Post-metamorphic Anurans Research Articles

Antipredator mechanisms of post-metamorphic anurans: a global database and classification system

A crucial step in any ethological study is to distinguish and classify the observed behavior into categories. The literature on anuran antipredator mechanisms is largely scattered and descriptive due to the opportunistic nature of the observations and the lack of a simple, widely accepted classification scheme. We propose an explanatory classification system of antipredator mechanisms for post-metamorphic anurans (i.e., juveniles and adults) based on a thorough review of the literature and observations made during fieldwork and in the laboratory since 1970. In addition, we provide a freely available global database on antipredator mechanisms of post-metamorphic anurans. The classification system is composed of 12 antipredator mechanisms and 28 variations distributed into three stages of defense (avoid detection, prevent attack, and counterattack). The database comprises 650 species and 39 families providing a unique opportunity to investigate ecological and evolutionary questions regarding antipredator mechanisms of anuran. We provide a general overview of geographic, taxonomic, and phylogenetic patterns found in the database. Both our studies and that of our colleagues added 70 species to the database. The number of publications on antipredator mechanisms increased substantially after the year 2000. We hope to spark a renewed interest in antipredator mechanisms of post-metamorphic anurans to understand further the evolution of predator–prey interactions. Predation is a phenomenon of great ecological and evolutionary significance. Hence, the study of antipredator mechanisms may provide some of the most fascinating answers to questions regarding species “struggle for existence.” Based on extensive fieldwork, laboratory observations, and a thorough literature survey, we propose a classification system of antipredator mechanisms for anurans and provide a database of antipredator mechanisms elicited by frogs. We describe each mechanism, discuss the variations, and provide images for most antipredator mechanisms.

Detritus Quality and Locality Determines Survival and Mass, but Not Export, of Wood Frogs at Metamorphosis.

Single-site experiments have demonstrated detritus quality in wetlands can have strongly negative, neutral, and even positive influences on wildlife. However, an examination of the influence of detritus quality across several regions is lacking and can provide information on whether impacts from variation in detritus quality are consistent across species with wide ranges. To address this gap in regional studies we examined effects of emergent and allochthonous detritus of different nutrient qualities on amphibians and assessed a mechanism that may contribute to potential impacts. We used aquatic mesocosms to raise wood frogs (Rana sylvatica) from two regions of the United States with whole plants from purple loosestrife (Lythrum salicaria), leaf litter from native hardwood trees, and a mixture of both. We examined several metrics of amphibian fitness and life history, including survival, number of days to metamorphosis, and size at metamorphosis. Further, we quantified whether the effects of detritus type could translate to variation in anuran biomass or standing stock of nitrogen or phosphorus export. Our results show detritus with high nutrient quality (purple loosestrife) negatively influenced survival of wood frogs, but increased size of metamorphic individuals in two different regions of the United States. Despite the decrease in survival, the increase in size of post-metamorphic anurans raised with high quality detritus resulted in anuran biomass and standing stock of N and P export being similar across treatments at both locations. These results further demonstrate the role of plant quality in shaping wetland ecosystem dynamics, and represent the first demonstration that effects are consistent within species across ecoregional boundaries.

A Case of Scavenging Behavior by the Japanese Rice Frog,Fejervarya kawamurai(Amphibia: Anura: Dicroglossidae)

Abstract: Most of metamorphosed terrestrial frogs feed only on moving organisms and rarely exhibit scavenging behavior in nature. We here report a case of scavenging by the Japanese Rice Frog, Fejervarya kawamurai, which fed on a dead Black-spotted Frog, Pelophylax nigromaculatus at the edge of paddy field in central Japan. This observation is the first case of Fejervarya, feeding on a dead animal in nature and is an important addition to the cases of this unique behavior, which has been reported only for limited number of anuran species so far. In contrast, the behavior is more often reported for frogs in captivity, and F. kawamurai may be a useful species for examining scavenging behavior in post metamorphic anurans.

Warmer temperatures reduce the costs of inducible defences in the marine toad, Rhinella marinus.

Many of the far-reaching impacts of climate change on ecosystem function will be due to alterations in species interactions. However, our understanding of the effects of temperature on the dynamics of interactions between species is largely inadequate. Inducible defences persist in prey populations because defensive traits increase survival in the presence of predators but are costly when they are absent. Large-scale changes in the thermal climate are likely to alter the costs or benefits of these defences for ectotherms, whose physiological processes are driven by environmental temperature. A shift in costs of defensive traits would affect not only predator-prey interactions, but also the strength of selection for inducible defences in natural populations. We investigate the effect of temperature on the costs of behavioural defences in larvae of the marine toad, Rhinella marinus. Larvae were reared in the presence or absence of predator cues at both 25 and 30 °C. When exposed to predation cues, larvae reduced activity and spent less time feeding. Exposure to predation cues also reduced metabolic rate, presumably as a by-product of reducing activity levels. Larvae exposed to predation cues also grew more slowly, were smaller at metamorphosis and were poorer jumpers after metamorphosis--three traits associated with fitness in post-metamorphic anurans. We found that the costs of behavioural defences, in terms of larval growth, post-metamorphic size and jumping performance, were exacerbated at cooler temperatures. The thermal sensitivity of costs associated with defensive traits may explain geographic variation in plasticity of defensive traits in other species and suggests that changes in environmental temperature associated with climate change may affect predator-prey interactions in subtle ways not previously considered.

Long‐term endemism of two highly divergent lineages of the amphibian‐killing fungus in the Atlantic Forest of Brazil

The recent global spread of the amphibian-killing fungus [Batrachochytrium dendrobatidis (Bd)] has been closely tied to anthropogenic activities; however, regional patterns of spread are not completely understood. Using historical samples, we can test whether Bd was a spreading or endemic pathogen in a region within a particular time frame, because those two disease states provide different predictions for the regional demographic dynamics and population genetics of Bd. Testing historical patterns of pathogen prevalence and population genetics under these predictions is key to understanding the evolution and origin of Bd. Focusing on the Atlantic Forest (AF) of Brazil, we used qPCR assays to determine the presence or absence of Bd on 2799 preserved postmetamorphic anurans collected between 1894 and 2010 and used semi-nested PCRs to determine the frequency of rRNA ITS1 haplotypes from 52 samples. Our earliest date of detection was 1894. A mean prevalence of 23.9% over time and spatiotemporal patterns of Bd clusters indicate that Bd has been enzootic in the Brazilian AF with no evidence of regional spread within the last 116years. ITS1 haplotypes confirm the long-term presence of two divergent strains of Bd (BdGPL and Bd-Brazil) and three spatiotemporally broad genetic demes within BdGPL, indicating that Bd was not introduced into southeast Brazil by the bullfrog trade. Our data show that the evolutionary history and pathogen dynamics of Bd in Brazil is better explained by the endemic pathogen hypothesis.

Interpopulation Variability in Evasive Behavior in the Oregon Spotted Frog (Rana pretiosa)

Few data exist that quantify evasive behavior in postmetamorphic anurans. On the basis of our casual observations that Oregon Spotted Frogs (Rana pretiosa) from one of two different populations appeared to exhibit a more pronounced evasive response, we used a pseudopredator stimulus to quantify the evasive response of juveniles from the two populations. We drew test animals from a pool of animals for each population that were captive-reared under identical conditions. Using latency to initial response, we compared the distribution of response times between the two populations at two sequential intervals over the rearing period. In both experiments, the Conboy Lake population had shorter latency-to-response times than the Black River population. However, we also found that latency-to-response times were shorter during the second test interval than during the first test interval for each population. The basis of population differences in response times may reside in differences in the predator set influencing each population, contaminants differentially influencing the Black River population in a negative manner, or some combination of both. Explanation for the faster latency-to-response times in the second experiment is unclear since both maturation and the length of the captive rearing interval may contribute to the effect, but they are confounded in this study.

Invasive bullfrogs as predators in a Neotropical assemblage: What frog species do they eat?

Anurans are important prey for the American bullfrogLithobates catesbeianus, but field assessments of its diet in the context of a local prey assemblage are lacking. We aimed to identify the frog species consumed by an invasive bullfrog population in subtropical South America, and to assess their relative importance among other types of prey. Characterization of the frog assemblage in the study area also allowed us to calculate the degree of electivity of the recorded anuran prey, in order to gain insight regarding bullfrog feeding preferences and to test if the bullfrog prey composition differed from a random sample of the assemblage. A total of 32.6% of the bullfrogs had at least one anuran in the stomach contents, and post-metamorphic anurans represented 49.1% of the relative prey importance for adult bullfrogs. Anurans were preyed on by all size classes, and constituted the volumetrically most important prey category in the diet of individuals heavier than 100 g. Cycloramphidae, Hylidae and Leiuperidae were positively selected, andHypsiboas pulchellusandPhysalaemus cuvieriwere the species most often taken. We found a low occurrence of cannibalism, despite the high density of bullfrogs at the study site. Our results showed that the degree of electivity differed among bullfrog prey types, suggesting that some frog species may be preyed on in a higher proportion than their relative abundance in the assemblage. Testing the clues provided by this assemblage-level approach may lead to a better assessment of the interactions between bullfrogs and the native frog fauna.

Seasonal pattern of chytridiomycosis in common river frog (Amietia angolensis ) tadpoles in the South African Grassland Biome

Environmental parameters such as temperature and rainfall influence the biology of amphibians and are likely to similarly influence the growth and prevalence of associated pathogens. Amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), causes an infectious disease, chytridiomycosis, in amphibians worldwide. Field studies on post-metamorphic anurans from tropical Australia have correlated increased prevalence with cool winter temperatures, but similar studies are lacking from Africa. We monitored the seasonality of amphibian chytrid in the Highveld of South Africa through microscopic examination of common river frog (Amietia angolensis ) tadpoles over 12 months.Within the study area Bd was found to be widespread, but largely limited to riverine systems. The seasonal infection pattern was inconsistent with the findings of past studies, which showed that prevalence usually peaks during the cooler months of the year. This study indicates that infection levels increased during spring in the Grassland Biome, when temperatures favoured optimum thermal growth of the fungus and when streams reached minimum flow levels.

Seasonal Pattern of Chytridiomycosis in Common River Frog (Amietia angolensis) Tadpoles in the South African Grassland Biome

Environmental parameters such as temperature and rainfall influence the biology of amphibians and are likely to similarly influence the growth and prevalence of associated pathogens. Amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), causes an infectious disease, chytridiomycosis, in amphibians worldwide. Field studies on post-metamorphic anurans from tropical Australia have correlated increased prevalence with cool winter temperatures, but similar studies are lacking from Africa. We monitored the seasonality of amphibian chytrid in the Highveld of South Africa through microscopic examination of common river frog (Amietia angolensis) tadpoles over 12 months. Within the study area Bd was found to be widespread, but largely limited to riverine systems. The seasonal infection pattern was inconsistent with the findings of past studies, which showed that prevalence usually peaks during the cooler months of the year. This study indicates that infection levels increased during spring in the Grassland Biome, when temperatures favoured optimum thermal growth of the fungus and when streams reached minimum flow levels.

An invasive species imposes selection on life-history traits of a native frog

As well as their direct ecological impacts on native taxa, invasive species can impose selection on phenotypic attributes (morphology, physiology, behaviour, etc.) of the native fauna. In anurans, body size at metamorphosis is a critical life-history trait: for most challenges faced by post-metamorphic anurans, larger size at metamorphosis probably enhances survival. However, our studies on Australian frogs (Limnodynastes convexiusculus) show that this pattern can be reversed by the arrival of an invasive species. When metamorph frogs first encounter invasive cane toads (Bufo marinus), they try to eat the toxic invader and, if they are able to do so, are likely to die from poisoning. Because frogs are gape-limited predators, small metamorphs cannot ingest a toad and thus survive long enough to disperse away from the natal pond (and thus from potentially deadly toads). These data show that larger size at metamorphosis can reduce rather than increase anuran survival rates, because larger metamorphs are more easily able to ingest (and thus be poisoned by) metamorph cane toads. Our results suggest that patterns of selection on life-history traits of native taxa (such as size and age at metamorphosis, seasonal timing of breeding and duration of pondside aggregation prior to dispersal) can be modified by the arrival of an invasive species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 329‐336.

Terbinafine Hydrochloride in Ethanol Effectively Clears Batrachochytrium dendrobatidis in Amphibians

ABSTRACT Amphibian chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), has been implicated in the decline and extinction of amphibian species worldwide, in addition to catastrophic losses of animals in captivity. Conservation of threatened amphibians, including captive breeding and maintenance of animals in zoos, research facilities, and private collections, requires effective control of pathogens. Several chemical compounds, including Formalite III®, itraconazole, and chloramphenicol, have been used to treat amphibians infected with Bd, with varying levels of success. Here, we report successful clearance of Bd in five species of post-metamorphic anurans and one caudate species using terbinafine hydrochloride (HCl) in alcohol, which is available over the counter as Lamisil AT™ (Novartis Pharmaceuticals Inc., New York, NY). Treatments consisting of 5 min soak in fresh 0.01% or 0.005% terbinafine HCl in alcohol for either five consecutive days or for six treatments spread across 10 d...

Colors and Some Morphological Traits as Defensive Mechanisms in Anurans

Anurans may be brightly colored or completely cryptic. Generally, in the former situation, we are dealing with aposematism, and the latter is an example of camouflage. However, these are only simple views of what such colorations really mean and which defensive strategy is implied. For instance, a brightly colored frog may be part of a mimicry ring, which could be either Batesian, Müllerian, or Browerian. These are only examples of the diversity of color-usage systems as defensive strategies. Unfortunately, reports on the use of colors as defensive mechanisms are widespread in the available literature, and the possible functions are rarely mentioned. Therefore, we reviewed the literature and added new data to this subject. Then, we the use of colors (as defensive mechanism) into categories. Mimicry was divided into the subcategories camouflage, homotypy, and nondeceitful homotypy, and these groups were also subcategorized. Dissuasive coloration was divided into behavioral display of colors, polymorphism, and polyphenism. Aposematism was treated apart, but aposematic colorations may be present in other defensive strategies. Finally, we propose functions and forms of evolution for some color systems in post-metamorphic anurans and hope that this review can be the basis for future research, even on other animal groups.

Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996-2001.

A total of 44 amphibian mortality events and 20 morbidity events were reviewed retrospectively. The most common cause of amphibian mortality events was infection by ranaviruses (Family: Iridoviridae). Ranavirus epizootics have abrupt onset and affect late-stage larvae and recent metamorphs. Mortality events due to ranavirus infections affected only widespread and abundant amphibian species, and there was a clear association with high population densities. Chytrid fungal infections accounted for seven mortality events in postmetamorphic anurans only. Chytrid epizootics are insidious and easily overlooked in the field. While both ranavirus and chytrid fungal epizootics were associated with > 90% mortality rates at affected sites, only the chytrid fungal infections were linked to multiple amphibian population declines. Three primitive fungal organisms in the newly erected clade, Mesomycetozoa, caused morbidities and mortalities in anurans and salamanders.

Are Archeobatrachian Anurans Ambidextrous? Assessing Handedness in Bombina orientalis

Lateralized behaviors (i.e., handedness), in the absence of conspicuous morphological asymmetry, have been noted in a variety of nonmammalian vertebrates, including certain fishes, frogs, and birds (reviewed in Bisazza et al., 1998; Vallortigara et al., 1999). Lateralized behaviors, such as turning preference during the initiation of a startle response, may facilitate quick reaction. When these behaviors first evolved, though, is unknown. Yamashita et al. (2000) suggested that lateralized behaviors might be common among anurans. However, their presence in any archeobatrachian anurans has not been assessed. One of the most basal archeobatrachian families is the Bombinatoridae (Cannatella, 1999). Here, we test tadpoles and postmetamorphic juveniles of the bombinatorid taxon Bombina orientalis for turning bias and forelimb use, respectively, to determine whether lateralized behaviors occur in this family. There is a fairly extensive literature on handedness in postmetamorphic anurans, at least for neobatrachian taxa. Dill (1977), for example, examined jumping direction in the Pacific tree frog, Hyla regilla, and found a significant left side preference in certain individuals. Bisazza et al. (1997) and Robins et al. (1998) examined handedness in toads of the genus Bufo using a series of protocols. Their first test required each toad to remove a plastic balloon from its head. In this test, Bufo bufo showed significantly greater use of the right forelimb than the left at the population level. Their second test consisted of placing a thin wet strip of paper on a toad's snout and noting which limb it used to clean the paper off. Again, B. bufo showed significant use of the right forelimb. The third test was an underwater righting test in which each toad was submerged in water in a supine position and allowed to right itself. In this test, Bufo marinus exhibited a right forelimb preference, causing it to roll to the left side. In addition, Robins et al. (1998) found lateralized hind limb use by B. marinus, Bufo viridis, and B. bufo when allowed to right themselves on a dry surface. Specifically B. marinus and B. bufo showed a significant preferential use of the right hind limb, and B. viridis showed significant use of the left hind limb. More recently, behavioral laterality was reported in the preferred turning direction of anuran larvae (Wassersug et al., 1999; Yamashita et al., 2000). When tadpoles are startled, or when they descend after surfacing to take a gulp of air, they can turn preferentially

Emesis and space motion sickness in amphibians

Amphibians possess the ability to vomit in response to a variety of stimuly that provoke emesis in mammals. Pharmacological studies have establish that the ejection of gastric contents and the basic mechanism for vomiting have been phylogenetically conserved among these tetrapods. As part of on-going comparative studies on emesis in vertebrates, we previously documented that some postmetamorphic anurans and salamander larvae experience motion-induced emesis when exposed to the provocative stimulus of parabolic aircraft flight. However, more recent experiments suggest that there are strict conditions for inducing emesis in amphibians exposed to parabolic flight and that amphibians are not as sensitive to this stimulus as mammals. Further studies on emesis in lower vertebrates may help us understand the processes that cause emesis in abnormal gravitational regimes.

Avoidance Response of Post-Metamorphic Anurans to Cues of Injured Conspecifics and Predators

Despite the widespread occurrence of chemically mediated antipredator responses among larval anurans, little is known concerning whether anurans utilize chemical cues after metamorphosis. Larval western toads (Bufo boreas) and red-legged frogs (Rana aurora) both exhibit antipredator responses when exposed to alarm cues of injured conspecifics. There is some debate as to whether larval Cascades frogs (Rana cascadae) show a similar response. In this study, we documented that toads and red-legged frogs respond to cues of injured conspecifics after metamorphosis, while Cascades frogs do not The avoidance