Indirect facilitation of a native mesopredator by an invasive species: are cane toads re-shaping tropical riparian communities?

Top predators can suppress mesopredators both by killing them and by motivating changes in their behavior, and there are numerous examples of mesopredator release caused by declines in top predator populations. Demonstrated cases of invasive species triggering such releases among vertebrate trophic linkages (indirect facilitation), however, are rare. The invasive cane toad, Bufo marinus, has caused severe population-level declines in some Australian predators via lethal toxic ingestion. During a long-term study of the direct impacts of cane toads on predatory monitor lizards in tropical Australia, we documented significant, marked increases in annual counts of a mesopredator, the common tree snake (Dendrelaphis punctulatus). Mean snake counts during surveys of 70-km river transects at two sites increased from <1 individual per survey during 2001–2006, to 8–18 per survey in 2007. These increases occurred approximately 3 years following the arrival of cane toads, and 1–3 years after 71–96 % population declines in three species of predatory monitor lizards (Varanus panoptes, V. mertensi, and V. mitchelli). These data suggest a mesopredator release: the dramatic reduction of predatory monitor lizards caused increases in the tree snake by decreasing predation risk. The increases in tree snake counts were not attributable to either abiotic factors, or a trophic subsidy. The severe declines of predatory monitor lizards, coupled with recent evidence of cascading effects on their prey, suggest that cane toads are re-shaping riparian communities in tropical Australia through both direct negative effects and indirect facilitation.     

Cane toads a threat to West Indian wildlife: mortality of Jamaican boas attributable to toad ingestion

The notorious “cane toad” (Bufo marinus) is considered to be one of the 100 worst invasive species in the world. A native of South and Central America, Mexico, and the Rio Grande Valley of the United States, this large toad was intentionally introduced to islands in the Caribbean, and subsequently throughout the southern Pacific, as a biological control agent to combat sugar cane pests. Unfortunately, the primary result of those introductions has been deleterious impacts on native biotas, primarily through competition and predation. More recently, the cane toad has devastated populations of amphibian-eating predators in Australia, through the ingestion of this highly toxic anuran. Elsewhere, however, the impact of the toad on native predators has not been documented. Here we report the first evidence that the cane toad is impacting native predators in other geographic regions. Specifically, we document death due to cane toad poisoning in the endemic and threatened Jamaican boa (Epicrates subflavus). To our knowledge, this is the first report of cane toads causing mortality in naturally occurring predators outside of Australia. Like all members of the genus, B. marinus secretes a powerful bufogenin toxin, which is often fatal if ingested by naïve species that have not co-evolved with Bufo species. Our results should therefore serve as a warning that other endemic predator species in the West Indies and elsewhere may be at risk. Thus, efforts to control the population growth and spread of cane toads may be of even greater conservation concern than previously recognized.     

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.     

Adaptation or preadaptation: why are keelback snakes (<Emphasis Type="Italic">Tropidonophis mairii</Emphasis>) less vulnerable to invasive cane toads (<Emphasis Type="Italic">Bufo marinus</Emphasis>) than are other Australian snakes?

Biological invasions can expose native predators to novel prey which may be less nutritious or detrimental to predators. The introduction and subsequent spread of cane toads (Bufo marinus) through Australia has killed many anuran-eating snakes unable to survive the toad’s toxins. However, one native species, the keelback snake (Tropidonophis mairii), is relatively resistant to toad toxins and remains common in toad-infested areas. Is the keelback’s ability to coexist with toads a function of its ancestral Asian origins, or a consequence of rapid adaptation since cane toads arrived in Australia? And does the snake’s feeding preference for frogs rather than toads reflect an innate or learned behaviour? We compared keelback populations long sympatric with toads with a population that has encountered toads only recently. Unlike toad-vulnerable snake species, sympatry with toads has not affected keelback toxin tolerances or feeding responses: T. mairii from toad-sympatric and toad-naïve populations show a similar sensitivity to toad toxin, and a similar innate preference for frogs rather than toads. Feeding responses of neonatal keelbacks demonstrate that learning plays little or no role in the snake’s aversion to toads. Thus, behavioural aversion to B. marinus as prey, and physiological tolerance to toad toxins are pre-existing innate characteristics of Australian keelbacks rather than adaptations to the cane toad’s invasion of Australia. Such traits were most likely inherited from ancestral keelbacks that adapted to the presence of bufonids in Asia. Our results suggest that the impact of invasive species on native taxa may be strongly influenced by the biogeographic histories of the species involved.     

The ecological impact of commercial beehives on invasive cane toads (<Emphasis Type="Italic">Rhinella marina</Emphasis>) in eastern Australia

Understanding the factors that affect an invasive species’ viability and distribution has vital implications for biocontrol. In Australia, invasive cane toads (Rhinella marina) are anecdotally reported to utilise commercial beehives as a prey resource, but that interaction has never been studied in detail. We investigated the impact of apiaries on cane toads in northern New South Wales via mark-recapture surveys, dissections, and camera-trap observations. Cane toads were the most frequent visitors to apiaries, followed by bandicoots and corvid birds. Cane toads at apiaries were more abundant and in better body condition (i.e., larger mass relative to snout-urostyle length) than were toads at nearby control sites. Toads at beehives contained more prey items per stomach (mostly bees, which were never recorded in the stomachs of toads from other sites), and adult female toads at beehives had larger livers and ovaries relative to body size. We conclude that commercial apiaries attract cane toads, influence their diets, and increase their feeding rates and reproductive capacity. Like other habitat modifications wrought by agricultural activities, honey bee colonies provide resources that facilitate the spread of cane toads through an otherwise harsh landscape matrix. Minor modifications to beehives could exclude toads, thereby eliminating their positive impact on the invader.     

Wildfires modify the parasite loads of invasive cane toads

The frequency and severity of wildfires are increasing due to anthropogenic modifications to habitats and to climate. Post-fire landscapes may advantage invasive species via multiple mechanisms, including changes to host–parasite interactions. We surveyed the incidence of endoparasitic lungworms (Rhabdias pseudosphaerocephala) in invasive cane toads (Rhinella marina) in near-coastal sites of eastern Australia, a year after extensive fires in this region. Both the prevalence of infection and number of worms in infected toads increased with toad body size in unburned areas. By contrast, parasite load decreased with toad body size in burned areas. By killing moisture-dependent free-living lungworm larvae, the intense fires may have liberated adult cane toads from a parasite that can substantially reduce the viability of its host. Smaller toads, which are restricted to moist environments, did not receive this benefit from fires.     

Modification by an invasive ecosystem engineer shifts a wet prairie to a monotypic stand

At the landscape scale, ecosystem engineers are expected to increase species diversity; however, diversity could decline if the ecosystem engineer is over-abundant. Thus, invasive ecosystem engineers are expected to have strong impacts, due to their high abundances and novel disturbances. An invasive ecosystem engineer, the feral swine (Sus scrofa), is a species that creates intense soil disturbances, altering soil and plant communities. In this study, we examine the effects of this invasive ecosystem engineer on experimental plant plots that had been protected for over a decade. Feral swine avoided recently burned plots and preferred plots with N addition. Rooted plots shifted from a bunchgrass dominated wet prairie to a monotypic stand of the native, Lachnanthes caroliana. Feral swine were also attracted to plots with existing patches of L. caroliana suggesting a potential positive feedback between swine activity and L. caroliana patch expansion that could result in an alternative state.     

The influence of wild and cultivatedGramineae andCyperaceae on populations of sugarcane borers and their parasites in North India

Sugarcane borers frequently inhabit wild and semi-cultivated grasses growing in the proximity of cane fields. In India, in view of the year-round cultivation of sugarcane, wild grasses are not necessary for the perpetuation of borer species, but observations indicate that certain borer species migrate from wild or other cultivated grasses to cane, thereby increasing levels of infestation in cane during certain seasons. Parasitism of borer species when present in cane is compared with that in wild or other cultivated grasses.Telenomus spp. amongst egg parasites andApanteles flavipes amongst larval parasites are striking examples of parasites which show preference for the same borer species when they occur on wild hosts than on cane, as indicated by the degrees of parasitism. It is concluded that though wild grasses do not as a rule constitute a threat to the cultivation of sugarcane, they could indirectly influence borer populations in cane, parasitism of borers and consequently the extent of damage to cane. This study also reveals thatA. flavipes is highly polyphagous, attacking a number of host species occurring on a wide variety of host plants. Despite its polyphagous nature, it has proved extremely successful againstDiatraea saccharalis in Barbados, which indicates a need for some rethinking on the use of polyphagous natural enemies in biological control programmes.     

On the fringe of the invasion: the ecology of cane toads in marginally-suitable habitats

Understanding how invasive species flourish under climatic conditions outside those found within their native range can inform management. In southeastern Australia, cane toads (Rhinella marina) are spreading into montane areas cooler than have been predicted to be suitable. We monitored the presence of active toads in two high-elevation sites (750–1010 m above sea level [asl]) and two adjacent low-elevation sites (150–210 m asl) in northeastern New South Wales over spring and summer. We radio-tracked 28 field-collected adult toads (n = 5–9 toads per site) and quantified their thermoregulatory opportunities and body temperatures. Toads were active at low-elevation sites in spring, but were not seen in high-elevation sites until late summer. At low elevations, toads had access to a wide range of temperatures and selected cool diurnal refugia. In montane sites, toads had less control over their temperatures, because thermal differentials between exposed and sheltered microhabitats were smaller. Overall though, body temperatures of toads at high-elevation sites in summer were not different to those of conspecifics at lower elevations in spring. As a result, toads at high elevations moved as far (mean daily displacement around 50 m) as did low-elevation conspecifics. Toads in high elevations spent the day in superficial shelter, often partly exposed. Thus, although toads only appear in high-elevation sites seasonally, their behaviour at those sites (spending the day exposed; moving extensively at night) likely exacerbates their ecological impact by bringing them to the attention of vulnerable native predators.     

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.     

Skin resistance to water gain and loss has changed in cane toads (Rhinella marina) during their Australian invasion

The water‐permeable skin of amphibians renders them highly sensitive to climatic conditions, and interspecific correlations between environmental moisture levels and rates of water exchange across the skin suggest that natural selection adapts hydroregulatory mechanisms to local challenges. How quickly can such mechanisms shift when a species encounters novel moisture regimes? Cutaneous resistance to water loss and gain in wild‐caught cane toads (Rhinella marina) from Brazil, USA (Hawai''i) and Australia exhibited strong geographic variation. Cutaneous resistance was low in native‐range (Brazilian) toads and in Hawai''ian populations (where toads were introduced in 1932) but significantly higher in toads from eastern Australia (where toads were introduced in 1935). Toads from recently invaded areas in western Australia exhibited cutaneous resistance to water loss similar to the native‐range populations, possibly because toads are restricted to moist sites within this highly arid landscape. Rates of rehydration exhibited significant but less extreme geographic variation, being higher in the native range than in invaded regions. Thus, in less than a century, cane toads invading areas that impose different climatic challenges have diverged in the capacity for hydroregulation.     

Frogs in the spotlight: a 16‐year survey of native frogs and invasive toads on a floodplain in tropical Australia

Although widespread declines in anuran populations have attracted considerable concern, the stochastic demographics of these animals make it difficult to detect consistent trends against a background of spatial and temporal variation. To identify long‐term trends, we need datasets gathered over long time periods, especially from tropical areas where anuran biodiversity is highest. We conducted road surveys of four anurans in the Australian wet–dry tropics on 4637 nights over a 16‐year period. Our surveys spanned the arrival of invasive cane toads (Rhinella marina), allowing us to assess the invader's impact on native anuran populations. Our counts demonstrate abrupt and asynchronous shifts in abundance and species composition from one year to the next, not clearly linked to rainfall patterns. Typically, periods of decline in numbers of a species were limited to 1–2 years and were followed by 1‐ to 2‐year periods of increase. No taxa showed consistent declines over time, although trajectories for some species showed significant perturbations coincident with the arrival of toads. None of the four focal frog species was less common at the end of the study than at the beginning, and three of the species reached peak abundances after toad arrival. Survey counts of cane toads increased rapidly during the initial stage of invasion but have subsequently declined and fluctuated. Distinguishing consistent declines versus stochastic fluctuations in anuran populations requires extensive time‐series analysis, coupled with an understanding of the shifts expected under local climatic conditions. This is especially pertinent when assessing impacts of specific perturbations such as invasive species.     

Detecting the impact of invasive species on native fauna: Cane toads (Bufo marinus), frillneck lizards (Chlamydosaurus kingii) and the importance of spatial replication

An understanding of which native species are severely impacted by an anthropogenic change (such as the arrival of an invasive species) and which are not is critical to prioritizing conservation efforts. However, it is difficult to detect such impacts if the native taxa exhibit strong stochastic variations in abundance; a ‘natural’ population decline might be wrongly interpreted as an impact of the invader. Frillneck lizards (Chlamydosaurus kingii) are large iconic Australian agamids, and have been reported to decline following the invasion of toxic cane toads. We monitored three populations of the species in the savanna woodland of tropical Australia over a 7‐year period bracketing toad arrival. One population crashed, one remained stable and one increased. Hence, studies on any single population might have inferred that cane toads have negative, negligible or positive effects on frillneck lizards. With the benefit of spatial replication, and in combination with observations of prey choice by captive lizards, our data suggest that invasive cane toads have had little or no effect on frillneck abundance.     

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.     

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.     

The Interacting Effects of Ungulate Hoofprints and Predatory Native Ants on Metamorph Cane Toads in Tropical Australia

Many invasive species exploit the disturbed habitats created by human activities. Understanding the effects of habitat disturbance on invasion success, and how disturbance interacts with other factors (such as biotic resistance to the invaders from the native fauna) may suggest new ways to reduce invader viability. In tropical Australia, commercial livestock production can facilitate invasion by the cane toad (Rhinella marina), because hoofprints left by cattle and horses around waterbody margins provide distinctive (cool, moist) microhabitats; nevertheless the same microhabitat can inhibit the success of cane toads by increasing the risks of predation or drowning. Metamorph cane toads actively select hoofprints as retreat-sites to escape dangerous thermal and hydric conditions in the surrounding landscape. However, hoofprint geometry is important: in hoofprints with steep sides the young toads are more likely to be attacked by predatory ants (Iridomyrmex reburrus) and are more likely to drown following heavy rain. Thus, anthropogenic changes to the landscape interact with predation by native taxa to affect the ability of cane toads in this vulnerable life-history stage to thrive in the harsh abiotic conditions of tropical Australia.     

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.     

The impact of invasive cane toads on native wildlife in southern Australia

Commonly, invaders have different impacts in different places. The spread of cane toads (Rhinella marina: Bufonidae) has been devastating for native fauna in tropical Australia, but the toads' impact remains unstudied in temperate‐zone Australia. We surveyed habitat characteristics and fauna in campgrounds along the central eastern coast of Australia, in eight sites that have been colonized by cane toads and another eight that have not. The presence of cane toads was associated with lower faunal abundance and species richness, and a difference in species composition. Populations of three species of large lizards (land mullets Bellatorias major, eastern water dragons Intellagama lesueurii, and lace monitors Varanus varius) and a snake (red‐bellied blacksnake Pseudechis porphyriacus) were lower (by 84 to 100%) in areas with toads. The scarcity of scavenging lace monitors in toad‐invaded areas translated into a 52% decrease in rates of carrion removal (based on camera traps at bait stations) and an increase (by 61%) in numbers of brush turkeys (Alectura lathami). The invasion of cane toads through temperate‐zone Australia appears to have reduced populations of at least four anurophagous predators, facilitated other taxa, and decreased rates of scavenging. Our data identify a paradox: The impacts of cane toads are at least as devastating in southern Australia as in the tropics, yet we know far more about toad invasion in the sparsely populated wilderness areas of tropical Australia than in the densely populated southeastern seaboard.     

Adrenocortical stress responses influence an invasive vertebrate's fitness in an extreme environment

Continued range expansion into physiologically challenging environments requires invasive species to maintain adaptive phenotypic performance. The adrenocortical stress response, governed in part by glucocorticoid hormones, influences physiological and behavioural responses of vertebrates to environmental stressors. However, any adaptive role of this response in invasive populations that are expanding into extreme environments is currently unclear. We experimentally manipulated the adrenocortical stress response of invasive cane toads (Rhinella marina) to investigate its effect on phenotypic performance and fitness at the species'' range front in the Tanami Desert, Australia. Here, toads are vulnerable to overheating and dehydration during the annual hot–dry season and display elevated plasma corticosterone levels indicative of severe environmental stress. By comparing unmanipulated control toads with toads whose adrenocortical stress response was manipulated to increase acute physiological stress responsiveness, we found that control toads had significantly reduced daily evaporative water loss and higher survival relative to the experimental animals. The adrenocortical stress response hence appears essential in facilitating complex phenotypic performance and setting fitness trajectories of individuals from invasive species during range expansion.