, indicating if future conservation priorities for some species should be enhanced.     

Amphibian diversity in Polish cities: Taxonomic diversity,functional diversity and evolutionary distinctiveness

As a process affecting animal communities, urbanization has been the subject of numerous studies. However, amphibians are still among the least studied vertebrate groups in urbanized landscapes. Generally, it has been found that the process of loss of amphibian diversity is nonrandom, with species from older evolutionary lines at greater risk. Regional data on amphibian assemblages in urban areas is a very useful tool for assessing how these assemblages react to changes.The aim of the present paper is to assess the diversity of amphibians in Polish cities based on data in the relevant literature, exploring different metrics (e.g., taxonomic, functional, and evolutionary diversity) calculated in amphibian species assemblages. We used data from 18 articles (including grey literature), characterized by comparable research methods and published between 1999 and 2017.Overall, amphibian species richness (ASR) amounted to an average of 9 species, ranging from 5 to 11 species per city. The higher species richness occurred in Białystok in North-west of Poland. Functional evenness (FEve), evolutionary distinctiveness (ED sum), and functional richness (FRic) were strongly positively correlated with ASR. However, ED mean was not significantly correlated with the total number of species in the community. Three taxa, the hybridogenetic water frogs Pelophylax esculentus complex, the common toad Bufo bufo, and the common frog Rana temporaria, occurred in all analyzed amphibian assemblages. Our study is one of the first attempts to compare urban amphibian assemblages, using different and complementary diversity metrics on a large spatial scale. In conclusion, we highlight that urban areas play an important role for conservation of amphibians, because they support amphibian assemblages characterized by a high level of overall diversity.     

A molecular phylogenetic study of the genus Ribeiroia (Digenea): trematodes known to cause limb malformations in amphibians

Species of Ribeiroia (Trematoda: Psilostomidae) are known to cause severe limb malformations and elevated mortality in amphibians. However, little is known regarding the number of species in this genus or its relation to other taxa. Species of Ribeiroia have historically been differentiated by slight differences among their larval stages. To better understand the systematics and biogeography of this genus and their potential relevance to the distribution of malformed amphibians, specimens identified as Ribeiroia were collected across much of the known range, including samples from 5 states in the United States (8 sites) and 2 islands in the Caribbean (Puerto Rico and Guadeloupe). A cercaria from East Africa identified as Cercaria lileta (Fain, 1953), with attributes suggestive of Ribeiroia (possibly R. congolensis), was also examined. The intertranscribed spacer region 2 (ITS-2) of the ribosomal gene complex was sequenced and found to consist of 429 nucleotides (nt) for R. ondatrae (United States) and 427 nt for R. marini (Caribbean), with only 6 base differences noted between the 2 species. The ITS-2 region of C. lileta (429 nt) aligned closely with those of the 2 other Ribeiroia species in a phylogenetic analysis that included related trematode genera. This evidence suggests that a third Ribeiroia species exists in tropical Africa. Variation in ITS-2 within R. ondatrae was nonexistent among the 8 populations from North America. Our study further suggests that Ribeiroia spp. originally parasitized Biomphalaria sp., and that a host switch to a closely related snail, Helisoma sp., may have occurred in the lineage represented by R. ondatrae. However, relationships within the Echinostomatidae are not understood well enough to make any robust conclusions at this time.     

Climate change and amphibian declines: is there a link?

Abstract. Global climates have been changing, sometimes rapidly and dramatically, throughout the evolutionary history of amphibians. Therefore, existing amphibian species have been derived from those that have survived major climatic disturbances. Although recent global climate change has resulted in warming in many regions, temperatures in some areas to date have not changed measurably, or have even cooled. Declines of some amphibian populations have been correlated with climate events, but demonstrations of direct causal relationships need further research. Data are available indicating some indirect effect of climate change on the initiation of breeding activities of some amphibians that occur earlier than in previous springs, but the costs and benefits of these changes are just beginning to be investigated. Climate may also play an indirect role in facilitating epidemics of infectious disease. Regardless of the role that climate changes may have played in past and current amphibian declines, future shifts in climate, should they prove as dramatic as predicted, will certainly pose challenges for surviving amphibian populations and for successful recovery efforts of species that have suffered declines.     

Examining the evidence for chytridiomycosis in threatened amphibian species

Extinction risks are increasing for amphibians due to rising threats and minimal conservation efforts. Nearly one quarter of all threatened/extinct amphibians in the IUCN Red List is purportedly at risk from the disease chytridiomycosis. However, a closer look at the data reveals that Batrachochytrium dendrobatidis (the causal agent) has been identified and confirmed to cause clinical disease in only 14% of these species. Primary literature surveys confirm these findings; ruling out major discrepancies between Red List assessments and real-time science. Despite widespread interest in chytridiomycosis, little progress has been made between assessment years to acquire evidence for the role of chytridiomycosis in species-specific amphibian declines. Instead, assessment teams invoke the precautionary principle when listing chytridiomycosis as a threat. Precaution is valuable when dealing with the world's most threatened taxa, however scientific research is needed to distinguish between real and predicted threats in order to better prioritize conservation efforts. Fast paced, cost effective, in situ research to confirm or rule out chytridiomycosis in species currently hypothesized to be threatened by the disease would be a step in the right direction. Ultimately, determining the manner in which amphibian conservation resources are utilized is a conversation for the greater conservation community that we hope to stimulate here.     

Taxonomic selectivity in amphibians: ignorance, geography or biology?

Many taxa, including amphibians, have been shown to have a taxonomically non-random distribution of threatened species. There are three possible non-exclusive reasons for this selectivity: non-random knowledge of species conservation status, clades endemic to different regions experiencing different intensities of threatening process and the effects of clade-specific biological attributes on the susceptibility of species to these processes. This paper tests the sufficiency of the first two explanations using extinction risk evaluations from the 2004 Global Amphibian Assessment. Our results indicate that they cannot alone account for the degree of non-randomness in extinction risk among amphibian families. The overall distribution of threatened amphibians remained taxonomically non-random when species of unknown conservation status were omitted, and significant selectivity was detected not only at a global geographic scale but also in country- and site-specific data sets. Furthermore, the same families tend to be over- or underthreatened within different countries. Together, these results suggest that biological differences among amphibian families play an important role in determining species' susceptibility to anthropogenic threatening processes.