A review of chemical ecology in poison frogs

Herein we review what is known about the chemical ecology of poison frogs with a focus on dendrobatid poison frogs. While five anuran families are known to have an alkaloid-derived chemical defense, the dendrobatids have been studied in greatest detail and provides chemical ecologists with a complex model system for understanding how chemical defenses operate in real time and may have evolved through evolutionary time. We describe the diversity of alkaloid defenses known from frogs, alkaloid sequestration, biosynthesis and modification, and we review what is known concerning arthropod sources for alkaloids. There is variation in nearly every attribute of the system and we try to describe some of the challenges associated with unraveling the complexities of this model system.     

Impact of Invasive Cane Toads on Australian Birds

Abstract: The cane toad (Bufo marinus), a large, toxic, American anuran, was introduced to Australia in 1935. Populations of many of Australia's reptiles (snakes, varanid lizards, crocodiles) and carnivorous mammals (dasyurid marsupials) have declined because these predators are killed by the toad's powerful toxins. In contrast to these well‐studied species, little is known about the cane toads impacts on Australian birds. We reviewed published and unpublished data on behavioral interactions between Australian avian predators and cane toads and collated distributional and dietary information to identify avian taxa potentially at risk from cane toad invasion. Cane toads are sympatric with 172 frog‐eating bird species in Australia, and an additional 8 bird species overlap with the predicted future range of the toad. Although many bird species thus are potentially at risk, behavioral observations suggest the risk level is generally low. Despite occasional reports of Australian birds being killed when they ingest cane toads, most birds either ignore toads or survive the predation event. The apparently higher tolerance of Australian birds to toad toxins, compared with Australian reptiles and marsupials, may reflect genetic exchange between Australian birds and Asian populations that encounter other bufonid species regularly and hence have evolved the capacity to recognize or tolerate this toxic prey.     

Effects of Economic Prosperity on Numbers of Threatened Species

Abstract: We used data from over 100 countries to investigate the link between numbers of threatened species and per-capita gross national product. We corrected for factors that might otherwise confound such a relationship. Our study was motivated by the continuing debate over the relationship between environmental degradation and per-capita income. Proponents of the environmental Kuznets-curve hypothesis argue that although environmental degradation may increase initially, increases in per-capita income will eventually result in greater environmental quality. Theoretical objections and the lack of widespread empirical evidence recently have thrown doubt on the existence of such a pattern. Treating threat to biodiversity as one potential indicator of environmental degradation, we divided threatened species into seven taxonomic groups ( plants, mammals, birds, amphibians, reptiles, fishes, and invertebrates) and analyzed each group separately. Count-data regression analysis indicated that the number of threatened species was related to per-capita gross national product in five of seven taxonomic groups. Birds were the only taxonomic group in which numbers of threatened species decreased throughout the range of developed countries' per-capita gross national product. Plants, amphibians, reptiles, and invertebrates showed increasing numbers of threatened species throughout this same range. If these relationships hold, increasing numbers of species from several taxonomic groups are likely to be threatened with extinction as countries increase in prosperity. A key challenge is to understand the interactions among consumer preferences, biology, and institutions that lead to the relationship observed for birds and to see whether this knowledge can be applied to conservation of other taxa.     

Predators usurp prey defenses? Toxicokinetics of tetrodotoxin in common garter snakes after consumption of rough-skinned newts

Snakes are common predators of organisms, such as amphibians, with toxic defenses that can be lethal to other predators. Because snakes do not have the option of dissecting prey into edible versus inedible components, they face a full dose of any chemical defenses encountered during attempted predation. This limitation has likely resulted in intense selection favoring the evolution of alternative mechanisms for dealing with prey toxins. These mechanisms can be physiological (e.g., resistance to prey toxins) or behavioral (e.g., toxin sampling and rejection). When physiological resistance arises, the possibility of bioaccumulation of a toxin results. We examined the coevolutionary interaction between the common garter snake (Thamnophis sirtalis) and the rough-skinned newt (Taricha granulosa), which contains a powerful neurotoxin called tetrodotoxin (TTX). In some populations syntopic with newts, individuals of T. sirtalis have evolved resistance to TTX. We examined the persistence of TTX in T. sirtalis after administration of an oral dose of TTX to investigate the possibility that snakes are sequestering TTX. The half-life of TTX in snake liver was estimated at 8.1?days. Accordingly, clearance of 99% of a single dose of TTX averages 61?days. Negative fitness consequences of intoxication during and after newt consumption may be balanced by co-opting the newts?? chemical defense for protection from the snakes?? own predators. Accounting of the coevolutionary dynamic between snakes and newts must incorporate post-consumption affects of lingering TTX.     

Chemical investigations of defensive steroid sequestration by the Asian snake Rhabdophis tigrinus

Rhabdophis tigrinus is an Asian natricine snake that possesses unusual defensive glands on the dorsal surface of its neck. These nuchal glands typically contain cardiotonic steroidal toxins known as bufadienolides, which are also abundant in the skin of toads. Feeding experiments demonstrated that toads consumed as prey are the ultimate sources of the bufadienolides in nuchal glands of R. tigrinus. Indeed, snakes on a toad-free Japanese island (Kinkasan, Miyagi Prefecture) lack these compounds in their nuchal glands, confirming that these snakes are unable to synthesize defensive bufadienolides. However, when snakes from Kinkasan are fed toads in the laboratory, they accumulate bufadienolides in their nuchal glands, indicating that they have not lost the ability to sequester defensive compounds from prey. In contrast, R. tigrinus from a toad-rich island (Ishima, Tokushima Prefecture) possess large quantities of bufadienolides, reflecting the abundance of toads from which these compounds can be sequestered. Feeding experiments involving gravid R. tigrinus demonstrated that bufadienolides can be provisioned to offspring so that hatchlings are chemically defended before their first toad meal. Maternal provisioning of bufadienolides can take place through two routes: by deposition in yolk and by diffusion in utero, even late in gestation. We applied bufadienolides to the surface of eggs from Kinkasan and found that the embryos are able to take up these compounds into their nuchal glands, demonstrating the feasibility of uptake across the eggshell. Female R. tigrinus provision bufadienolides to their offspring in direct proportion to their own level of chemical defense. By feeding toad-derived bufotoxins to R. tigrinus hatchlings, we determined that the sequestration of these compounds involves at least three types of modification: hydrolytic cleavage of suberylarginine side chains, hydroxylation, and epimerization.     

Influence of Forest Fragmentation on Community Structure of Frogs and Lizards in Northeastern Costa Rica

Abstract:  To better understand responses of reptiles and amphibians to forest fragmentation in the lowland Neotropics, we examined community and population structure of frogs and lizards in the fragmented landscape surrounding La Selva Biological Station in the Sarapiquí region of northeastern Costa Rica. We used diurnal quadrats and nocturnal transects to sample frogs and lizards in nine forest fragments (1–7 ha each) and La Selva (1100 ha). Species richness in all fragments combined was 85% of that found in La Selva with comparable sampling effort. Richness varied from 10 to 24 species among forest fragments, compared with 36 species at La Selva. Lizard density was higher and frog density was lower in forest fragments than in La Selva. Community composition varied among sites and by fragment size class, and species occurrence was nested with respect to fragment area. Isolation and habitat variables did not significantly affect species richness, composition, or nestedness. We classified 34% of species as fragmentation sensitive because they were absent or occurred at low densities in fragments. Nevertheless, the relatively high diversity observed in the entire set of fragments indicates that preserving a network of small forest patches may be of considerable conservation value to the amphibians and reptiles of this region.     

Species Inequality in Scientific Study

Abstract: Some conservationists argue for a focused effort to protect the most critically endangered species, and others suggest a large‐scale endeavor to safeguard common species across large areas. Similar arguments are applicable to the distribution of scientific effort among species. Should conservation scientists focus research efforts on threatened species, common species, or do all species deserve equal attention? We assessed the scientific equity among 1909 mammals, birds, reptiles, and amphibians of southern Africa by relating the number of papers written about each species to their status on the International Union for Conservation of Nature Red List. Threatened large mammals and reptiles had more papers written about them than their nonthreatened counterparts, whereas threatened small mammals and amphibians received less attention than nonthreatened species. Threatened birds received an intermediate amount of attention in the scientific literature. Thus, threat status appears to drive scientific effort among some animal groups, whereas other factors (e.g., pest management and commercial interest) appear to dictate scientific investment in particular species of other groups. Furthermore, the scientific investment per species differed greatly between groups—the mean number of papers per threatened large mammal eclipsed that of threatened reptiles, birds, small mammals, and amphibians by 2.6‐, 15‐, 216‐, and more than 500‐fold, respectively. Thus, in the eyes of science, all species are not created equal. A few species commanded a great proportion of scientific attention, whereas for many species information that might inform conservation is virtually nonexistent.     

Food and feeding of Amphiesma stolatum (Linnaeus 1758)

The food and feeding behaviour of Amphiesma stolatum was studied. A total of 117 snakes were examined to analyse the diet composition. Ten live snakes were maintained in enclosure for evaluating the feeding habit, choice of food and rate of assimilation. The anurans constituted the major diet of the food spectrum. In captivity, fishes (fry), amphibians and reptiles were consumed by the snakes. A. stolatum exihibited Elaphe type of hunting behaviour. In most cases the snake struck the prey at its head. The assimilation rate with frog was highest.     

The effectiveness of surrogate taxa to conserve freshwater biodiversity

Establishing protected areas has long been an effective conservation strategy and is often based on readily surveyed species. The potential of any freshwater taxa to be a surrogate for other aquatic groups has not been explored fully. We compiled occurrence data on 72 species of freshwater fishes, amphibians, mussels, and aquatic reptiles for the Great Plains, Wyoming (U.S.A.). We used hierarchical Bayesian multispecies mixture models and MaxEnt models to describe species’ distributions and the program Zonation to identify areas of conservation priority for each aquatic group. The landscape‐scale factors that best characterized aquatic species’ distributions differed among groups. There was low agreement and congruence among taxa‐specific conservation priorities (<20%), meaning no surrogate priority areas would include or protect the best habitats of other aquatic taxa. Common, wideranging aquatic species were included in taxa‐specific priority areas, but rare freshwater species were not included. Thus, the development of conservation priorities based on a single freshwater aquatic group would not protect all species in the other aquatic groups.     

Relationships between Plant and Animal Species Richness at a Regional Scale in China

Abstract:  Important questions in conservation biology and ecology include whether species diversities of different groups of organisms are correlated and, in particular, whether plant diversity influences animal diversity. I used correlation and partial regression analyses to examine the relationships between species richness of vascular plants and four major groups of terrestrial vertebrates (mammals, amphibians, reptiles, and birds) in 28 provinces in China. Species richness data were obtained from the literature. Environmental variables included normalized difference vegetation index, mean January temperature, mean annual temperature, annual precipitation, May through August precipitation, actual evapotranspiration, potential evapotranspiration, and elevation range. Species richness was strongly and positively correlated among the five groups of organisms. Plant richness was correlated with animal richness more strongly than the richness of different animal groups correlated with each other except for reptile richness, which had a slightly higher correlation with amphibian richness than with plant richness. Plant richness uniquely explained 41 times more variance in the species richness of the four vertebrate groups combined than environmental variables uniquely did, suggesting that plant richness influences terrestrial vertebrate richness at the regional scale examined. Because of strong correlations between the diversity of vascular plants and vertebrates, the diversity of vascular plants may be used as a surrogate for the diversity of terrestrial animals in China. My results have implications for selection of areas to be protected at both regional and local scales.     

A Meta-Analysis of the Effects of Ultraviolet B Radiation and Its Synergistic Interactions with pH, Contaminants, and Disease on Amphibian Survival

Abstract:  Human alterations to natural systems have resulted in a loss of biological diversity around the world. Amphibian population losses have been more severe than those of birds and mammals. Amphibian population declines are likely due to many factors including habitat loss, disease, contaminants, introduced species and ultraviolet-B (UVB) radiation. The effect of UVB, however, varies widely among species and can vary within populations of the same species or at different life-history stages. This variation has often led to opposing conclusions about how UVB affects amphibians. We used meta-analysis techniques to explore the overall effects of UVB radiation on survival in amphibians. We also used recently developed factorial meta-analytic techniques to quantify potential interactions between UVB radiation and other stressors on amphibians. Ultraviolet-B radiation reduced survival of amphibians by 1.9-fold compared with shielded controls. Larvae were more susceptible to damage from UVB radiation compared with embryos, and salamanders were more susceptible compared with frogs and toads. Furthermore, UVB radiation interacted synergistically with other environmental stressors and resulted in greater than additive effects on survival when 2 stressors were present. Our results suggest that UVB radiation is an important stressor in amphibians, particularly in light of potential synergisms between UVB and other stressors in amphibian habitats.     

Rarity of Organisms in the Sand Pine Scrub Habitat of Florida

Naturalists conceive of "rare" organisms as those narrow in geographic range, restricted to few habitats, or small in population sizes. Because rare organisms may be rare in a variety of ways, a particular conservation strategy that purports to protect them may not do so effectively in all cases; therefore, categorization of rarity in advance could help ensure that the chosen strategy has a reasonable chance of success in a particular case. We placed plants, amphibians, and reptiles resident in the Sand Pine scrub habitat of Florida into categories of rarity. Determining if and in what way a particular organism is rare proved difficult, because the process requires exact specification of what is meant by "narrow,""restricted," and "small." Furthermore, the process requires choice of a scale for judging rarity and relies upon data that are likely to be of variable availability and reliability. We categorized rarity by several schemes, and they produced distributions of taxa among categories of rarity that largely were similar to one another but that diverged in telling ways. The distributions of taxa among categories of rarity produced by any scheme were different for scrub plants than for scrub amphibians and reptiles. Likewise, these distributions were different than those produced by previously published studies of rarity. We found that the results of our categorization schemes did not match particularly well with the official listing of scrub organisms as endangered or potentially endangered.     

Assessing the Potential Impact of Cane Toads on Australian Snakes

Abstract:   Cane toads ( Bufo marinus ) are large, highly toxic anurans that were introduced into Australia in 1937. Anecdotal reports suggest that the invasion of toads into an area is followed by dramatic declines in the abundance of terrestrial native frog-eating predators, but quantitative studies have been restricted to nonpredator taxa or aquatic predators and have generally reported minimal impacts. Will toads substantially affect Australian snakes? Based on geographic distributions and dietary composition, we identified 49 snake taxa as potentially at risk from toads. The impact of these feral prey also depends on the snakes' ability to survive after ingesting toad toxins. Based on decrements in locomotor (swimming) performance after ingesting toxin, we estimate the LD₅₀ of toad toxins for 10 of the at-risk snake species. Most species exhibited a similar low ability to tolerate toad toxins. Based on head widths relative to sizes of toads, we calculate that 7 of the 10 taxa could easily ingest a fatal dose of toxin in a single meal. The exceptions were two colubrid taxa (keelbacks [  Tropidonophis mairii ] and slatey-grey snakes [  Stegonotus cucullatus ]) with much higher resistance to toad toxins (up to 85-fold) and one elapid (swamp snakes [  Hemiaspis signata ]) with low resistance but a small relative head size and thus low maximum prey size. Overall, our analysis suggests that cane toads threaten populations of approximately 30% of terrestrial Australian snake species.     

The ecological impact of invasive cane toads on tropical snakes: field data do not support laboratory-based predictions

Predicting which species will be affected by an invasive taxon is critical to developing conservation priorities, but this is a difficult task. A previous study on the impact of invasive cane toads (Bufo marinus) on Australian snakes attempted to predict vulnerability a priori based on the assumptions that any snake species that eats frogs, and is vulnerable to toad toxins, may be at risk from the toad invasion. We used time-series analyses to evaluate the accuracy of that prediction, based on >3600 standardized nocturnal surveys over a 138-month period on 12 species of snakes and lizards on a floodplain in the Australian wet-dry tropics, bracketing the arrival of cane toads at this site. Contrary to prediction, encounter rates with most species were unaffected by toad arrival, and some taxa predicted to be vulnerable to toads increased rather than declined (e.g., death adder Acanthophis praelongus; Children's python Antaresia childreni). Indirect positive effects of toad invasion (perhaps mediated by toad-induced mortality of predatory varanid lizards) and stochastic weather events outweighed effects of toad invasion for most snake species. Our study casts doubt on the ability of a priori desktop studies, or short-term field surveys, to predict or document the ecological impact of invasive species.     

The roles of climate, phylogenetic relatedness, introduction effort, and reproductive traits in the establishment of non-native reptiles and amphibians

We developed a method to predict the potential of non-native reptiles and amphibians (herpetofauna) to establish populations. This method may inform efforts to prevent the introduction of invasive non-native species. We used boosted regression trees to determine whether nine variables influence establishment success of introduced herpetofauna in California and Florida. We used an independent data set to assess model performance. Propagule pressure was the variable most strongly associated with establishment success. Species with short juvenile periods and species with phylogenetically more distant relatives in regional biotas were more likely to establish than species that start breeding later and those that have close relatives. Average climate match (the similarity of climate between native and non-native range) and life form were also important. Frogs and lizards were the taxonomic groups most likely to establish, whereas a much lower proportion of snakes and turtles established. We used results from our best model to compile a spreadsheet-based model for easy use and interpretation. Probability scores obtained from the spreadsheet model were strongly correlated with establishment success as were probabilities predicted for independent data by the boosted regression tree model. However, the error rate for predictions made with independent data was much higher than with cross validation using training data. This difference in predictive power does not preclude use of the model to assess the probability of establishment of herpetofauna because (1) the independent data had no information for two variables (meaning the full predictive capacity of the model could not be realized) and (2) the model structure is consistent with the recent literature on the primary determinants of establishment success for herpetofauna. It may still be difficult to predict the establishment probability of poorly studied taxa, but it is clear that non-native species (especially lizards and frogs) that mature early and come from environments similar to that of the introduction region have the highest probability of establishment.     

Nuchal glands: a novel defensive system in snakes

Of the various chemical defensive adaptations of vertebrates, nuchal glands are among the most unusual. First described in a Japanese natricine snake, Rhabdophis tigrinus, in 1935, these organs are embedded under the skin of the neck region as a series of paired glands that have neither lumina nor ducts. The major chemical components of the glandular fluid are bufadienolides, which are cardiotonic steroids also found in the skin secretion of toads. Here we review early studies of nuchal glands and briefly introduce our recent findings on the sequestration of bufadienolides from consumed toads and the maternal provisioning of those sequestered compounds. We summarize behavioral studies associated with the antipredator function of the nuchal glands, which have been conducted during our more than decade-long collaboration. Results of preliminary analyses on the possible costs of toad-eating and on the ultrastructure of the nuchal glands are also presented. Finally, we discuss the evolutionary origin of the nuchal glands and suggest future directions designed to understand the biological importance of these novel vertebrate organs, which have evolved in a limited number of snake species.     

Effects of climate change and anthropogenic activity on ranges of vertebrate species endemic to the Qinghai–Tibet Plateau over 40 years

Over the past 40 years, the climate has been changing and human disturbance has increased in the vast Qinghai–Tibet Plateau (QTP). These 2 factors are expected to affect the distribution of a large number of endemic vertebrate species. However, quantitative relationships between range shifts and climate change and human disturbance of these species in the QTP have rarely been evaluated. We used occurrence records of 19 terrestrial vertebrate species (birds, mammals, amphibians, and reptiles) occurring in the QTP from 1980 to 2020 to quantify the effects of climate change and anthropogenic impacts on the distribution of these 4 taxonomic groups and estimated species range changes in each species. The trend in distribution changes differed among the taxonomic groups, although, generally, ranges shifted to central QTP. Climate change contributed more to range variation than human disturbance (the sum of the 4 climatic variables contributed more than the sum of the 4 human disturbance variables for all 4 taxonomic groups). Suitable geographic range increased for most mammals, amphibians, and reptiles (+27.6%, +18.4%, and +27.8% on average, respectively), whereas for birds range decreased on average by 0.9%. Quantitative evidence for climate change and human disturbance associations with range changes for endemic vertebrate species in the QTP can provide useful insights into biodiversity conservation under changing environments.     

Chemical defenses, nutritional quality, and structural components in three sponge species: Ircinia felix, I. campana, and Aplysina fulva

Allocating chemical defenses to regions or tissues most at risk for predatory attack may provide protection while simultaneously minimizing associated metabolic costs. Chemical defense allocation patterns were investigated in the aspiculate sponges Ircinia felix, I. campana, and Aplysina fulva collected between July 2005 and April 2006 from J Reef off the coast of Georgia, U.S.A. It was predicted that chemical defenses would be (1) higher in the outermost 2 mm layer of the sponge; (2) positively correlated with tissue nutritional quality; and (3) correlated with structural components such as spongin fibers. Whereas defensive chemicals were concentrated in the outer 2 mm of A. fulva, the Ircinia species had higher concentrations in deeper tissue layers. Furthermore, no significant positive or negative correlation between chemical defenses and nutritional quality or levels of structural components was observed in these sponges. Overall, these results do not support the prediction that predation pressure by fish and large mobile invertebrates significantly impacts chemical defense allocation in these sponges.     

Benefits to poorly studied taxa of conservation of bird and mammal diversity on islands

Protected area delineation and conservation action are urgently needed on marine islands, but the potential biodiversity benefits of these activities can be difficult to assess due to lack of species diversity information for lesser known taxa. We used linear mixed effects modeling and simple spatial analyses to investigate whether conservation activities based on the diversity of well‐known insular taxa (birds and mammals) are likely to also capture the diversity of lesser known taxa (reptiles, amphibians, vascular land plants, ants, land snails, butterflies, and tenebrionid beetles). We assembled total, threatened, and endemic diversity data for both well‐known and lesser known taxa and combined these with physical island biogeography characteristics for 1190 islands from 109 archipelagos. Among physical island biogeography factors, island area was the best indicator of diversity of both well‐known and little‐known taxa. Among taxonomic factors, total mammal species richness was the best indicator of total diversity of lesser known taxa, and the combination of threatened mammal and threatened bird diversity was the best indicator of lesser known endemic richness. The results of other intertaxon diversity comparisons were highly variable, however. Based on our results, we suggest that protecting islands above a certain minimum threshold area may be the most efficient use of conservation resources. For example, using our island database, if the threshold were set at 10 km² and the smallest 10% of islands greater than this threshold were protected, 119 islands would be protected. The islands would range in size from 10 to 29 km² and would include 268 lesser known species endemic to a single island, along with 11 bird and mammal species endemic to a single island. Our results suggest that for islands of equivalent size, prioritization based on total or threatened bird and mammal diversity may also capture opportunities to protect lesser known species endemic to islands. Beneficios de los Taxa Poco Estudiados para la Conservación de la Diversidad de Aves y Mamíferos en Islas     

Conspicuous displays in cryptic males of a polytypic poison-dart frog

The evolution of aposematism is linked to increased opportunities for conspicuous sexual displays since detection by potential predators is no longer disadvantageous. Therefore, phenotypic divergence in aposematic species leading to relatively cryptic forms is expected to constrain such opportunities, by restoring the trade-off between natural and sexual selection on the boldness of sexual displays. We asked if and how a derived phenotype of the poison-dart frog Oophaga granulifera that appears relatively cryptic to potential predators exhibits conspicuous sexual displays for potential mates. We used visual modeling of frog contrasts against their natural backgrounds to test if for conspecifics green frogs appear less conspicuous than red frogs as they do for birds. We conducted behavioral observations of focal red and green males to determine if green frogs adjust their display behavior to the availability of potential mates. Dorsal brightness is known to influence female preferences in at least one poison frog species. We found that, despite being less visible under some measures, green frogs may appear as bright as red frogs for conspecifics but not birds, when viewed on dark backgrounds. Additionally, green males called more intermittently than red males when advertising to distant females, but they exhibited a dramatic increase in calling activity in proximity of a female and were as active as red males in this context. Together, our results suggest that green frogs retain context-dependent conspicuousness to conspecifics despite the evolution of relative crypsis to potential predators.