Cane Toad Bufo Marinus Research Articles

Factors affecting the vulnerability of cane toads (Bufo marinus) to predation by ants

Experimental evidence on the determinants of prey vulnerability is scarce, especially for vertebrates in the field. Invasive species offer robust opportunities to explore prey vulnerability, because the intensity of predation on or by such animals has not been eroded by coevolution. Around waterbodies in tropical Australia, native meat ants (Iridomyrmex reburrus) consume many metamorph cane toads (Bufo marinus, an invasive anuran). We document the determinants of toad vulnerability, especially the roles of toad body size and ant density. Larger metamorphs were attacked sooner (because they attracted more ants), but escaped more often. Overall, smaller toads were more likely to be killed. Ant densities influenced toad responses, as well as attack rate and success. Data on the immediate outcomes of attacks underestimate mortality: more than 73% of apparent ‘escapees’ died within 24 h. Because mortality during this period was independent of toad size, predation was less size selective than suggested by immediate outcomes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 738–751.

Adaptation or preadaptation: why are keelback snakes (Tropidonophis mairii) less vulnerable to invasive cane toads (Bufo marinus) 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-naive 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.

Indirect ecological impacts of an invasive toad on predator–prey interactions among native species

One of the many ways that invasive species can affect native ecosystems is by modifying the behavioural and ecological interactions among native species. For example, the arrival of the highly toxic cane toad (Bufo marinus) in tropical Australia has induced toad-aversion in some native predators. Has that shift also affected the predators’ responses to native prey—for example, by reducing vulnerability of native tadpoles via a mimicry effect, or increasing vulnerability of other prey types (such as insects) via a shift in predator feeding tactics? We exposed a native predator (northern trout gudgeon, Mogurnda mogurnda) to toad tadpoles in the laboratory, and measured effects of that exposure on the fish’s subsequent intake of native tadpoles and crickets. As predicted, toad-exposed fishes reduced their rate of predation on (palatable) tadpoles of native frogs (Litoria caerulea and L. nasuta). If alternative prey (crickets) were available also, the toad-exposed fishes shifted even more strongly away from predation on native tadpoles. Thus, invasion of a toxic species can provide a mimicry benefit to native taxa that resemble the invader, and can shift predation pressure onto other taxa.

Parasites and pathogens lag behind their host during periods of host range advance

The process of rapid range expansion (as seen in many invasive species, and in taxa responding to climate change) may substantially disrupt host-parasite dynamics. Parasites and pathogens can have strong regulatory effects on their host population and, in doing so, exert selection pressure on host life history. We construct a simple individual-based model of host-parasite dynamics during range expansion. This model shows that the parasites and pathogens of a range-expanding host are likely to be absent from the host's invasion front, because stochastic events (serial founder events) in low-density frontal populations result in local extinctions or transmission failure of the parasite/pathogen and, hence, a preponderance of uninfected hosts in the invasion vanguard. This pattern is true for both density-dependent and density-independent transmission rates, although it is exacerbated in the case of density-dependent transmission because, in this case, transmission rates also decline on the front. Data from field surveys on the prevalence of lungworms (Rhabdias pseudosphaerocephala) in invasive cane toads (Bufo marinus) support these predictions, in showing that toads in newly invaded areas of tropical Australia lack the parasite, which only arrives 1-3 years after the toads themselves. The resultant "honeymoon phase" immediately post-invasion, when individuals in the invasion-front population are virtually pathogen-free, may lead to altered host population dynamics on the invasion front, causing, for example, high densities in invasion-front populations, followed by a decline in numbers as parasites and pathogens arrive and begin to reduce host viability. The honeymoon phase may ultimately impact the evolution of life-history investment strategies in both host and parasite on the invasion vanguard, as hosts are released from immune challenges and parasites continuously expand into a favorable and unoccupied niche.

Turgid female toads give males the slip: a new mechanism of female mate choice in the Anura

In many anuran species, males vocalize to attract females but will grasp any female that comes within reach and retain their hold unless displaced by a rival male. Thus, female anurans may face strong selection to repel unwanted suitors, but no mechanism is known for doing so. We suggest that a defensive trait (the ability to inflate the body to ward off attack) has been co-opted for this role: by inflating their bodies, females are more difficult for males to grasp and hence, it is easier for another male to displace an already amplexed rival. Inflating a model female cane toad (Bufo marinus) strongly reduced a male's ability to maintain amplexus; and females who were experimentally prevented from inflating their bodies experienced no successful takeovers from rival males, in contrast to control females. Thus, the ability of a female cane toad to inflate her body may allow her to manipulate the outcome of male-male competition. This overlooked mechanism of anuran mate choice may reflect a common evolutionary pattern, whereby females co-opt defensive traits for use in sexual selection.

The power of myth: the (non) impact of invasive cane toads (Bufo marinus) on domestic chickens (Gallus gallus)

Myths about invasive species are widespread in the general community, even when contrary to scientific evidence. Public revulsion against invasive cane toads (Bufo marinus) in Australia has encouraged the belief that toads pose a significant risk to domestic poultry, by poisoning fowls that eat toads or that drink water contaminated by toads. Although discredited by scientists in 1938, within 2 years of the toads’ introduction to Australia, the myth continues to flourish. We conducted experimental trials to evaluate the vulnerability of chickens to toad-contaminated water, and to toad ingestion. No ill effects were seen, with one chicken consuming 45 small toads without falling ill. Thus, available evidence suggests that cane toads do not imperil domestic poultry.

GENOTYPIC ANALYSIS OF MUCOR FROM THE PLATYPUS IN AUSTRALIA

Mucor amphibiorum is the only pathogen known to cause significant morbidity and mortality in the free-living platypus (Ornithorhynchus anatinus) in Tasmania. Infection has also been reported in free-ranging cane toads (Bufo marinus) and green tree frogs (Litoria caerulea) from mainland Australia but has not been confirmed in platypuses from the mainland. To date, there has been little genotyping specifically conducted on M. amphibiorum. A collection of 21 Mucor isolates representing isolates from the platypus, frogs and toads, and environmental samples were obtained for genotypic analysis. Internal transcribed spacer (ITS) region sequencing and GenBank comparison confirmed the identity of most of the isolates. Representative isolates from infected platypuses formed a clade containing the reference isolates of M. amphibiorum from the Centraal Bureau voor Schimmelcultures repository. The M. amphibiorum isolates showed a close sequence identity with Mucor indicus and consisted of two haplotypes, differentiated by single nucleotide polymorphisms within the ITS1 and ITS2 regions. With the exception of isolate 96-4049, all isolates from platypuses were in one haplotype. Multilocus fingerprinting via the use of intersimple sequence repeats polymerase chain reaction identified 19 genotypes. Two major clusters were evident: 1) M. amphibiorum and Mucor racemosus; and 2) Mucor circinelloides, Mucor ramosissimus, and Mucor fragilis. Seven M. amphibiorum isolates from platypuses were present in two subclusters, with isolate 96-4053 appearing genetically distinct from all other isolates. Isolates classified as M. circinelloides by sequence analysis formed a separate subcluster, distinct from other Mucor spp. The combination of sequencing and multilocus fingerprinting has the potential to provide the tools for rapid identification of M. amphibiorum. Data presented on the diversity of the pathogen and further work in linking genetic diversity to functional diversity will provide critical information for its management in Tasmanian river systems.

Adjusting to a toxic invader: native Australian frogs learn not to prey on cane toads

Biological invasions provide opportunities to study novel behavioral interactions between predators and their prey. To withstand detrimental effects from a potentially lethal invader, a native taxon must somehow adjust to the invader’s presence. Cane toads (Bufo marinus) are highly toxic to native Australian anurans and constitute a major threat if consumed. We recorded the responses of Australian marbled frogs (Limnodynastes convexiusculus) during their first encounters with edible-sized cane toads. The frogs exhibited rapid avoidance learning: toad-exposed frogs were less likely to attack subsequently encountered cane toads (and hence more likely to survive). Among-clutch variance in learning rates and in physiological tolerance to toad toxins was low, suggesting that genetically based adaptive changes to frog feeding responses will be slow (especially given that rapid learning reduces mortality and thus reduces the fitness decrement of initial willingness to attack a toad). Hence, rapid taste aversion learning is the primary mechanism enabling marbled frogs to persist in the presence of a potentially fatal invader. In combination with previous work, our study shows that some native predators adjust to the threat posed by cane toad invasion via taste aversion learning, whereas others show genetically based modification of feeding responses. More generally, both learning and adaptation enable vulnerable native taxa to survive the arrival of a toxic invasive species. Key words: behavior, Bufo marinus, frog, invasive species, learning, predator. [Behav Ecol]

Predation on toxic cane toads (Bufo marinus) may imperil bluetongue lizards (Tiliqua scincoides intermedia, Scincidae) in tropical Australia

Context. Detecting ecological impacts of invasive species can be extremely difficult. Even major population declines may be undetectable without extensive long-term data if the affected taxon is rare and/or difficult to census, and exhibits stochastic variation in abundance as a result of other factors. Our data suggest such a situation in an iconic Australian reptile species, the bluetongue lizard. Originally restricted to Central and South America, cane toads (Bufo marinus) are rapidly spreading through tropical Australia. Most native predators have no evolutionary history of exposure to the toads’ distinctive chemical defences (bufadienolides), and many varanid lizards, elapid snakes, crocodiles and marsupials have been killed when they have attempted to consume toads. Aims. Scincid lizards have not been considered vulnerable to toad invasion; however, one lineage (the bluetongues, genus Tiliqua) consists of large omnivores that may be affected. Our field and laboratory research aimed to elucidate this concern. Methods. Nightly surveys for bluetongue lizards (Tiliqua scincoides intermedia) and cane toads were conducted along two adjacent roadways on the Adelaide River floodplain of the Northern Territory. Scent discrimination trials in the laboratory assessed lizard responses to chemical cues from three food types (native frogs, cane toads and ‘preferred foods’) by counting tongue-flicks and biting elicited by cotton swabs. A subset of lizards was presented with live toads. Key results. Numbers of bluetongues encountered during standardised field surveys in the Darwin region declined soon after toads arrived, and we have not recorded a single lizard for the last 20 months. In the laboratory, foraging responses of bluetongues were as intense to cane-toad scent as to the scent of native frogs, and many of the lizards we tested attempted to consume toads, and were poisoned as a result. Conclusions and implications. The population decline of bluetongues in this region appears to have been the direct result of fatal ingestion of toxic cane toads. Our studies thus add a scincid lizard species to the list of native Australian predators imperilled by cane-toad invasion, and point to the difficulty of detecting invader impact even for an iconic species in a system subject to detailed survey work.

Predator behaviour and morphology mediates the impact of an invasive species: cane toads and death adders in Australia

AbstractThe arrival of an invasive species can have severe impacts on native species. The extent of the impact, as well as the speed at which native species may mount an adaptive response, depend upon the correlation between impact and the individual phenotypes of the native species. Strong correlation between phenotype and impact within the native species raises the possibility of rapid adaptive response to the invader. Here, we examine the impact of a dangerous newly arrived prey species (the highly toxic cane toad Bufo marinus) on naïve predators (death adders Acanthophis praelongus) in northern Australia. During laboratory trials and field radiotracking, toads killed 48% of the adders we studied. Long‐term monitoring of the population also suggests a massive decline (>89%) in recent years concurrent with the arrival of toads. Variation in snake physiology (resistance to toad toxin) had little bearing on snake survival in the field. Snake behaviour (tendency to attack toads) and morphology (body size and head size), however, were strong predictors of snake survival. Smaller snakes with relatively small heads, and snakes that were unwilling to attack toads in the laboratory, had much higher survival rates in the field. These results show that toads have a massive impact on death adder populations, but that snake phenotypes strongly mediate this impact. Thus natural selection is operating on these adder populations and an adaptive response is a possibility. If these adders can rapidly shift toad‐relevant morphological and behavioural traits (either through plastic or evolved means), they will ultimately face a lowered impact from this toxic invader.

Impact of Invasive Cane Toads on Australian Birds

The cane toad (Bufo marinus), a large, toxic, American anuran, was introduced to Australia in 1935. Populations of many of Australia's reptiles (snakes, varanid lizards, crocodiles) and carnivorous mammals (dasyurid marsupials) have declined because these predators are killed by the toad's powerful toxins. In contrast to these well-studied species, little is known about the cane toads impacts on Australian birds. We reviewed published and unpublished data on behavioral interactions between Australian avian predators and cane toads and collated distributional and dietary information to identify avian taxa potentially at risk from cane toad invasion. Cane toads are sympatric with 172 frog-eating bird species in Australia, and an additional 8 bird species overlap with the predicted future range of the toad. Although many bird species thus are potentially at risk, behavioral observations suggest the risk level is generally low. Despite occasional reports of Australian birds being killed when they ingest cane toads, most birds either ignore toads or survive the predation event. The apparently higher tolerance of Australian birds to toad toxins, compared with Australian reptiles and marsupials, may reflect genetic exchange between Australian birds and Asian populations that encounter other bufonid species regularly and hence have evolved the capacity to recognize or tolerate this toxic prey.

Z and W sex chromosomes in the cane toad (Bufo marinus)

The cane toad (Bufo marinus) is one of the most notorious animal pests encountered in Australia. Members of the genus Bufo historically have been regarded as having genotypic sex determination with male homogamety/female heterogamety. Nevertheless, as with many toads, karyotypic analyses of the cane toad have so far failed to identify heteromorphics sex chromosomes. In this study, we used comparative genomic hybridization, reverse fluorescence staining, C-banding, and morphometric analyses of chromosomes to characterize sex chromosome dimorphism in B. marinus. We found that females consistently had a length dimorphism associated with a nucleolus organizer region (NOR) on one of the chromosome 7 pair. A strong signal over the longer NOR in females, and the absence of a signal in males indicated sex-specific DNA sequences. All females were heterozygous and all males homozygous, indicating a ZZ/ZW sex chromosomal system. Our study confirms the existence of sex chromosomes in this species. The ability to reliably identify genotypic sex of cane toads will be of value in monitoring and control efforts in Australia and abroad.

Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area

Cane toads (Bufo marinus) are now moving about 5 times faster through tropical Australia than they did a half-century ago, during the early phases of toad invasion. Radio-tracking has revealed higher daily rates of displacement by toads at the invasion front compared to those from long-colonised areas: toads from frontal populations follow straighter paths, move more often, and move further per displacement than do toads from older (long-established) populations. Are these higher movement rates of invasion-front toads associated with modified locomotor performance (e.g. speed, endurance)? In an outdoor raceway, toads collected from the invasion front had similar speeds, but threefold greater endurance, compared to conspecifics collected from a long-established population. Thus, increased daily displacement in invasion-front toads does not appear to be driven by changes in locomotor speed. Instead, increased dispersal is associated with higher endurance, suggesting that invasion-front toads tend to spend more time moving than do their less dispersive conspecifics. Whether this increased endurance is a cause or consequence of behavioural shifts associated with rapid dispersal is unclear. Nonetheless, shifts in endurance between frontal and core populations of this invasive species point to the complex panoply of traits affected by selection for increased dispersal ability on expanding population fronts.

Larval alarm pheromones as a potential control for invasive cane toads (Bufo marinus) in tropical Australia

Novel approaches to control invasive species are urgently needed. Cane toads (Bufo marinus) are large, highly toxic anurans that are spreading rapidly through tropical Australia. Injured toad larvae produce an alarm pheromone that elicits rapid avoidance by conspecifics but not by frog larvae. Experiments in outdoor ponds show that repeated exposure to the pheromone reduced toad tadpole survival rates (by >50%) and body mass at metamorphosis (by 20%). The alarm pheromone did not induce tadpoles to seek shelter, but accelerated ontogenetic differentiation. Perhaps reflecting mortality of weaker individuals during larval life, growth rates post-metamorphosis were higher in animals emerging from the pheromone exposure treatment than from the control treatment. Nonetheless, body size differentials established at metamorphosis persisted through the first 8 days of post-metamorphic life. We will need substantial additional research before evaluating whether the alarm pheromone provides a way to reduce cane toad recruitment in nature, but our field trials are encouraging in this respect.

Evidence for Predation on Terrestrial Cane Toads 'Bufo Marinus' by the Sooty Grunter 'Hephaestus Fuliginosus' in Northern Australia

Expansion of the Cane Toad Bufo marinus across Australia has been implicated in the population declines of a range of indigenous terrestrial and semi-aquatic vertebrate fauna. Stomach content analysis of a number of Sooty Grunter 'Hephaestus fuliginosus' recently collected in the Northern Territory has highlighted occasional consumption of the terrestrial life history stages of Cane Toads by this widespread northern Australian freshwater fish, with minimal apparent effect. The impacts of Cane Toad invasion on freshwater fish communities remains one of the many information gaps surrounding the ecosystem effects of toad colonisation in Australia.

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 deter- minants of cane toad impact on native tadpoles.

Cloning and expression of candidate sexual development genes in the cane toad (Bufo marinus)

The development of the reproductive system in bufonids (true toads) is unique in several respects: sexual differentiation occurs later than in other anurans, and toads develop a Bidder's organ, a rudimentary ovary that can be manipulated in males to produce mature oocytes. To illuminate the genesis of this unusual reproductive system, we isolated from the cane toad (Bufo marinus) the orthologues of several known vertebrate sex-determining genes, determined their primary structure, and studied their expression by reverse transcriptase-polymerase chain reaction and in situ hybridization of tissue sections. We report here that cane toad Sox9, Dmrt1, and p450aromatase (Cyp19a1) are highly homologous to their counterparts in other vertebrates. They show profiles of expression that generally follow patterns observed in other taxa, but with some novel features. Our data suggest that these genes likely play key roles in sex determination and early gonad development in bufonids.

The evolution of growth rates on an expanding range edge

Individuals in the vanguard of a species invasion face altered selective conditions when compared with conspecifics behind the invasion front. Assortment by dispersal ability on the expanding front, for example, drives the evolution of increased dispersal, which, in turn, leads to accelerated rates of invasion. Here I propose an additional evolutionary mechanism to explain accelerating invasions: shifts in population growth rate (r). Because individuals in the vanguard face lower population density than those in established populations, they should (relative to individuals in established populations) experience greater r-selection. To test this possibility, I used the ongoing invasion of cane toads (Bufo marinus) across northern Australia. Life-history theory shows that the most efficient way to increase the rate of population growth is to reproduce earlier. Thus, I predict that toads on the invasion front will exhibit faster individual growth rates (and thus will reach breeding size earlier) than those from older populations. Using a common garden design, I show that this is indeed the case: both tadpoles and juvenile toads from frontal populations grow around 30 per cent faster than those from older, long established populations. These results support theoretical predictions that r increases during range advance and highlight the importance of understanding the evolution of life history during range advance.

Something different for dinner? Responses of a native Australian predator (the keelback snake) to an invasive prey species (the cane toad)

Predictions from foraging theory suggest that the probability a native predator will incorporate a novel type of prey (such as an invasive species) into its diet depends upon the potential benefits (e.g., nutrient input) vs. costs (e.g., handling time) of ingesting it. Cane toads (Bufo marinus) were introduced to Australia in 1935 and are highly toxic to many frog-eating snakes, thus there was strong selection to delete toads from the diet of these species. What has happened, however, to the feeding responses of an Australian snake species that is able to consume toads without dying? Our field surveys in northeastern Queensland show that, despite their high tolerance to toad toxins (compared to other native snakes), keelbacks (Tropidonophis mairii) feed primarily on native frogs rather than cane toads. This pattern occurs because the snakes show active prey preferences; even under standardized conditions in the laboratory, snakes are more likely to consume frogs than toads. When they are force-fed, snakes frequently regurgitate toads but not frogs. Thus, despite the high availability of the abundant toads, these invasive anurans are largely avoided as prey. This probably occurs because consumption of toads, although not lethal to keelbacks, causes significant sublethal effects and confers little nutritional benefit. Hence, keelback populations are not threatened by toad invasion, but neither do the snakes benefit substantially from the availability of a new type of potential prey.

Mechanical Properties of the Hindlimb Bones of Bullfrogs and Cane Toads in Bending and Torsion

When compared with most vertebrates, frogs use a novel style of jumping locomotion powered by the hindlimbs. Hindlimb bones of frogs must withstand the potentially erratic loads associated with such saltatory locomotion. To evaluate the load bearing capacity of anuran limb bones, we used three-point bending, torsion, and hardness tests to measure the mechanical properties of the femur and tibiofibula from adults of two species that use different jumping styles: explosively jumping bullfrogs (Rana (Lithobates) catesbeiana) and cyclically hopping cane toads (Bufo (Chaunus) marinus). Yield stress and strain values for R. catesbeiana and B. marinus hindlimb bones are within the range of values previously reported for other vertebrates. However, anuran hindlimb bones generally stand out as having higher yield stresses in bending than those of closely related, nonsaltatory salamanders, highlighting the importance of considering phylogenetic context in comparisons of bone functional capacity and adaptation. Stiffness values for both frog species tested were also high, which may facilitate efficient transmission of muscular forces while jumping. Elevated stiffness may also contribute to some discrepancies between determinations of bone properties via hardness versus bending tests. In comparisons between species, B. marinus bones showed significantly higher bending yield stresses than R. catesbeiana, whereas R. catesbeiana bones showed significantly higher torsional yield stresses than B. marinus. These differences may correlate with differences in jumping style and limb anatomy between ranid and bufonid frogs, suggesting that evolutionary changes in bone mechanical properties may help to accommodate new functional demands that emerge in lineages.