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.     

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.     

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.     

Fatal attraction: adaptations to prey on native frogs imperil snakes after invasion of toxic toads

Adaptations that enhance fitness in one situation can become liabilities if circumstances change. In tropical Australia, native snake species are vulnerable to the invasion of toxic cane toads. Death adders (Acanthophis praelongus) are ambush foragers that (i) attract vertebrate prey by caudal luring and (ii) handle anuran prey by killing the frog then waiting until the frog''s chemical defences degrade before ingesting it. These tactics render death adders vulnerable to toxic cane toads (Bufo marinus), because toads elicit caudal luring more effectively than do native frogs, and are more readily attracted to the lure. Moreover, the strategy of delaying ingestion of a toad after the strike does not prevent fatal poisoning, because toad toxins (unlike those of native frogs) do not degrade shortly after the prey dies. In our laboratory and field trials, half of the death adders died after ingesting a toad, showing that the specialized predatory behaviours death adders use to capture and process prey render them vulnerable to this novel prey type. The toads'' strong response to caudal luring also renders them less fit than native anurans (which largely ignored the lure): all toads bitten by adders died. Together, these results illustrate the dissonance in behavioural adaptations that can arise following the arrival of invasive species, and reveal the strong selection that occurs when mutually naive species first interact.     

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.     

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).     

Cues for cannibalism: cane toad tadpoles use chemical signals to locate and consume conspecific eggs

Although animals of many species kill and consume conspecifics, most such cases probably involve serendipitous encounters between the individuals concerned. In some taxa, however, cannibalism is an active process, with predatory individuals searching out and consuming specific types of conspecific prey items. Although anuran tadpoles often have been reported to consume conspecific eggs, this behaviour has been interpreted as a by‐product of usual foraging behaviours rather than a result of targeted searching. Our field and laboratory studies in tropical Australia show that the tadpoles of invasive cane toads Bufo marinus are strongly attracted to chemical cues from conspecific eggs; the effective cues are released late in embryonic development, as the jelly coat breaks down. Tadpoles of native Australian frog species were attracted to the eggs of toads only rarely. If deployed as bait in traps, chemical cues from toad eggs could provide a way to selectively remove toad larvae from waterbodies.     

The enduring toxicity of road-killed cane toads (<Emphasis Type="Italic">Rhinella marina</Emphasis>)

The primary ecological impact of invasive cane toads (Rhinella marina) in Australia is mediated by their powerful toxins, which are fatal to many native species. Toads use roads as invasion corridors and feeding sites, resulting in frequent road-kills. The flattened, desiccated toad carcasses remain highly toxic despite being heated daily to >40°C for many months during the tropical dry-season. In controlled laboratory experiments, native tadpoles (Cyclorana australis, Litoria rothii), fishes (Mogurnda mogurnda) and leeches (Family Erpobdellidae) died rapidly when we added fragments of sun-dried toad to their water, even if the native animals had no physical access to the carcass. Given the opportunity, native tadpoles and fishes strongly avoided the vicinity of dried toad fragments. Hence, long-dead toads may contaminate roadside ponds formed by early wet-season rains and induce avoidance and/or mortality of native anuran larvae, fishes and invertebrates. Our studies show that the toxicity of this invasive species does not end with the toad’s death, and that methods for disposing of toad carcasses (e.g., after culling operations) need to recognize the persistent danger posed by those carcasses.     

Embryonic exposure to conspecific chemicals suppresses cane toad growth and survival

Adaptations to suppress the viability of conspecifics may provide novel ways to control invasive taxa. The spread of cane toads (Rhinella marina) through tropical Australia has had severe ecological impacts, stimulating a search for biocontrol. Our experiments show that cane toad tadpoles produce waterborne chemical cues that suppress the viability of conspecifics encountering those cues during embryonic development. Brief (72 h) exposure to these cues in the egg and post-hatching phases massively reduced rates of survival and growth of larvae. Body sizes at metamorphosis (about three weeks later) were almost twice as great in control larvae as in tadpole-exposed larvae. The waterborne cue responsible for these effects might provide a weapon to reduce toad recruitment within the species' invaded range.     

Responses of Australian wading birds to a novel toxic prey type, the invasive cane toad Rhinella marina

The impact of invasive predators on native prey has attracted considerable scientific attention, whereas the reverse situation (invasive species being eaten by native predators) has been less frequently studied. Such interactions might affect invasion success; an invader that is readily consumed by native species may be less likely to flourish in its new range than one that is ignored by those taxa. Invasive cane toads (Rhinella marina) in Australia have fatally poisoned many native predators (e.g., marsupials, crocodiles, lizards) that attempt to ingest the toxic anurans, but birds are more resistant to toad toxins. We quantified prey preferences of four species of wading birds (Nankeen night heron, purple swamphen, pied heron, little egret) in the wild, by offering cane toads and alternative native prey items (total of 279 trays offered, 14 different combinations of prey types). All bird species tested preferred the native prey, avoiding both tadpole and metamorph cane toads. Avoidance of toads was strong enough to reduce foraging on native prey presented in combination with the toads, suggesting that the presence of cane toads could affect predator foraging tactics, and reduce the intensity of predation on native prey species found in association with toads.     

Impact of the invasive cane toad (Bufo marinus) on an Australian frog (Opisthodon ornatus) depends on minor variation in reproductive timing

Invasive species are widely viewed as unmitigated ecological catastrophes, but the reality is more complex. Theoretically, invasive species could have negligible or even positive effects if they sufficiently reduce the intensity of processes regulating native populations. Understanding such mechanisms is crucial to predicting ultimate ecological impacts. We used a mesocosm experiment to quantify the impact of eggs and larvae of the introduced cane toad (Bufo marinus) on fitness-related traits (number, size and time of emergence of metamorphs) of a native Australian frog species (Opisthodon ornatus). The results depended upon the timing of oviposition of the two taxa, and hence the life-history stages that came into contact. Growth and survival of O. ornatus tadpoles were enhanced when they preceded B. marinus tadpoles into ponds, and reduced when they followed B. marinus tadpoles into ponds, relative to when tadpoles of both species were added to ponds simultaneously. The dominant tadpole-tadpole interaction is competition, and the results are consistent with competitive priority effects. However, these priority effects were reduced or reversed when O. ornatus tadpoles encountered B. marinus eggs. Predation on toxic toad eggs reduced the survival of O. ornatus and B. marinus. The consequent reduction in tadpole densities allowed the remaining O. ornatus tadpoles to grow more rapidly and to metamorphose at larger body sizes (>60% disparity in mean mass). Thus, exposure to B. marinus eggs reduced the number of O. ornatus metamorphs, but increased their body sizes. If the increased size at metamorphosis more than compensates for the reduced survival, the effective reproductive output of native anurans may be increased rather than decreased by the invasive toad. Minor interspecific differences in the seasonal timing of oviposition thus have the potential to massively alter the impact of invasive cane toads on native anurans.     

School for Skinks: Can Conditioned Taste Aversion Enable Bluetongue Lizards (Tiliqua scincoides) to Avoid Toxic Cane Toads (Rhinella marina) as Prey?

The invasion of cane toads (Rhinella marina) through Australia imperils native predators that are killed if they consume these toxic anurans. The magnitude of impact depends upon the predators’ capacity for aversion learning: toad impact is lower if predators can learn not to attack toads. In laboratory trials, we assessed whether bluetongue lizards (Tiliqua scincoides) – a species under severe threat from toads – are capable of learned taste aversion and whether we can facilitate that learning by exposing lizards to toad tissue combined with a nausea‐inducing chemical (lithium chloride). Captive bluetongues rapidly learned to avoid the ‘unpalatable’ food. Taste aversion also developed (albeit less strongly) in response to meals of minced cane toad alone. Our data suggest that taste aversion learning may help bluetongue lizards survive the onslaught of cane toads, but that many encounters will be fatal because the toxin content of toads is so high relative to lizard tolerance of those toxins. Thus, baiting with nausea‐inducing (but non‐lethal) toad products might provide a feasible management option to reduce the impact of cane toad invasion on these native predators.     

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

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Interacting impacts of invasive plants and invasive toads on native lizards

The ecological impacts of an invasive species may be reduced by prior invasions if selective pressures imposed by earlier events preadapt the native biota to deal with the newer arrival. In northwestern Australia, invasion of the cane toad (Rhinella marina) kills many native predators if they ingest the highly toxic toads. Remarkably, the toads' defensive toxins (bufadienolides) are chemically similar to those of another invasive species: an ornamental plant from Madagascar, Bryophyllum spp. (Crassulaceae, mother-of-millions). Omnivorous lizards (bluetongue skinks, Tiliqua scincoides) are imperiled by the invasion of toads in northwestern Australia, but conspecifics from other areas of the continent (those where exotic plants were introduced and including areas where toads have yet to invade) are less affected because they exhibit higher physiological tolerance of toad toxins (and also of plant toxins). The willingness of captive bluetongues to consume both toads and these plants and the high correlation in the lizards' sensitivity to toad toxins versus plant toxins suggest that exotic plants may have imposed strong selection on the lizards' physiological tolerance of bufadienolides. As a result, populations of lizards from areas previously exposed to these alien plants may be preadapted to deal with the toxins of the more recent anuran invader.     

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.     

Behavioural flexibility allows an invasive vertebrate to survive in a semi-arid environment

Plasticity or evolution in behavioural responses are key attributes of successful animal invasions. In northern Australia, the invasive cane toad (Rhinella marina) recently invaded semi-arid regions. Here, cane toads endure repeated daily bouts of severe desiccation and thermal stress during the long dry season (April–October). We investigated whether cane toads have shifted their ancestral nocturnal rehydration behaviour to one that exploits water resources during the day. Such a shift in hydration behaviour could increase the fitness of individual toads by reducing exposure to desiccation and thermal stress suffered during the day even within terrestrial shelters. We used a novel method (acoustic tags) to monitor the daily hydration behaviour of 20 toads at two artificial reservoirs on Camfield station, Northern Territory. Remarkably, cane toads visited reservoirs to rehydrate during daylight hours, with peaks in activity between 9.00 and 17.00. This diurnal pattern of rehydration activity contrasts with nocturnal rehydration behaviour exhibited by adult toads in their native geographical range and more mesic parts of Australia. Our results demonstrate that cane toads phase shift a key behaviour to survive in a harsh semi-arid landscape. Behavioural phase shifts have rarely been reported in invasive species but could facilitate ongoing invasion success.     

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.     

Active foraging for toxic prey during gestation in a snake with maternal provisioning of sequestered chemical defences

Many animals sequester dietary defensive compounds and incorporate them into the offspring, which protects the young against predation. One possible but poorly investigated question is whether females of such species actively prey upon toxic diets. The snake Rhabdophis tigrinus sequesters defensive steroids from toads consumed as prey; it also feeds on other amphibians. Females produce chemically armed offspring in direct proportion to their own level of toad-derived toxins by provisioning the toxins to their eggs. Our field observations of movements and stomach contents of radio-tracked R. tigrinus showed that gravid snakes preyed upon toads by actively foraging in the habitat of toads, even though toads were a scarce resource and toad-searching may incur potential costs. Our Y-maze experiments demonstrated that gravid females were more likely to trail the chemical cues of toads than were males or non-gravid females. These results showed behavioural switching in females and active foraging for scarce, toxic prey during gestation. Because exploitation of toads by gravid females results in their offspring being more richly endowed with prey-derived toxins, active foraging for toxic prey is expected to be an adaptive antipredator trait, which may enhance chemical defence in offspring.     

Behavioural responses of native predators to an invasive toxic prey species

One important impact of invasive species may be to modify the behaviour of native taxa. For example, the invasion of highly toxic cane toads (Bufo marinus) kills many anurophagous native predators, but other predators learn to recognize and avoid the toxic invader. We exposed native fish (northern trout gudgeons, Mogurnda mogurnda) and Dahl's aquatic frogs (Litoria dahlii) to cane toad tadpoles, then monitored the predator's responses during subsequent trials. Both the frogs and fish initially attacked toad tadpoles, but rapidly learned not to do so. Fish and adult frogs retained their aversion for at least a week, whereas recently metamorphosed frogs did not. Clearly, the spread of cane toads through tropical Australia can modify feeding responses of native aquatic predators. For predators capable of rapid avoidance learning, the primary impact of cane toads may be on foraging behaviour rather than mortality.     

Effects of an invasive species on refuge‐site selection by native fauna: The impact of cane toads on native frogs in the Australian tropics

Invasive species can induce shifts in habitat use by native taxa: either by modifying habitat availability, or by repelling or attracting native species to the vicinity of the invader. The ongoing invasion of cane toads (Rhinella marina) through tropical Australia might affect native frogs by affecting refuge‐site availability, because both frogs and toads frequently shelter by day in burrows. Our laboratory and field studies in the wet‐dry tropics show that native frogs of at least three species (Litoria tornieri, Litoria nasuta and Litoria dahlii) preferentially aggregate with conspecifics, and with (some) other species of native frogs. However, the frogs rarely aggregated with cane toads either in outdoor arenas or in standardized experimental burrows that we monitored in the field. The native frogs that we tested either avoided burrows containing cane toads (or cane toad scent) or else ignored the stimulus (i.e. treated such a burrow in the same way as they did an empty burrow). Native frogs selected a highly non‐random suite of burrows as diurnal retreat sites, whereas cane toads were less selective. Hence, even in the absence of toads, frogs do not use many of the burrows that are suitable for toads. The invasion of cane toads through tropical Australia is unlikely to have had a major impact on retreat‐site availability for native frogs.