Foraging Responses of the Larvae of Invasive Bullfrogs(Lithobates catesbeianus): Possible Implications for Bullfrog Control and Ecological Impact in China

The predatory behavior of invasive species can affect their ecological impact, and offer opportunities for targeted control. In Australia, tadpoles of invasive cane toads(Rhinella marina) do not consume eggs of native anurans, but are strongly attracted to(and consume) newly-laid eggs of conspecifics; chemical cues from such eggs(or adult secretions) thus can be used to attract toad tadpoles to traps. Do other invasive anurans show similar selectivity? Our laboratory trials on a Chinese population of invasive American bullfrogs(Lithobates catesbeianus) revealed similar behaviors as exhibited by Australian cane toads. Bullfrog tadpoles rarely consumed the eggs of native anurans, but were attracted to both bullfrog eggs and bullfrog skin secretions. Although the attraction response was less intense in bullfrogs than in cane toads, it might nonetheless enable selective removal of bullfrog tadpoles from invaded sites.     

Choosy cannibals: Targeted consumption of conspecific hatchlings by larval cane toads is triggered by species‐specific defensive toxins

In many species, cannibalism is uncommon and involves nonselective consumption of conspecifics as well as heterospecifics. However, within their invasive Australian range, cane toad larvae (Rhinella marina) specifically target and voraciously consume the eggs and hatchlings of conspecifics, often extirpating entire clutches. In contrast, toad larvae rarely consume the eggs and hatchlings of native frogs. Here, we use laboratory studies to demonstrate that this selective consumption is triggered by species‐specific chemical cues: maternally‐invested bufadienolide toxins that otherwise defend cane toad eggs and hatchlings against predators. We find that these cues stimulate feeding behaviors in toad tadpoles, such that the addition of bufadienolide toxins to the water column increases predation on eggs, not only of conspecifics, but also of native anuran species that are otherwise usually ignored. In contrast, we find that cannibalism rates on conspecific hatchlings are high and unaffected by the addition of bufadienolide cues. The maternally‐invested toxins present in conspecific eggs may therefore be more easily detected post‐hatching, at which point tadpole feeding behaviors are induced whether or not additional toxin cues are present. As bufadienolide cues have previously been found to attract toad tadpoles to vulnerable hatchlings, our present findings demonstrate that the same toxin cues that attract cannibalistic tadpoles also induce them to feed, thereby facilitating cannibalism through multiple behavioral effects. Because native fauna do not produce bufadienolide toxins, the species specificity of these chemical cues in the Australian landscape may have facilitated the evolution of targeted (species‐specific) cannibalism in invasive cane toad populations. Thus, these bufadienolide toxins confer cost (increased vulnerability to cannibalism in early life‐stages) as well as benefit (reduced vulnerability to predation by other taxa).     

Vulnerability of an Australian anuran tadpole assemblage to the toxic eggs of the invasive cane toad (Bufo marinus)

The invasion of cane toads (Bufo marinus) across tropical Australia has fatally poisoned many native predators; the most frequent victims may be tadpoles of native frogs, which die when they consume the toxic eggs of the toads. Field studies have documented high and species‐specific mortality of tadpoles following toad spawning. To clarify the determinants of tadpole vulnerability, we conducted 1593 laboratory trials in which single tadpoles were exposed to 10 toad eggs, either with or without an alternative food source (lettuce). At least some tadpoles within all 15 species tested consumed toad eggs. Interspecific variance in survival rates (from 0 to >70%) was driven by feeding responses not by physiological tolerance to toxins: almost all native tadpoles that consumed eggs died rapidly. Tadpole mortality was decreased by the presence of an alternative food source in four species, increased in two species, and not affected in seven species. In three of four taxa where we tested both small (early‐stage) and large (late‐stage) tadpoles, both mean survival rates and the effects of alternative food on survival shifted with tadpole body size. Trials with one species (Limnodynastes convexiusculus) showed no significant inter‐clutch variation in feeding responses or tolerance to toxins. Overall, our data show that cane toad eggs are highly toxic to native anuran tadpoles, but that whether or not a tadpole is killed by encountering toad eggs depends upon a complex interaction between the native anuran's species, its body size, and whether or not alternative food was present. In nature, larval vulnerability also depends upon the seasonal timing and location of spawning events, and habitat selection and foraging patterns of the tadpoles. Our results highlight the complexity of vulnerability determinants, and identify ecological factors (rather than physiology or feeding behaviour) as the primary determinants of cane toad impact on native tadpoles.     

Exploiting intraspecific competitive mechanisms to control invasive cane toads (Rhinella marina)

If invasive species use chemical weapons to suppress the viability of conspecifics, we may be able to exploit those species-specific chemical cues for selective control of the invader. Cane toads (Rhinella marina) are spreading through tropical Australia, with negative effects on native species. The tadpoles of cane toads eliminate intraspecific competitors by locating and consuming newly laid eggs. Our laboratory trials show that tadpoles find those eggs by searching for the powerful bufadienolide toxins (especially, bufogenins) that toads use to deter predators. Using those toxins as bait, funnel-traps placed in natural waterbodies achieved near-complete eradication of cane toad tadpoles with minimal collateral damage (because most native (non-target) species are repelled by the toads' toxins). More generally, communication systems that have evolved for intraspecific conflict provide novel opportunities for invasive-species control.     

Field trials of chemical suppression of embryonic cane toads (Rhinella marina) by older conspecifics

1. Laboratory experiments have shown that the viability of embryos of the invasive cane toad (Rhinella marina) can be reduced by exposure to chemical cues from older conspecific larvae. These effects (very strong in laboratory trials) may offer an exciting new approach to controlling this problematic invasive species in Australia. However, the degree to which the method works in natural environments has yet to be assessed.
2. Our experiments in the laboratory and in seminatural outdoor waterbodies show that chemical cues from tadpoles do indeed suppress the growth, development, and survival of conspecific larvae that are exposed as embryos and do so in a dose‐dependent manner; higher tadpole densities cause greater suppression of embryos.
3. In seminatural outdoor waterbodies, suppressor‐exposed tadpoles were less than half as likely to survive to metamorphosis as were controls, and were much smaller when they did so and hence, less likely to survive the metamorph stage. Additionally, female cane toads were less likely to oviposit in a waterbody containing free‐ranging (but not cage‐enclosed) tadpoles, suggesting that the presence of tadpoles (rather than the chemical cues they produce) may discourage oviposition.
4. Broadly, our results suggest that the suppression effect documented in laboratory studies does indeed occur in the field also, and hence that we may be able to translate that approach to develop new and more effective ways to reduce rates of recruitment of peri‐urban populations of cane toads in their invasive range.

     

Understanding the toad code: Behavioural responses of cane toad (Chaunus marinus) larvae and metamorphs to chemical cues

Abstract Larvae of many anuran taxa display strong behavioural responses to chemical cues, including alarm signals from injured conspecific tadpoles. We exposed tadpoles and metamorphs from an Australian population of the invasive cane toad (Chaunus[Bufo] marinus) to a range of chemical stimuli and quantified their responses both in the laboratory and in the field. Filtered fluids containing scent cues from crushed conspecifics elicited strong avoidance from tadpoles, whereas other cues (e.g. scent of food, of native‐range fish or urodele predators, and thermal stimuli) did not. Apparent aggregation of tadpoles in response to scent cues proved to be an artifact of tank design, and was an indirect consequence of avoidance of those cues. Field trials confirmed that free‐ranging toad tadpoles and metamorphs avoided chemical cues from crushed conspecifics, suggesting that the chemicals inducing this response might provide an opportunity to develop targeted control methods for this invasive species.     

The reaction of tadpoles of the common toad (Bufo bufo L.) to chemical signals from individuals of their own and other species

In behavioral experiments, toad tadpoles-recipients chose between two parts of test aquarium with chemical signals of donor tadpoles of the same or different (Rana esculenta) species. The youngest studied tadpoles (43-45 stages) preferred the part of the aquarium with chemical cues from sibs as compared to non-sibs. No reliable difference in "non-sibs: water" system was observed. In "tadpoles of the same species: tadpoles of the other species" system, recipient tadpoles chose "their" part of the aquarium. Hence, toad tadpoles revealed a trend to aggregate with their sibs and avoid R. esculenta toads in the presence of certain chemical cues and in the absence of visual signals.     

The role of biotic and abiotic cues in stimulating aggregation by larval cane toads (Rhinella marina)

Tadpoles of the cane toad (Rhinella marina) form dense aggregations in the field, but the proximate cues eliciting this behavior are not well understood. We sampled water‐bodies in the Northern Territory of Australia, finding that the density of cane toad tadpoles increased with increasing temperature. Furthermore, we conducted laboratory experiments to explore the roles of biotic factors (attraction to conspecifics; chemical cues from an injured conspecific; food) and spatially heterogeneous abiotic factors (light levels, water depth, physical structure) to identify the cues that induce tadpole aggregation. Annulus and binary choice trials demonstrated weak but significant attraction between conspecifics. Tadpoles decreased swimming speeds, but did not increase grouping in response to cues from an injured conspecific. Larvae aggregated in response to abiotic cues (high levels of illumination and proximity to physical structures) and were strongly attracted to feeding conspecifics. Overall, aggregation by cane toad tadpoles is likely driven by weak social attraction coupled with a shared preference for specific abiotic features, creating loose aggregations that are then reinforced by movement toward feeding conspecifics.     

Mechanisms of competition between tadpoles of Australian frogs (Litoria spp.) and invasive cane toads (Rhinella marina)

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Metamorphic synchrony and aggregation as antipredator responses in American toads

Safety in numbers serves as an antipredator defense strategy in many organisms, as aggregation can reduce the probability of predation for individual group members. It has long been suggested that some organisms are under selective pressure to synchronize vulnerable life stages with conspecifics, but there have been very few experimental tests of this hypothesis. Furthermore, the role of aggregation of conspecific animals within cohorts during vulnerable life stages is poorly understood.
Previous studies indicate that predation pressure may select for synchronous metamorphosis and the subsequent formation of metamorphic aggregations in North American toad species. In a series of laboratory experiments, I demonstrated that 1) Bufo americanus tadpoles in the presence of a predator exhibit higher levels of aggregation than tadpoles maintained in the absence of predator stimuli, and 2) B. americanus exposed to predator chemical cues metamorphose more synchronously than control tadpoles. I also found that toads at the climax of metamorphosis exhibit higher levels of aggregation than pre-metamorphic individuals. These results support the hypothesis that predation pressure has played a role in selection for life stage synchrony, and that aggregation serves as an antipredator defense in animals with synchronous transitions.     

The Ability of Three Species of Tadpoles to Differentiate among Potential Fish Predators

The ability of prey to respond to novel predator cues may depend on the generality or specificity of the response to predator cues. We used laboratory behavioral experiments to examine the ability of tadpoles of three species of anurans (American toad, Bufo americanus ; bullfrog, Rana catesbeiana ; and green frog, R. clamitans ) to respond to the presence of two native potential predators (bluegill, Lepomis macrochirus ; and largemouth bass, Micropterus salmoides ) and one non-native potential predator (goldfish, Carassius auratus ). We also examined the effect of tadpole size on the behavioral responses of American toads and green frogs to predator cues. All three species of tadpoles responded to the presence of predator cues, although the specific responses varied among species. American toads and green frogs reduced activity in the presence of at least some fish cues, but bullfrog tadpoles did not change their activity. Bullfrogs decreased use of vegetation in the presence of some predator cues, whereas American toads and green frogs did not. American toads only responded to the presence of bluegill cues but not the other fish predator cues, whereas bullfrogs and green frogs responded more generally to the fish predators. In both American toads and green frogs, tadpole size affected behavior. For American toads, activity increased, as did the use of the vegetated side of the aquarium, in larger tadpoles. Not only did size affect American toad behavior, but it also influenced the responses of the tadpoles to predator cues. For green frogs, activity decreased in larger tadpoles. Our results suggest that behavioral responses of tadpoles to predator cues can be influenced by both the identity of the predator and the prey, as well as the size of the potential prey.     

Impacts of eggs and tadpoles of the invasive cane toad (Bufo marinus) on aquatic predators in tropical Australia

Invasive species affect native ecosystems in a variety of ways, and the magnitude of impact may depend upon many factors. In an invading species such as the cane toad (Bufo marinus), the multiphasic life history creates a potential for impact to differ between life history stages. Previous research on the impact of cane toads in Australia has focused on fatal poisoning of predators that ingest terrestrial stages of the toad, but aquatic stages (eggs, larvae) are toxic also. We exposed nine native Australian fish species and one native Australian turtle species to the eggs and larvae of toads. Strong species differences were evident, both in palatability (propensity to attack the egg or larva), and in subsequent responses (e.g. taste and reject the item, vs. ingest it). Toad eggs were less likely than toad tadpoles to be attacked, but also less likely to be rejected before ingestion (probably because the non‐toxic jelly coat masks the presence of toxins in the ovum). As a result, predators were far more likely to be killed by ingesting toad eggs than toad tadpoles. Fortuitously, the spatial and temporal availability of toad egg masses restricts encounter rates with predators, so that overall ecological impact may be low despite the high vulnerability of a fish or turtle that encounters such an egg mass. Understanding such ontogenetic shifts in the nature of interactions and magnitude of impact is crucial if we are to understand the overall ecological impact of invasive species.     

Interacting biocontrol programmes: invasive cane toads reduce rates of breakdown of cowpats by dung beetles

Ecological interactions among invasive species can affect not only the success of the invaders, but also their impact on ecosystems in the invaded range. In Australia, both dung beetles (subfamily Scarabaeinae) and cane toads (Rhinella marina) were introduced for biocontrol: the beetles to break down bovine faeces piles (cowpats) that otherwise accumulate and reduce pasture productivity, and the cane toad to consume scarab beetles that eat sugarcane and thus reduce sugar production. The dung beetles have been a success, whereas the toads have been a failure. Our experimental studies show that as well as impacting native fauna directly, cane toads reduce the rate of cowpat breakdown by consuming dung beetles. In the laboratory, dehydrated toads actively sought out cowpats based on scent cues, and in field enclosures, the presence of a cane toad significantly reduced rates of cowpat decomposition. Although toads have benefited from agricultural activities, their spread across Australia likely has reduced the effectiveness of one of the most successful biocontrol programmes ever conducted in that continent.     

Life history consequences of feeding versus non-feeding in a facultatively non-feeding toad larva

Summary Bufo periglenes, a toad endemic to montane Costa Rica, produces an unusually small clutch of large, yolk-rich eggs. The toads breed in small ephemeral pools that are unpredictable in duration and may be low in food availability. Two congeners, Bufo coniferus and Bufo marinus, occur nearby, breed in more permanent bodies of water that offer more food, and exhibit the typical toad pattern of large clutches of small eggs. Tadpoles of all three species feed on detritus and suspended organic material. By raising tadpoles of the three species individually with and without food I investigated the relationship between egg size (yolk provision) and tadpole survival. All of the unfed B. coniferus and B. marinus tadpoles grew little and died soon after developing to the hindlimb bud stage. On the other hand, all of the unfed B. periglenes tadpoles metamorphosed successfully, demonstrating that the tadpoles are facultatively non-feeding; developmental time from hatching to metamorphosis was significantly shorter for unfed tadpoles than for fed tadpoles, but fed individuals were significantly larger at transformation. Faster developmental rate and larger body size at transformation are both advantageous for frogs and toads, but cannot be attained simultaneously. Large egg size may afford flexibility in unpredictable environments. In pools where food is available, tadpoles presumably eat, take longer to metamorphose, but are larger at transformation than tadpoles developing in nutrient-poor sites. Small body size at transformation (a consequence of not eating) has potential costs, but the large quantity of yolk provided by a large egg enhances the probability of metamorphosis in food-limited environments.     

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.     

Sink or swim: a test of tadpole behavioral responses to predator cues and potential alarm pheromones from skin secretions

Chemical signaling is a vital mode of communication for most organisms, including larval amphibians. However, few studies have determined the identity or source of chemical compounds signaling amphibian defensive behaviors, in particular, whether alarm pheromones can be actively secreted from tadpoles signaling danger to conspecifics. Here we exposed tadpoles of the common toad Bufo bufo and common frog Rana temporaria to known cues signaling predation risk and to potential alarm pheromones. In both species, an immediate reduction in swimming activity extending over an hour was caused by chemical cues from the predator Aeshna cyanea (dragonfly larvae) that had been feeding on conspecific tadpoles. However, B. bufo tadpoles did not detectably alter their behavior upon exposure to potential alarm pheromones, neither to their own skin secretions, nor to the abundant predator-defense peptide bradykinin. Thus, chemicals signaling active predation had a stronger effect than general alarm secretions of other common toad tadpoles. This species may invest in a defensive strategy alternative to communication by alarm pheromones, given that Bufonidae are toxic to some predators and not known to produce defensive skin peptides. Comparative behavioral physiology of amphibian alarm responses may elucidate functional trade-offs in pheromone production and the evolution of chemical communication.     

The power of the seasons: rainfall triggers parental care in poison frogs

The quality of breeding sites is of great importance for the reproductive success and accordingly the fitness of many animal species. Hence, individuals should decide carefully where to rear their offspring. Often parents have to account for multiple characteristics of habitat quality at once, which in turn might change over time. Specimens confronted with such variability may evolve the ability to display context-dependant decision plasticity. Anuran amphibians breeding in ephemeral pools largely face two risks for their offspring: desiccation and predation. The Neotropical poison frog Ranitomeya variabilis deposits both eggs and tadpoles in phytotelmata. These small tadpole nurseries lower the risk of offspring predation. However, because most poison frog tadpoles are cannibalistic, even these pools need to be surveyed for predators, and parents tend to avoid deposition with conspecifics. We tested if this avoidance behaviour does change in parental R. variabilis depending on seasonal circumstances. Over several months we provided the frogs the option to deposit their eggs or tadpoles in pools that did and did not contain chemical cues of cannibalistic conspecifics, respectively. During the rainy season, frogs strongly avoided conspecific cues for both eggs and tadpoles. Anyway, with the change to the dry season, parental preferences changed such that parent frogs were more likely to deposit tadpoles (but not eggs) in pools containing cues of conspecific tadpoles. We suggest that R. variabilis, a species that typically isolates its cannibalistic offspring, has evolved a plastic feeding behaviour with regard to the risk of phytotelmata desiccation. We interpret that parents provide older tadpoles with younger ‘trophic’ tadpoles in order to accelerate their development and save them from impending desiccation.     

Far from home: responses of an American predator species to an American prey species in a jointly invaded area of Australia

Far from their native ranges in the Americas, two invasive species come into contact in Australian waterbodies. Cane toads (Rhinella marina) fatally poison many anurophagous predators, whereas eastern mosquito fish (Gambusia holbrooki) voraciously consume anuran larvae. As cane toads spread south along Australia’s east coast, they are colonizing areas where mosquito fish are abundant. What happens when these two American invaders encounter each other in Australia? We tested the responses to toad tadpoles of mosquito fish from populations that were sympatric versus allopatric with cane toads. Toad-sympatric fish generally ignored toad tadpoles. Toad-allopatric fish initially consumed a few tadpoles, but rapidly developed an aversion to these toxic prey items. The laboratory-reared progeny of toad-allopatric fishes were more likely to approach toad tadpoles than were the offspring of toad-sympatric fishes, but the two groups learned toad-avoidance at similar rates. Thus, mosquito fish show an innate aversion to cane toad tadpoles (perhaps reflecting coevolution with North American bufonid taxa), as well as an ability to rapidly learn taste-aversion. Our comparisons among populations suggest that several decades of toad-free existence in Australia caused a decline in the fishes’ innate (heritable) aversion to toads, but did not affect the fishes’ capacity to learn toad-avoidance after an initial exposure. Any impact of mosquito fish on cane toads thus is likely to be transitory. The rapid (<100-year) time frame of these shifts (the initial weakening of the fishes’ response during toad-allopatry, and its recovery after secondary contact) emphasizes the dynamic nature of faunal responses during biological invasions, and the interplay between adaptation and phenotypic plasticity.     

Competing tadpoles: Australian native frogs affect invasive cane toads (Rhinella marina) in natural waterbodies

The cane toad (Rhinella marina) is one of the most successful invasive species worldwide, and has caused significant negative impacts on Australian fauna. Experimental work in the laboratory and in mesocosms has shown that tadpoles of native frogs can affect survival, size at metamorphosis and duration of larval period of cane toad tadpoles. To test if these effects occur in nature, we conducted a field experiment using two temporary ponds where we set up enclosures with tadpoles of native green tree frogs (Litoria caerulea) and cane toads in treatments with a range of densities and combinations. The presence of green tree frog tadpoles significantly decreased the growth rate of toad tadpoles and increased the duration of their larval period in both ponds; in one pond, frog tadpoles also significantly reduced the body length and mass of metamorph toads. Toad tadpoles did not have any significant negative effects on green tree frog tadpoles, but there was strong intraspecific competition within the latter species: increased frog tadpole density resulted in increased larval period and reduced survival, growth rate and size at metamorphosis for frogs at one or both ponds. Our results are encouraging for the possibility of using native frogs as one component of an integrated approach to the biological control of cane toads.     

Chemical defense of toad tadpoles under risk by four predator species

Many organisms use inducible defenses as protection against predators. In animals, inducible defenses may manifest as changes in behavior, morphology, physiology, or life history, and prey species can adjust their defensive responses based on the dangerousness of predators. Analogously, prey may also change the composition and quantity of defensive chemicals when they coexist with different predators, but such predator‐induced plasticity in chemical defenses remains elusive in vertebrates. In this study, we investigated whether tadpoles of the common toad (Bufo bufo) adjust their chemical defenses to predation risk in general and specifically to the presence of different predator species; furthermore, we assessed the adaptive value of the induced defense. We reared tadpoles in the presence or absence of one of four caged predator species in a mesocosm experiment, analyzed the composition and quantity of their bufadienolide toxins, and exposed them to free‐ranging predators. We found that toad tadpoles did not respond to predation risk by upregulating their bufadienolide synthesis. Fishes and newts consumed only a small percentage of toad tadpoles, suggesting that bufadienolides provided protection against vertebrate predators, irrespective of the rearing environment. Backswimmers consumed toad tadpoles regardless of treatment. Dragonfly larvae were the most voracious predators and consumed more predator‐naïve toad tadpoles than tadpoles raised in the presence of dragonfly cues. These results suggest that tadpoles in our experiment had high enough toxin levels for an effective defense against vertebrate predators even in the absence of predator cues. The lack of predator‐induced phenotypic plasticity in bufadienolide synthesis may be due to local adaptation for constantly high chemical defense against fishes in the study population and/or due to the high density of conspecifics.