Shared behavioral responses and predation risk of anuran larvae and adults exposed to a novel predator

Invasive species are a regional and global threat to biological diversity. In order to evaluate an invasive predator species’ potential to harm populations of native prey species, it is critical to evaluate the behavioral responses of all life stages of the native prey species to the novel predator. The invasion of the African clawed frog (Xenopus laevis) into southern California provides an opportunity to evaluate the predation risk and behavioral responses of native amphibians. We performed predation trials and explored prey behavioral responses to determine how this invasive predator may impact native amphibian populations using Pacific chorus frogs (Pseudacris regilla) as a representative native California prey species. We found that X. laevis will readily prey upon larval and adult life stages of P. regilla. Behavior trials indicated that both larval and adult P. regilla exhibit prey response behaviors and will spatially avoid the novel invasive predator. The results suggest that native anurans may have a redundant predator response in both the larval and adult life stages, which could reduce the predatory impact of X. laevis but also drive emigration of native amphibians from invaded habitat.     

Functional response and area‐restricted search in a predator: seasonal exploitation of anurans by the European polecat,Mustela putorius

A study of the feeding habits and movements of 11 radiotracked polecats Mustela putorius in western France revealed that seasonal predation upon agile frogs, Rana dalmatina, was directly influenced by prey abundance and distribution. Although dietary structure showed the importance of mammalian prey (71.5%), polecats exploited nocturnal, terrestrial anurans in spring (31.6%). The periodic activity of anurans at spawning sites led both to a maximum density in spring and to a patchy distribution. The monthly variations in anuran dietary occurrences were associated with changes in frog availability. The functional response of polecats to frog density was sigmoidal shaped (type 3 response). Frog consumption rate increased more slowly than prey density but frogs were actively removed at higher density. It is therefore suggested that frog populations were moderately affected by the predator and this density dependent effect tends to stabilise anuran populations. Predation upon anurans was also correlated with a prey dispersion index as revealed by a polynomial regression. Polecats concentrated their predation on spawning congregations of the breeding adult frogs. Movements were smallest in spring and polecats changed their track length by increasing the difference between a succession of small movements and of longer journeys towards profitable sites. Changes in movements correlated with the anuran dispersion index and the response was sigmoidal (polynomial regression) revealing an area‐restricted search. This response may be regarded as an ‘aggregative response’ according to the first part of the definition of Begon et al. (1996) . Functional and area‐restricted search responses to the frog abundance and dispersion constitute an original example of predator‐prey coexistence strategies among vertebrates. I suggest that such predation could be favoured by the individualistic habits of the mustelid.     

The shape of things to come: linking developmental plasticity to post‐metamorphic morphology in anurans

Development consists of growth and differentiation, which can be partially decoupled and can be affected by environmental factors to different extents. In amphibians, variation in the larval environment influences development and causes changes in post‐metamorphic shape. We examined post‐metamorphic consequences, both morphological and locomotory, of alterations in growth and development. We reared tadpoles of two phylogenetically and ecologically distant frog species (the red‐eyed treefrog Agalychnis callidryas and the African clawed frog Xenopus laevis) under different temperatures with ad libitum food supply and under different food levels at a constant temperature. Low temperature and low food levels both resulted in similarly extended larval periods. However, low temperature yielded relatively long‐legged frogs with a lower degree of ossification than warm temperature, whereas low food yielded relatively short‐legged frogs with a higher degree of ossification than high food levels. Such allometric differences had no effect on locomotor performance of juveniles. Our results provide a basis for understanding the relationship between growth, differentiation and post‐metamorphic shape in anurans and help explain many of the discrepancies reported in previous studies.     

A review of ecological interactions between native frogs and invasive cane toads in Australia

Translocated from their native range in the Americas in 1935, cane toads (Rhinella marina, Bufonidae) have now spread through much of tropical and subtropical Australia. The toad's invasion and impact have attracted detailed study. In this paper, I review information on ecological interactions between cane toads and Australian anurans. The phylogenetic relatedness and ecological similarity between frogs and toads creates opportunities for diverse interactions, ranging from predation to competition to parasite transfer, plus a host of indirect effects mediated via impacts of toads on other species, and by people's attempts to control toads. The most clear‐cut effect of toads on frogs is a positive one: reducing predator pressure by fatally poisoning anuran‐eating varanid lizards. However, toads also have a wide range of other effects on frogs, some positive (e.g. taking up parasites that would otherwise infect native frogs) and others negative (e.g. eating frogs, poisoning frogs, competing with tadpoles). Although information on such mechanisms predicts intense interactions between toads and frogs, field surveys show that cane toad invasion has negligible overall impacts on frog abundance. That counter‐intuitive result is because of a broad balancing of negative and positive impacts, coupled with stochastic (weather‐induced) fluctuations in anuran abundance that overwhelm any impacts of toads. Also, the impacts of toads on frogs differ among frog species and life‐history stages, and depend upon local environmental conditions. The impacts of native frogs on cane toads have attracted much less study, but may well be important: frogs may impose biotic resistance to cane toad colonization, especially via competition in the larval phase. Overall, the interactions between native frogs and invasive toads illustrate the diverse ways in which an invader's arrival can perturb the native fauna by both direct and indirect mechanisms, and by which the native species can curtail an invader's success. These studies also offer a cautionary tale about the difficulty of predicting the impact of an invasive species, even with a clear understanding of mechanisms of direct interaction.     

Effects of an invasive anuran [the cane toad (Bufo marinus)] on the invertebrate fauna of a tropical Australian floodplain

The ways in which invasive organisms influence native ecosystems remain poorly understood. For example, feral cane toads Bufo marinus have spread extensively through tropical Australia over the last 70 years, but assessments of their ecological impact remain largely anecdotal. We conducted experimental trials to examine the effect of cane toad presence on invertebrate fauna in relatively small (2.4 × 1.2 m) outdoor enclosures on a floodplain near Darwin in the wet–dry tropics. Toads significantly reduced invertebrate abundance and species richness, but only to about the same degree as did an equivalent biomass of native anurans. Thus, if toads simply replaced native anurans, the offtake of invertebrates might not be substantially different from that due to native anurans before toad invasion. However, our field surveys suggest that toads cause a massive (fourfold) increase in total amphibian biomass. The end result is that cane toads act as a massive nutrient sink in the floodplain ecosystem because they consume vast numbers of invertebrates but (unlike native frogs) are largely invulnerable to predation by frog-eating predators.     

Native Australian frogs avoid the scent of invasive cane toads

Invasive species can affect the ecosystems they colonize by modifying the behaviour of native taxa; for example, avoidance of chemical cues from the invader may modify habitat use (shelter site selection) by native species. In laboratory trials, we show that metamorphs of most (but not all) native frog species on a tropical Australian floodplain avoid the scent of invasive cane toads (Bufo marinus Linnaeus 1758). Cane toads also avoid conspecific scent. This response might reduce vulnerability of metamorph frogs and toads to larger predatory toads. However, similar avoidance of one type of pungency control (garlic), and the presence of this avoidance behaviour in frogs at the toad invasion front (and hence, with no prior exposure to toads), suggest that this may not be an evolved toad‐specific response. Instead, our data support the simpler hypothesis that the metamorph anurans tend to avoid shelter sites that contain strong and unfamiliar scents. Temporal and spatial differences in activity of frogs versus toads, plus the abundance of suitable retreat sites during the wet season (the primary time of frog activity), suggest that avoiding toad scent will have only a minor impact on the behaviour of native frogs. However, this behavioural impact may be important when environmental conditions bring toads and frogs into closer contact.     

Adult frogs are sensitive to the predation risks of olfactory communication

Olfaction is a common sensory mode of communication in much of the Vertebrata, although its use by adult frogs remains poorly studied. Being part of an open signalling system, odour cues can be exploited by 'eavesdropping' predators that hunt by smell, making association with odour a high-risk behaviour for prey. Here, we show that adult great barred frogs (Mixophes fasciolatus) are highly attracted to odour cues of conspecifics and those of sympatric striped marsh frogs (Limnodynastes peronii). This attraction decreased significantly with the addition of odours of a scent-hunting predator, the red-bellied black snake (Pseudechis porphyriacus), indicating that frogs perceived predation risks from associating with frog odours. Male frogs, however, maintained some attraction to unfamiliar conspecific scents even with predator odours present, suggesting that they perceived benefits of odour communication despite the risk. Our results indicate that adult frogs can identify species and individuals from their odours and assess the associated predation risk, revealing a complexity in olfactory communication previously unknown in adult anurans.     

A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution

The African clawed frogs (Silurana and Xenopus), model organisms for scientific inquiry, are unusual in that allopolyploidization has occurred on multiple occasions, giving rise to tetraploid, octoploid, and dodecaploid species. To better understand their evolution, here we estimate a mitochondrial DNA phylogeny from all described and some undescribed species. We examine the timing and location of diversification, and test hypotheses concerning the frequency of polyploid speciation and taxonomy. Using a relaxed molecular clock, we estimate that extant clawed frog lineages originated well after the breakup of Gondwana, about 63.7 million years ago, with a 95% confidence interval from 50.4 to 81.3 million years ago. Silurana and two major lineages of Xenopus have overlapping distributions in sub-Saharan Africa, and dispersal-vicariance analysis suggests that clawed frogs originated in central and/or eastern equatorial Africa. Most or all extant species originated before the Pleistocene; recent rainforest refugia probably acted as "lifeboats" that preserved existing species, rather than "species pumps" where many new successful lineages originated. We estimate that polyploidization occurred at least six times in clawed frogs.     

Green Frogs Show Reduced Foraging Success in Habitats Invaded by Japanese knotweed

Habitat loss is causing amphibian population declines worldwide, so there is increased attention to forces that degrade remaining habitats. Terrestrial habitats surrounding wetlands are critical foraging areas for temperate anurans. We investigated plant community changes in two old fields invaded by Japanese knotweed (Fallopia japonica) and the foraging success of Green frogs (Rana clamitans) in invaded and non-invaded portions of those fields. Within each field, vegetation data were recorded in quadrats located along two transects bisecting the invasion fronts. We placed frogs in ‘foraging buckets’ along transects and measured their change in mass over a 38 h period. There were significant changes in vegetation structure and composition associated with Japanese knotweed invasion. Diverse assemblages of native plants that covered non-invaded plots were absent from areas invaded by Japanese knotweed. There was also a significant change in vegetation architecture between invaded and non-invaded habitats. Change in frog mass declined significantly along transects, with most frogs in non-invaded plots gaining mass and no frogs in invaded plots gaining mass. Most frogs from non-invaded plots but only two from invaded plots defecated shortly after removal from foraging buckets (verification of recent feeding). We hypothesize that Japanese knotweed invasions degrade terrestrial habitat quality for frogs by indirectly reducing arthropod abundance. Nonnative plant invasions may be another factor contributing to amphibian population declines.     

Quantifying Anuran Microhabitat Use to Infer the Potential for Parasite Transmission between Invasive Cane Toads and Two Species of Australian Native Frogs

Parasites that are carried by invasive species can infect native taxa, with devastating consequences. In Australia, invading cane toads (Rhinella marina) carry lungworm parasites (Rhabdias pseudosphaerocephala) that (based on previous laboratory studies) can infect native treefrogs (Litoria caerulea and L. splendida). To assess the potential of parasite transmission from the invader to the native species (and from one infected native frog to another), we used surveys and radiotelemetry to quantify anuran microhabitat use, and proximity to other anurans, in two sites in tropical Australia. Unsurprisingly, treefrogs spent much of their time off the ground (especially by day, and in undisturbed forests) but terrestrial activity was common at night (especially in anthropogenically modified habitats). Microhabitat overlap between cane toads and frogs was generally low, except at night in disturbed areas, whereas overlap between the two frog species was high. The situations of highest overlap, and hence with the greatest danger of parasite transmission, involve aggregations of frogs within crevices by day, and use of open ground by all three anuran species at night. Overall, microhabitat divergence between toads and frogs should reduce, but not eliminate, the transmission of lungworms from invasive toads to vulnerable native frogs.     

Foraging responses of predators to novel toxic prey: effects of predator learning and relative prey abundance

Learning to avoid toxic prey items may aid native predators to survive the invasion of highly toxic species, such as cane toads Bufo marinus in tropical Australia. If the predators’ initial aversion is generalized, native prey that resemble the toxic invader may receive a benefit through accidental mimicry. What ecological factors influence the acquisition of learned avoidance (and hence, the impact of invasion on both predators and native prey)? We conducted laboratory experiments to evaluate how the relative abundance of toad tadpoles compared to palatable native tadpoles (Litoria caerulea and L. rubella) affected the ability of native aquatic predators to discriminate between these two prey types. Both fish (northern trout gudgeon, Mogurnda mogurnda) and frogs (Dahl's aquatic frog, Litoria dahlii) learned to discriminate between toads and frogs within an eight‐day period. Higher abundance of toad tadpoles relative to frog tadpoles enhanced rates of predator learning, and thus reduced predation on toads and increased predation on native tadpoles. In the field, spatial and temporal variation in the relative abundance of cane toads compared to native frogs may influence the rates at which these novel toxic items are deleted from predator diets, and the duration of predator protection afforded to natives that resemble the invader.     

Presence of Batrachochytrium dendrobatidis in feral populations of Xenopus laevis in Chile

Batrachochytrium dendrobatidis (Bd) is a causal agent of disease and population decline of amphibian populations, and the extinction of several anuran species worldwide. Diverse hypotheses have been provided for the emergence of this fungus in different continents, ranging from global climate change to the vectoring of Bd via the international trade in amphibian species. In order to address these hypotheses, it is important to assess the current distribution of Bd in the context of introduced non-native amphibian species. We sampled several populations of the African clawed frog Xenopus laevis across its distribution in Chile in order to detect the presence of B. dendrobatidis and evaluate the role of this frog as a potential vector. In three of ten sites sampled, individuals harbored B. dendrobatidis infection, with an overall prevalence of infection across the studied populations of 24% (14 positive out of 58 analyzed specimens). The rapid spread exhibited by this frog within Chile suggests that transpecific transmission of the pathogen is possible, perhaps jeopardizing native species. This finding indicates the urgent need to establish long-term monitoring population programs in order to allow early detection disease-driven changes in the sizes of native populations, allowing the prompt application of conservation practices.     

Cannibalism or congeneric predation? The African clawed frog,Xenopus laevis (Daudin), preferentially predates on larvae of Cape platannas,Xenopus gilli Rose & Hewitt

Predators are not limited to prey from other species as they can cannibalise vulnerable individuals within their own population. The African clawed frog, Xenopus laevis (Daudin), is a predator with a broad diet, known to consume multiple prey species, including congeners and conspecifics. African clawed frogs occur in sympatry with the Endangered Cape platanna, Xenopus gilli Rose & Hewitt, which are under threat through competition and predation from X. laevis. We investigated the threat of X. laevis predation on X. gilli using choice and no‐choice experiments to evaluate the relative vulnerability of X. laevis and X. gilli larvae. Results showed that large X. gilli larvae had a significantly higher vulnerability to X. laevis predation compared to small X. gilli larvae. However, the same discrimination was not discerned when offered large and small X. laevis larvae, or mixed larvae of the same size. We report ontogenic shifts in behaviour of X. gilli larvae that may be a factor in contributing to the vulnerability of large X. gilli larvae to adult X. leavis predation. Congeneric predation likely has negative implications for the population structure of the Endangered X. gilli. Our study underlines the call for the removal of X. laevis to conserve populations of X. gilli.     

A striking lack of genetic diversity across the wide-ranging amphibian <Emphasis Type="Italic">Gastrophryne carolinensis</Emphasis> (Anura: Microhylidae)

We examine phylogeographic structure across a wide-ranging microhylid frog (Gastrophryne carolinensis) using both mitochondrial (mtDNA) and nuclear (AFLP) data. Species with similar ecological characteristics such as large range size, low vagility, or existence across known biogeographic barriers, often are comprised of multiple, cryptic lineages. Surprisingly, our analyses of both portions of the genome show very little phylogeographic or population genetic structure. The family Microhylidae is one of the largest families of anurans with over 60 genera and around 400 species distributed across much of the world (Americas, Asia, Africa, and Madagascar), but very few phylogeographic studies have assessed intraspecific genetic diversity across the mitochondrial and nuclear genomes. Our results suggest that G. carolinensis, one of only three species of microhylid native to the US, has experienced a severe population bottleneck with subsequent range expansion. Comparable molecular data from closely related microhylids, in addition to demographic and ecological analyses, will provide valuable insight into patterns of genetic diversity and the processes driving phylogeographic diversity in these wide-ranging frogs.     

Induction of ovulation in <Emphasis Type="Italic">Xenopus</Emphasis>without hCG injection: the effect of adding steroids into the aquatic environment

Background  

The African clawed frog, Xenopus laevis, is widely used in studies of oogenesis, meiotic cell cycle and early embryonic development. However, in order to perform such studies, eggs are normally collected after the injection of hCG into the dorsal lymph sac of fully-grown female frogs following pre-injection of PMSF. Although this protocol is established and used as standard laboratory approach, there are some concerns over whether the injections could cause the transmission of deleterious microorganisms. Moreover, these injection protocols require a competent skilled worker to carry out the procedure efficiently.     

Low genetic diversity of the successful invasive African clawed frog Xenopus laevis (Pipidae) in Chile

In Africa, the genus Xenopus presents cryptic species and diverse hybrids between species. It has been assumed that the invasive populations of this genus correspond to X. laevis and that they are derived from the subspecies that inhabits the Mediterranean Cape region of South Africa. In part, this is supported by the successful establishment of this species in several Mediterranean regions of the world. In Mediterranean Chile, Xenopus has invaded an area of about 21,000 km², with scarce attention to genetic aspects underlying its invasion. Using mitochondrial DNA sequences we determined that Xenopus laevis laevis from the Cape region of South Africa is the subspecies that invaded Chile. The analysis indicated that the invaders have low genetic diversity (only two haplotypes, compared to 10 in two localities of their native range), and that probably the invasion in Chile occurred only once. Landscape genetics revealed that factors such as aridity and elevation have determined the spread of the species, both from the ecological and genetic points of view. Our results show that the invasion of the African clawed frog in Chile has been successful for at least 30 years, in spite of low genetic variability, few events of introduction, low propagule pressure, and bottlenecks in the founding population.     

Batrachochytrium dendrobatidis in the live frog trade of Telmatobius (Anura: Ceratophryidae) in the tropical Andes

Species of frogs in the genus Telmatobius are traded and sold for human consumption in the Andes and in coastal cities of Peru and Bolivia. These frogs are harvested from wild populations. We report high prevalence of infection by the pathogenic fungus Batrachochytrium dendrobatidis in live frogs purchased at the main market in Cusco, Peru, from January 2008 to January 2010. We suggest that the transport of native anurans through the live frog trade could facilitate the spread of this fungus among Andean frogs. The tropical Andes are the most important biodiversity hotspot for amphibians. Because many neotropical taxa are known to be susceptible to chytridiomycosis, the presence of a large reservoir of infection in the frog trade poses a significant threat to amphibian conservation.     

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.     

<Emphasis Type="Italic">Xenopus laevis</Emphasis> (Daudin, 1802), a new exotic amphibian in Portugal

The African clawed frog Xenopus laevis has been introduced at several locations, including Mediterranean climate-type regions. In 2006, several individuals of this species were found inhabiting a stream at Oeiras, about 20 km W of Lisbon, Portugal. Although the place and time of introduction are not clearly identified, there are reasons to believe that this population may be the result of an almost 30-year-old introduction proceeding from research laboratories located nearby. Field surveys were conducted in 2007 and 2008 on the distribution and abundance of this species in the region. The species was found in two streams, about 5 km from each other. While being locally abundant, the adults of X. laevis are smaller than those from South Africa and California. In spite of an abundant production of eggs and tadpoles at one of the streams, no tadpoles were found in advanced developmental stages. Until now, most individuals were found in heavily urbanized areas that should constrain their ability to cross overland to other water bodies. An eradication program may be feasible, but the presence of adults on two streams indicates that the species may be expanding, in spite of the urban landscape.     

Predicting Predatory Outcomes in the Context of Carryover Effects: Interactions between Juvenile Frogs and Spider Predators

As representatives of organisms with complex life histories, frogs provide an ideal system to study predator‐induced carryover effects: how the risk of predation in one life stage can impact predator–prey interactions in a later stage. Invertebrate predation on frogs has been widely reported, although studies of the behavioral mechanisms underlying their interactions in the terrestrial stage have been lacking. We made detailed observations of interactions between a wolf spider (Tigrosa helluo) and Blanchard's cricket frog (Acris blanchardi) to determine factors that predict capture success and to evaluate potential carryover effects from aquatic predation risk. Juvenile frogs, reared with or without dragonfly predator cues, were placed in an arena with or without spider cues and allowed to interact with a spider. Spiders captured frogs, and an interaction between frog size and activity predicted frog survival. We found no evidence that either aquatic or terrestrial cues altered frog behavior or survival. By preying upon a demographically important life stage, spiders may contribute to population dynamics in frogs.