Effects of UV‐B Radiation on Anti‐Predator Behavior in Amphibians: Reply to Cummins

Cummins' (2002) criticism of our paper ( Kats et al. 2000 ) (1) displays a lack of understanding of experimental biology, (2) fails to report our results accurately, (3) places our paper in the wrong context, (4) seems unaware of much of the pertinent literature or selectively avoids certain references, and (5) takes the opportunity to criticize other papers examining the effects of ultraviolet radiation (UV, particularly UV‐B) on amphibians in the field. We address these issues below.     

Effects of UV-B Radiation on Anti-predator Behavior in Three Species of Amphibians

Ultraviolet radiation has been suggested as a possible contributing cause of amphibian declines around the world. Both laboratory and field studies have demonstrated that exposure to ultraviolet radiation can lead to increased mortality of developing amphibians. Virtually no studies have examined the sub‐lethal effects of ultraviolet on amphibian behavior. In this study, we examine the anti‐predator behavior of three species of amphibians after short‐term exposure to ultraviolet‐B radiation. Toad (Bufo boreas) juveniles that had been exposed to ultraviolet radiation did not respond to chemical extracts from conspecifics and heterospecifics as much as juveniles that had not been exposed. Both newt larvae (Taricha granulosa) that had been exposed to ultraviolet radiation and those that had not been exposed responded to chemical cues from conspecific predators by increasing the amount of time spent in shelter. Frog tadpoles (Rana cascadae) that had been exposed to ultraviolet radiation did not reduce their movement in response to chemical cues from predators as much as tadpoles that had not been exposed. These results indicate that ultraviolet exposure may have important sub‐lethal effects in amphibians that could adversely effect their fitness.     

Risk of predation enhances the lethal effects of UV‐B in amphibians

Amphibian declines are a prominent part of the global biodiversity crisis and have received special consideration because they have occurred relatively recently, on a global scale, and in seemingly pristine habitats where no obvious anthropogenic cause is apparent. Although several causes for declines have been implicated, the isolation of a singular cause has proven elusive. Consequently, it has been hypothesized that complex interactions between multiple environmental stressors, particularly those associated with global change, may be responsible. Increasing ultraviolet‐B radiation (UV‐B) associated with stratospheric ozone depletion is one such stressor that has received considerable attention. UV‐B causes enhanced lethal effects when combined with other factors such as aquatic pH, contaminants, temperature and pathogens, but little is known of how UV‐B interacts with pervasive biological stressors, such as risk of predation. We exposed Limnodynastes peronii tadpoles to UV‐B and predatory chemical cues in a controlled laboratory experiment to determine their independent and interactive effects on survival and morphology. We show that UV‐B and risk of predation interact synergistically to enhance mortality above the additive effects of the independent stressors, and that exposure to UV‐B affects the ability of tadpoles to morphologically respond to predatory chemical cues (i.e. predator‐induced phenotypic plasticity), which has implications for their survival in an environment with predators. This highlights the importance of considering both anthropogenic and naturally occurring stressors when examining the underlying causes of amphibian declines.     

Sub‐lethal UV‐C radiation induces callose,hydrogen peroxide and defence‐related gene expression in Arabidopsis thaliana

Exposure of plants to UV‐C irradiation induces gene expression and cellular responses that are commonly associated with wounding and pathogen defence, and in some cases can lead to increased resistance against pathogen infection. We examined, at a physiological, molecular and biochemical level, the effects of and responses to, sub‐lethal UV‐C exposure on Arabidopsis plants when irradiated with increasing dosages of UV‐C radiation. Following UV‐C exposure plants had reduced leaf areas over time, with the severity of reduction increasing with dosage. Severe morphological changes that included leaf glazing, bronzing and curling were found to occur in plants treated with the 1000 J·m^?2 dosage. Extensive damage to the mesophyll was observed, and cell death occurred in both a dosage‐ and time‐dependent manner. Analysis of H₂O₂ activity and the pathogen defence marker genes PR1 and PDF1.2 demonstrated induction of these defence‐related responses at each UV‐C dosage tested. Interestingly, in response to UV‐C irradiation the production of callose (β‐1,3‐glucan) was identified at all dosages examined. Together, these results show plant responses to UV‐C irradiation at much lower doses than have previously been reported, and that there is potential for the use of UV‐C as an inducer of plant defence.     

Chemical profiling of mycosporine‐like amino acids in twenty‐three red algal species

Rhodophyta produce a variety of chemically different mycosporine‐like amino acids (MAAs), compounds that are known as some of the strongest ultraviolet (UV) absorbing molecules in nature. Accordingly, they primarily act as photoprotectants against harmful levels of solar ultraviolet radiation in the UV‐A and UV‐B range. In order to get a deeper understanding of the chemical diversity of MAAs in red algae, pure standards of eleven mycosporine‐like amino acids were isolated from three different species (Agarophyton chilense, Pyropia plicata and Champia novae‐zelandiae) using various chromatographic methods. Their structures were confirmed by nuclear magnetic resonance and mass spectrometry. Four out of the eleven MAAs are reported for the first time in algae. In addition, a new high‐performance liquid chromatography method was developed for the separation of all isolated MAAs and successfully applied for the analysis of twenty‐three red algal species of marine origin. All of them contained MAAs, the most abundant compounds were shinorine, palythine, asterina‐330 and porphyra‐334. For some samples, the direct assignment of MAAs based on their UV spectra was not possible; therefore, the target analytes were enriched by a simple concentration step, followed by liquid chromatography‐mass spectrometry analysis of the extracts. This approach enabled a deeper insight into the MAA pattern of red algae, indicating that not only the four dominant ones are synthesized but also many others, which were often described as unknown compounds in previous studies.     

Long‐term monitoring of an amphibian community after a climate change‐ and infectious disease‐driven species extirpation

Infectious disease and climate change are considered major threats to biodiversity and act as drivers behind the global amphibian decline. This is, to a large extent, based on short‐term studies that are designed to detect the immediate and strongest biodiversity responses to a threatening process. What few long‐term studies are available, although typically focused on single species, report outcomes that often diverge significantly from the short‐term species responses. Here, we report the results of an 18‐year survey of an amphibian community exposed to both climate warming and the emergence of lethal chytridiomycosis. Our study shows that the impacts of infectious disease are ongoing but restricted to two out of nine species that form the community, despite the fact all species can become infected with the fungus. Climate warming appears to be affecting four out of the nine species, but the response of three of these is an increase in abundance. Our study supports a decreasing role of infectious disease on the community, and an increasing and currently positive effect of climate warming. We caution that if the warming trends continue, the net positive effect will turn negative as amphibian breeding habitat becomes unavailable as water bodies dry, a pattern that already may be underway.     

Clade‐specific consequences of climate change to amphibians in Atlantic Forest protected areas

The rapid global decline of amphibian population is alarming because many occur for apparently unknown or enigmatic reasons, even inside protected areas (PAs). Some studies have predicted the effects of climate change on amphibians’ distribution and extinction, but the relationship and consequences of climate change to the phylogenetic structure of amphibian assemblages remain obscure. By applying robust techniques for ecological niche modeling and a cutting‐edge approach on community phylogenetics, here, we evaluate how climate change affects the geographical pattern of amphibian species richness and phylogenetic diversity in the Atlantic Forest Biodiversity Hotspot, Brazil, as well as how the phylogenetic composition of amphibian assemblages respond to climate change. We found that most species contracted their ranges and that such responses are clade specific. Basal amphibian clades (e.g. Gymnophiona and Pipidae) were positively affected by climate change, whereas late‐divergent clades (e.g. Cycloramphidae, Centrolenidae, Eleutherodactylidae, Microhylidae) were severely impacted. Identifying major changes in the phylogenetic pool represents a first step towards a better understanding of how assembly processes related to climate change will affect ecological communities. A deep analysis of the impacts of climate change not only on species, but also on the evolutionary relationships among species might foster the discussion on clade‐level conservation priorities for this imperiled fauna.     

Beneficial effects of solar UV‐B radiation on soybean yield mediated by reduced insect herbivory under field conditions

Ultraviolet‐B radiation (UV‐B: 280–315 nm) has damaging effects on cellular components and macromolecules. In plants, natural levels of UV‐B can reduce leaf area expansion and growth, which can lead to reduced productivity and yield. UV‐B can also have important effects on herbivorous insects. Owing to the successful implementation of the Montreal Protocol, current models predict that clear‐sky levels of UV‐B radiation will decline during this century in response to ozone recovery. However, because of climate change and changes in land use practices, future trends in UV doses are difficult to predict. In the experiments reported here, we used an exclusion approach to study the effects of solar UV‐B radiation on soybean crops, which are extensively grown in many areas of the world that may be affected by future variations in UV‐B radiation. In a first experiment, performed under normal management practices (which included chemical pest control), we found that natural levels of UV‐B radiation reduced soybean yield. In a second experiment, where no pesticides were applied, we found that solar UV‐B significantly reduced insect herbivory and, surprisingly, caused a concomitant increase in crop yield. Our data support the idea that UV‐B effects on agroecosystems are the result of complex interactions involving multiple trophic levels. A better understanding of the mechanisms that mediate the anti‐herbivore effect of UV‐B radiation may be used to design crop varieties with improved adaptation to the cropping systems that are likely to prevail in the coming decades in response to agricultural intensification.     

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

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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.     

Global increases in ultraviolet B radiation: potential impacts on amphibian development and metamorphosis

Levels of ultraviolet B radiation (UVBR) reaching the Earth's surface have increased since the 1970s as a result of stratospheric ozone depletion caused by the emission of ozone-depleting substances (ODSs) such as chlorofluorocarbons. Despite international agreements to phase out harmful ODSs, these substances are persistent, and even under the most optimistic scenarios, stratospheric ozone levels will not return to pre-1980 levels for several decades. Furthermore, climate change may enhance chemical stratospheric ozone depletion. Global phenomena such as climate change, ozone depletion, and acidification of aquatic ecosystems interact to modify dissolved organic carbon levels in aquatic systems, thereby increasing the penetration of UVBR. Since amphibians inhabit both aquatic and terrestrial habitats and have unshelled eggs and permeable skin, they are vulnerable to changes in environmental conditions and habitat quality. Increased exposure of amphibians to UVBR can produce lethal and sublethal effects, especially in individuals that do not possess adequate defense mechanisms to protect themselves. In this article, we discuss worldwide increases in UVBR and the adverse effects of UVBR exposure on amphibians. Specifically, studies on the effects of UVBR on amphibian development and metamorphosis are summarized, and possible mechanisms of thyroid system disruption caused by UVBR exposure are considered.     

Phylogenetic distribution of symbiotic bacteria from Panamanian amphibians that inhibit growth of the lethal fungal pathogen Batrachochytrium dendrobatidis

The introduction of next‐generation sequencing has allowed for greater understanding of community composition of symbiotic microbial communities. However, determining the function of individual members of these microbial communities still largely relies on culture‐based methods. Here, we present results on the phylogenetic distribution of a defensive functional trait of cultured symbiotic bacteria associated with amphibians. Amphibians are host to a diverse community of cutaneous bacteria and some of these bacteria protect their host from the lethal fungal pathogen Batrachochytrium dendrobatidis (Bd) by secreting antifungal metabolites. We cultured over 450 bacterial isolates from the skins of Panamanian amphibian species and tested their interactions with Bd using an in vitro challenge assay. For a subset of isolates, we also completed coculture experiments and found that culturing isolates with Bd had no effect on inhibitory properties of the bacteria, but it significantly decreased metabolite secretion. In challenge assays, approximately 75% of the bacterial isolates inhibited Bd to some extent and these inhibitory isolates were widely distributed among all bacterial phyla. Although there was no clear phylogenetic signal of inhibition, three genera, Stenotrophomonas, Aeromonas and Pseudomonas, had a high proportion of inhibitory isolates (100%, 77% and 73%, respectively). Overall, our results demonstrate that antifungal properties are phylogenetically widespread in symbiotic microbial communities of Panamanian amphibians and that some functional redundancy for fungal inhibition occurs in these communities. We hope that these findings contribute to the discovery and development of probiotics for amphibians that can mitigate the threat of chytridiomycosis.     

Survival of three species of anuran metamorphs exposed to UV-B radiation and the pathogenic fungus Batrachochytrium dendrobatidis

When exploring the possible factors contributing to population declines, it is necessary to consider multiple, interacting environmental stressors. Here, we investigate the impact of 2 factors, ultraviolet radiation and disease, on the survival of anuran amphibians. Exposure to ultraviolet-B (UV-B) radiation increases mortality and results in various sub-lethal effects for many amphibian species. Infectious diseases can also negatively impact amphibian populations. In this study, we exposed metamorphic individuals (metamorphs) to both UV-B and Batrachochytrium dendrobatidis (BD), a fungal pathogen and cause of the disease chytridiomycosis, and monitored survival for 3 wk. We tested for possible interactions between UV-B and BD in 3 species: the Cascades frog Rana cascadae; the Western toad Bufo boreas; and the Pacific treefrog Hyla regilla. We found strong interspecific differences in susceptibility to BD. For example, R. cascadae suffered a large increase in mortality when exposed to BD; B. boreas also experienced mortality, but this effect was small relative to the R. cascadae response. H. regilla did not show any decrease in survival when exposed to either factor. No synergistic interactions between UV-B and BD were found for any of the test species. A previous study investigating the impact of BD on larval amphibians showed different species responses (Blaustein et al. 2005a). Our results highlight the importance of studying multiple life history stages when determining the impact of environmental stressors. The contrast between these 2 studies emphasizes how vulnerability to a pathogen can vary between life history stages within a single species.     

Comparison of regression methods for spatially‐autocorrelated count data on regularly‐ and irregularly‐spaced locations

It has long been known that insufficient consideration of spatial autocorrelation leads to unreliable hypothesis‐tests and inaccurate parameter estimates. Yet, ecologists are confronted with a confusing array of methods to account for spatial autocorrelation. Although Beale et al. (2010) provided guidance for continuous data on regular grids, researchers still need advice for other types of data in more flexible spatial contexts. In this paper, we extend Beale et al. (2010)‘s work to count data on both regularly‐ and irregularly‐spaced plots, the latter being commonly encountered in ecological studies. Through a simulation‐based approach, we assessed the accuracy and the type I errors of two frequentist and two Bayesian ready‐to‐use methods in the family of generalized mixed models, with distance‐based or neighbourhood‐based correlated random effects. In addition, we tested whether the methods are robust to spatial non‐stationarity, and over‐ and under‐dispersion – both typical features of species distribution count data which violate standard regression assumptions. In the simplest of our simulated datasets, the two frequentist methods gave inflated type I errors, while the two Bayesian methods provided satisfying results. When facing real‐world complexities, the distance‐based Bayesian method (MCMC with Langevin–Hastings updates) performed best of all. We hope that, in the light of our results, ecological researchers will feel more comfortable including spatial autocorrelation in their analyses of count data.     

Limited polymorphism of the functional MHC class II B gene in the black‐spotted frog (Pelophylax nigromaculatus) identified by locus‐specific genotyping

Amphibians can be more vulnerable to environmental changes and diseases than other species because of their complex life cycle and physiological requirements. Therefore, understanding the adaptation of amphibians to environmental changes is crucial for their conservation. Major histocompatibility complex (MHC) presents an excellent tool for the investigation of adaptive variations and the assessment of adaptive potential because it can be under strong diversifying selection. Here, we isolated the MHC class II B (MHCIIB) gene from cDNA sequences of the black‐spotted frog (Pelophylax nigromaculatus), a widespread amphibian species in China, and designed locus‐specific primers to characterize adaptive variability of this amphibian. Ten alleles were identified from 67 individual frogs of three populations and no more than two alleles were present in each individual animal. Furthermore, none of the sequences had indels or/and stop codons, which is in good agreement with locus‐specific amplification of a functional gene. However, we found low polymorphism at both nucleotide and amino acid levels, even in the antigen‐binding region. Purifying selection acting at this locus was supported by the findings that the d_N/d_S ratio across all alleles was below 1 and that negatively selected sites were detected by different methods. Allele frequency distributions were significantly different among geographic populations, indicating that physiographic factors may have strong effect on the genetic structure of the black‐spotted frog. This study revealed limited polymorphism of three adjacent black‐spotted frog populations at the functional MHCIIB locus, which may be attributed to region‐specific differences. The locus‐specific genotyping technique developed in this study would provide a foundation for future studies on adaptive divergence among different frog populations.     

Effects of an infectious fungus, Batrachochytrium dendrobatidis, on amphibian predator-prey interactions

The effects of parasites and pathogens on host behaviors may be particularly important in predator-prey contexts, since few animal behaviors are more crucial for ensuring immediate survival than the avoidance of lethal predators in nature. We examined the effects of an emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis, on anti-predator behaviors of tadpoles of four frog species. We also investigated whether amphibian predators consumed infected prey, and whether B. dendrobatidis caused differences in predation rates among prey in laboratory feeding trials. We found differences in anti-predator behaviors among larvae of four amphibian species, and show that infected tadpoles of one species (Anaxyrus boreas) were more active and sought refuge more frequently when exposed to predator chemical cues. Salamander predators consumed infected and uninfected tadpoles of three other prey species at similar rates in feeding trials, and predation risk among prey was unaffected by B. dendrobatidis. Collectively, our results show that even sub-lethal exposure to B. dendrobatidis can alter fundamental anti-predator behaviors in some amphibian prey species, and suggest the unexplored possibility that indiscriminate predation between infected and uninfected prey (i.e., non-selective predation) could increase the prevalence of this widely distributed pathogen in amphibian populations. Because one of the most prominent types of predators in many amphibian systems is salamanders, and because salamanders are susceptible to B. dendrobatidis, our work suggests the importance of considering host susceptibility and behavioral changes that could arise from infection in both predators and prey.     

Density‐dependent and density‐independent drivers of population change in Barton Springs salamanders

Understanding population change is essential for conservation of imperiled species, such as amphibians. Worldwide amphibian declines have provided an impetus for investigating their population dynamics, which can involve both extrinsic (density‐independent) and intrinsic (density‐dependent) drivers acting differentially across multiple life stages or age classes. In this study, we examined the population dynamics of the endangered Barton Springs Salamander (Eurycea sosorum) using data from a long‐term monitoring program. We were interested in understanding both the potential environmental drivers (density‐independent factors) and demographic factors (interactions among size classes, negative density dependence) to better inform conservation and management activities. We used data from three different monitoring regimes and multivariate autoregressive state‐space models to quantify environmental effects (seasonality, discharge, algae, and sediment cover), intraspecific interactions among three size classes, and intra‐class density dependence. Results from our primary data set revealed similar patterns among sites and size classes and were corroborated by our out‐of‐sample data. Cross‐correlation analysis showed juvenile abundance was most strongly correlated with a 9‐month lag in aquifer discharge, which we suspect is related to inputs of organic carbon into the aquifer. However, sedimentation limited juvenile abundance at the surface, emphasizing the importance of continued sediment management. Recruitment from juveniles to the sub‐adult size class was evident, but negative density‐dependent feedback ultimately regulated each size class. Negative density dependence may be an encouraging sign for the conservation of E. sosorum because populations that can reach carrying capacity are less likely to go extinct compared to unregulated populations far below their carrying capacity. However, periodic population declines coupled with apparent migration into the aquifer complicate assessments of species status. Although both density‐dependent and density‐independent drivers of population change are not always apparent in time series of animal populations, both have important implications for conservation and management of E. sosorum.     

Motile Zoospores of Batrachochytrium dendrobatidis Move Away from Antifungal Metabolites Produced by Amphibian Skin Bacteria

Chytridiomycosis is an amphibian skin disease that threatens amphibian biodiversity worldwide. The fungal agent of chytridiomycosis is Batrachochytrium dendrobatidis. There is considerable variation in disease outcomes such that some individuals and populations co-exist with the fungus and others quickly succumb to disease. Amphibians in populations that co-exist with the B. dendrobatidis have sublethal infections on their skins. Symbiotic skin bacteria have been shown in experiments and surveys to play a role in protecting amphibians from chytridiomycosis. Little is known about the mechanisms that antifungal skin bacteria use to ameliorate the effects of B. dendrobatidis. In this study, we identified that B. dendrobatidis isolate JEL 310 zoospores display chemotaxis, in the presence of two bacterially-produced metabolites (2,4-diacetylphloroglucinol and indole-3-carboxaldehyde). In the presence of either metabolite, B. dendrobatidis zoospores move more frequently away from the metabolite. Using parameters estimated from this study, a simple stochastic model of a random walk on a lattice was evaluated. The model shows that these individual behaviors over short time-scales directly lead to population behaviors over long time–scales, such that most zoospores will escape, or not infect a tryptone substrate containing the bacterially-produced metabolite, whereas many zoospores will infect the tryptone substrate containing no metabolite. These results suggest that amphibians that have skin bacteria produce antifungal metabolites that might be able to keep B. dendrobatidis infections below the lethal threshold and thus are able to co-exist with the fungus.     

Application of local gene induction by infrared laser‐mediated microscope and temperature stimulator to amphibian regeneration study

Urodele amphibians (newts and salamanders) and anuran amphibians (frogs) are excellent research models to reveal mechanisms of three‐dimensional organ regeneration since they have exceptionally high regenerative capacity among tetrapods. However, the difficulty in manipulating gene expression in cells in a spatially restricted manner has so far hindered elucidation of the molecular mechanisms of organ regeneration in amphibians. Recently, local heat shock by laser irradiation has enabled local gene induction even at the single‐cell level in teleost fishes, nematodes, fruit flies and plants. In this study, local heat shock was made with infrared laser irradiation (IR‐LEGO) by using a gene expression inducible system in transgenic animals containing a heat shock promoter, and gene expression was successfully induced only in the target region of two amphibian species, Xenopus laevis and Pleurodeles waltl (a newt), at postembryonic stages. Furthermore, we induced spatially restricted but wider gene expression in Xenopus laevis tadpoles and froglets by applying local heat shock by a temperature‐controlled metal probe (temperature stimulator). The local gene manipulation systems, the IR‐LEGO and the temperature stimulator, enable us to do a rigorous cell lineage trace with the combination of the Cre‐LoxP system as well as to analyze gene function in a target region or cells with less off‐target effects in the study of amphibian regeneration.     

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

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