Invasive Toads Research Articles

Acute impacts of invasive toads on the population demography of a native predator in tropical Australia

If an animal’s size, age and/or sex influence its vulnerability to an invasive species, the arrival of such an invader can cause rapid changes in the population demography of an affected species. We studied free-ranging varanid lizards (Yellow-spotted monitors, Varanus panoptes) at a site in tropical Australia during the influx of fatally toxic cane toads, Rhinella marina. Mortality was inferred from shifts in population structure, as well as the survival rates (time to death) of 107 radio-tracked lizards. Of 57 deaths whose cause was unambiguous, 32 were due to fatal poisoning by ingesting a cane toad; the other 25 lizards were consumed by pythons. Size and age structure shifted between years, such that the population post-invasion was dominated by smaller, younger lizards, and by females rather than males. Radiotelemetric monitoring confirmed that survival rates were reduced more in males than in females in the post-toad year, with males most at risk late in the dry-season, when food was scarce and females were nesting rather than foraging. Pythons disproportionately consumed larger female lizards during the nesting season. Toad-induced poisoning of adult male varanids (which are larger and bolder than females) likely produced a population that was more resilient to toad impact, but less easily surveyed by conventional techniques.

Taste aversion training can educate free-ranging crocodiles against toxic invaders.

Apex predators play critical ecological roles, making their conservation a high priority. In tropical Australia, some populations of freshwater crocodiles (Crocodylus johnstoni) have plummeted by greater than 70% due to lethal ingestion of toxic invasive cane toads (Rhinella marina). Laboratory-based research has identified conditioned taste aversion (CTA) as a way to discourage consumption of toads. To translate those ideas into landscape-scale management, we deployed 2395 baits (toad carcasses with toxin removed and containing a nausea-inducing chemical) across four gorge systems in north-western Australia and monitored bait uptake with remote cameras. Crocodile abundance was quantified with surveys. Free-ranging crocodiles rapidly learned to avoid toad baits but continued to consume control (chicken) baits. Toad invasion at our sites was followed by high rates of crocodile mortality (especially for small individuals) at a control site but not at nearby treatment sites. In areas with high connectivity to other waterbodies, repeated baiting over successive years had continuing positive impacts on crocodile survival. In summary, we succeeded in buffering the often-catastrophic impact of invasive cane toads on apex predators.

Spatial variation in genomic signatures of local adaptation during the cane toad invasion of Australia.

Adaptive evolution can facilitate species' range expansions across environmentally heterogeneous landscapes. However, serial founder effects can limit the efficacy of selection, and the evolution of increased dispersal during range expansions may result in gene flow swamping local adaptation. Here, we study how genetic drift, gene flow and selection interact during the cane toad's (Rhinella marina) invasion across the heterogeneous landscape of Australia. Following its introduction in 1935, the cane toad colonised eastern Australia and established several stable range edges. The ongoing, more rapid range expansion in north-central Australia has occurred concomitant with an evolved increase in dispersal capacity. Using reduced representation genomic data of Australian cane toads from the expansion front and from two areas of their established range, we test the hypothesis that high gene flow constrains local adaptation at the expansion front relative to established areas. Genetic analyses indicate the three study areas are genetically distinct but show similar levels of allelic richness, heterozygosity and inbreeding. Markedly higher gene flow or recency of colonisation at the expansion front have likely hindered local adaptation at the time of sampling, as indicated by reduced slopes of genetic-environment associations (GEAs) estimated using a novel application of geographically weighted regression that accounts for allele surfing; GEA slopes are significantly steeper in established parts of the range. Our work bolsters evidence supporting adaptation of invasive species post-introduction and adds novel evidence for differing strengths of evolutionary forces among geographic areas with different invasion histories.

Physiological and behavioral responses to novel saline conditions in an invasive treefrog.

Salinity can be an environmental stressor for anurans, as their highly permeable skin makes them prone to osmotic stress when exposed to saline conditions. However, certain anuran species have colonized areas near saltwater habitats, suggesting an ability to acclimate to saline conditions. Here, we evaluated physiological and behavioral responses to saline conditions in adult Cuban treefrogs (Osteopilus septentrionalis), an invasive anuran found throughout Florida. To examine their response to salinity, adult frogs were maintained in two treatments simulating a freshwater (0.5 ppt) or brackish (8.0 ppt) environment for 6 weeks. To assess their physiological response to this potential stressor, all frogs were submerged in a brackish solution to quantify individual weight change every 2 weeks. We found that frogs maintained in brackish solution lost more weight at Weeks 2 and 6 when compared to Week 0, suggesting that salinity may be an environmental stressor for Cuban treefrogs. Yet, the weight change at Week 4 was similar to the pre-exposure period, which may indicate that constant exposure to salinity may alter their physiological response to saline conditions. To supplement the physiological analyses, we investigated avoidance behavior towardsaline conditions by offering individuals a choice between freshwater or brackish environments. Our results showed that Cuban treefrogs chose freshwater environments more frequently and may thus avoid saline ones. This study reveals that salinity may induce plastic and avoidance responses in Cuban treefrogs, potentially allowing them to expand their range into areas typically stressful for most anurans.

Neural and sensory basis of homing behavior in the invasive cane toad, Rhinella marina.

The behavioral, sensory, and neural bases of vertebrate navigation are primarily described in mammals and birds. However, we know much less about navigational abilities and mechanisms of vertebrates that move on smaller scales, such as amphibians. To address this knowledge gap, we conducted an extensive field study on navigation in the cane toad, Rhinella marina. First, we performed a translocation experiment to describe how invasive toads in Hawai'i navigate home following displacements of up to one kilometer. Next, we tested the effect of olfactory and magnetosensory manipulations on homing, as these senses are most commonly associated with amphibian navigation. We found that neither ablation alone prevents homing, suggesting that toad navigation is multimodal. Finally, we tested the hypothesis that the medial pallium, the amphibian homolog to the hippocampus, is involved in homing. By comparing neural activity across homing and non-homing toads, we found evidence supporting the involvement of the medial pallium, lateral pallium, and septum in navigation, suggesting a conservation of neural structures supporting navigation across vertebrates. Our study lays the foundation to understand the behavioral, sensory, and neural bases of navigation in amphibians and to further characterize the evolution of behavior and neural structures in vertebrates.

Femoral bone structure and mechanics at the edge and core of an expanding population of the invasive frog Xenopus laevis.

Understanding how living tissues respond to changes in their mechanical environment is a key question in evolutionary biology. Invasive species provide an ideal model for this as they are often transplanted between environments that differ drastically in their ecological and environmental context. Spatial sorting, the name given to the phenomenon driving differences between individuals at the core and edge of an expanding range, has been demonstrated to impact the morphology and physiology of Xenopus laevis from the invasive French population. Here, we combined a structural analysis using micro-CT scanning and a functional analysis by testing the mechanical properties of the femur to test whether the increased dispersal at the range edge drives differences in bone morphology and function. Our results show significant differences in the inner structure of the femur as well as bone material properties, with frogs from the centre of the range having more robust and resistant bones. This is suggestive of an energy allocation trade-off between locomotion and investment in bone formation, or alternatively, may point to selection for fast locomotion at the range edge. Overall, our results provide insights on the growth of the long bones and the formation of trabecular bone in frogs.

Defenses of whirligig beetles against native and invasive frogs.

Many native insects have evolved defenses against native predators. However, their defenses may not protect them from non-native predators due to a limited shared history. The American bullfrog, Aquarana catesbeiana (Anura: Ranidae), which has been intentionally introduced to many countries, is believed to impact native aquatic animals through direct predation. Adults of whirligig beetles (Coleoptera: Gyrinidae), known for swimming and foraging on the water surface of ponds and streams, reportedly possess chemical defenses against aquatic predators, such as fish. Although whirligig beetles potentially encounter both bullfrogs and other frogs in ponds and lakes, the effectiveness of their defenses against frogs has been rarely studied. To assess whether whirligig beetles can defend against native and non-native frogs, we observed the behavioral responses of the native pond frog, Pelophylax nigromaculatus (Anura: Ranidae), and the invasive non-native bullfrog, A. catesbeiana, to native whirligig beetles, Gyrinus japonicus and Dineutus orientalis, in Japan. Adults of whirligig beetles were provided to frogs under laboratory conditions. Forty percent of G. japonicus and D.orientalis were rejected by P. nigromaculatus, while all whirligig beetles were easily consumed by A. catesbeiana. Chemical and other secondary defenses of G. japonicus and D. orientalis were effective for some individuals of P. nigromaculatus but not for any individuals of A. catesbeiana. These results suggest that native whirligig beetles suffer predation by invasive non-native bullfrogs in local ponds and lakes in Japan.

Teacher toads: Buffering apex predators from toxic invaders in a remote tropical landscape

AbstractEven after research identifies new approaches for wildlife management, translating those methods for delivery can be logistically challenging. In tropical Australia, invasive cane toads (Rhinella marina) fatally poison many anuran‐eating native predators. Small‐scale trials show that vulnerable predators exposed to small (nonlethal) toads can learn to delete toads from their diets, increasing survival of those predators after toads invade. We deployed this method in the remote Kimberley region of tropical Australia, with >200,000 eggs, tadpoles, or metamorph toads released in advance of the expanding toad invasion front. Remote camera surveys before and after “teacher toad” deployment showed that large monitor lizards (Varanus panoptes) were almost extirpated from control plots but remained abundant in treatment plots, indicating broad‐scale success of this novel intervention.

Imperfect adaptation by freshwater crocodiles to the invasion of a toxic prey species

Novel interactions between invaders and native species that have evolved in their absence may impose strong selective pressures that drive species to extinction or prompt rapid co-evolution and learning. Here, we report on the effects that invasive cane toads, a toxic prey species, have had on freshwater crocodile populations in 7 waterholes of the Victoria River, Australia, before and up to 14 years after toads invaded. We recorded observations of crocodiles attacking toads, dissected dead crocodiles to determine if they had eaten toads and indexed the abundances of cane toads, live crocodiles and dead crocodiles. Following toad-invasion we observed crocodiles attacking cane toads. Dead crocodiles were only observed following the invasion of toads and 62% of the 71 dead crocodiles we dissected had toads in their stomachs. Counts of dead crocodiles showed a humped relationship with time since toad invasion and declined markedly after 3 years post-toad invasion. Live crocodile abundance declined sharply following toad-invasion, but this decline attenuated approximately 4 years post-invasion. The pulse of crocodile mortality and attenuation of the rate of crocodile population decline suggests that crocodiles have evolved or learned to enable co-existence with toads. However, crocodile populations have shown no sign of recovery in the 8–14 years post toad invasion. Our findings highlight that adaptation by native species to the presence of invaders may be imperfect and thus may not necessarily entail numerical recovery of populations to pre-invasion levels, but instead downward shifts to new equilibria due to ongoing interactions with invaders.

Invading new climates at what cost? Ontogenetic differences in the thermal dependence of metabolic rate in an invasive amphibian

Global warming can either promote or constrain the invasive potential of alien species. In ectotherm invaders that exhibit a complex life cycle, success is inherently dependent on the capacity of each developmental stage to cope with environmental change. This is particularly relevant for invasive anurans, which disperse on land while requiring water for reproduction. However, it remains unknown how the different life stages respond in terms of energy expenditure under different climate change scenarios. We here quantified the oxygen uptake of frogs at rest (a proxy of the standard metabolic rate) in the aquatic phase (at the tadpole and climax, i.e. during metamorphosis, stages) and in the terrestrial phase (metamorphosed stage) at three environmental temperatures. To do so, we used marsh frogs (Pelophylax ridibundus), an amphibian with the largest invasive range within the palearctic realm and for which their adaptation to global warming might be key to their invasion success. Beyond an increase of metabolic rate with temperature, our data show variation in thermal adaptation across life stages and a higher metabolic cost during metamorphosis. These results suggest that the cost to shift habitat and face changes in temperature may be a constraint on the invasive potential of species with a complex life cycle which may be particularly vulnerable during metamorphosis.

The first intermediate host of the invasive frog trematode Glypthelmins quieta in Japan.

Glypthelmins quieta is a frog trematode native to North and Central America. This trematode was recently detected in Japan in the American bullfrog Lithobates catesbeianus, which was introduced from North America to Japan. As the first intermediate host of G. quieta, typically a snail, has not yet been identified in Japan, we conducted a snail survey in eastern Japan to screen for an intermediate host using DNA barcoding based on the nuclear 28S ribosomal RNA and mitochondrial cytochrome c oxidase subunit 1. We sampled 3 different snail species, Orientogalba ollula, Physella acuta, and Sinotaia quadrata histrica (157 individuals in total), and only the freshwater snail Physella acuta, which is also believed to have been introduced from North America to Japan, had sporocysts of G. quieta in its hepatopancreas. The introduction of the intermediate and definitive hosts from North America may have facilitated the invasion of G. quieta into Japan.

Effects of Invasive Toad Calls and Synthetic Tones on Call Properties of Native Australian Toadlets

Effects of Invasive Toad Calls and Synthetic Tones on Call Properties of Native Australian Toadlets

Establishment and Occurrence History of Three Invasive Anuran Species Across the Florida Peninsula

Establishment and Occurrence History of Three Invasive Anuran Species Across the Florida Peninsula

What makes a great invader? Anatomical traits as predictors of locomotor performance and metabolic rate in an invasive frog.

Invasive species are characterized by their ability to establish and spread in a new environment. In alien populations of anurans, dispersal and fitness-related traits such as endurance, burst performance and metabolism are key to their success. However, few studies have investigated inter-individual variation in these traits and more specifically have attempted to understand the drivers of variation in these traits. Associations of anatomical features may be excellent predictors of variation in performance and could be targets for selection or subject to trade-offs during invasions. In this study, we used marsh frogs (Pelophylax ridibundus), a species that has been introduced in many places outside its native range and which is now colonizing large areas of Western Europe. We first measured the inter-individual variation in resting metabolism, the time and distance they were able to jump until exhaustion, and their peak jump force, and then measured the mass of specific organs and lengths of body parts suspected to play a role in locomotion and metabolism. Among the 5000 bootstrap replicates on body size-corrected variables, our statistical models most often selected the stomach (75.42%), gonads (71.46%) and the kidneys (67.26%) as predictors of inter-individual variation in metabolism, and the gluteus maximus muscle (97.24%) mass was the most frequently selected predictor of jump force. However, endurance was poorly associated with the anatomical traits (R2distance=0.42, R2time=0.37). These findings suggest that selection on these predictors may lead to physiological changes that may affect the colonization, establishment and dispersal of these frogs.

Parasitic helminths of alien invasive anurans in Butuan City, Northeastern Mindanao, Philippines.

This study aimed to identify the helminth parasites of invasive anuran species in selected barangays in Butuan City, Philippines. In urbanized areas, invasive species dominate anuran diversity, and one of the primary threats they pose to native wildlife is the transmission of diseases and parasites. Out of the 91 collected individuals of invasive anuran species, Rhinella marina was the most abundant (88 %), followed by Hoplobatrachus rugulosus (12 %) and Kaloula pulchra (3 %). The study identified five species of parasites, with Spirometra sp. being the most prevalent (17.58 %), followed by Echinostoma sp. (16.5 %), Rhabdias bufonis (14.3 %), Cosmocerca sp. (6.6 %), and Strongyloides stercoralis (3.30 %), respectively. Spirometra sp. also had the highest intensity (7.67), followed by Cosmocerca sp. (5), Strongyloides stercoralis (3.33), Rhabdias bufonis (3.30), and Echinostoma sp. (2.73). This parasitological survey revealed that H. rugulosus had the highest prevalence and infection of parasites, and residential areas had the highest parasite prevalence among the habitat types. Adult hosts were found to harbor a higher prevalence and intensity, and male hosts had a higher prevalence. The results highlight the high risk of parasite transmission from anurans to other animals and emphasize the need for the community to control the population of invasive anuran species for the safety of native anurans and to prevent zoonotic transmission to other animals and humans.

DO Toxic Invasive Prey Become a Toxin Source for Native Consumers?

Toxic organisms can become food that potentially harms consumers. When these organisms become invasive species, the harm often turns to a serious threat that disrupts native ecosystems. On the other hand, there are consumers that can exploit toxic organisms for food and sequester intact toxins from them for the consumers' own chemical defense. Therefore, it can be expected that toxic invasive prey can become a toxin source for native consumers. Here, we focused on the relationship between toads, which are one of the major toxic invasive organisms and possess bufadienolides (BDs), and Rhabdophis snakes, which sequester BDs from toads. On Sado Island, Japan, R. tigrinus is native, but no toads had inhabited this island until Bufo japonicus formosus was introduced as a domestic invasive species in 1963 and 1964. At present, invasive toads are distributed only in the southwestern part of the island. We collected a total of 25 and 24 R. tigrinus from areas allopatric and sympatric with toads, respectively. Then, we investigated the possession of BDs and the BD profile of these snakes. We found that only R. tigrinus sympatric with toads possessed BDs, whereas all snakes allopatric with toads lacked BDs. Based on the characteristics of the BD profile, the toxin source was identified as B. j. formosus. Our findings show that a new case of impact caused by toxic invasive species, i.e., "toxin supply to native consumers from invasive prey", could occur.

Rapidly evolved traits enable new conservation tools: perspectives from the cane toad invasion of Australia.

Natural populations can show rapid adaptive responses to intense (human-mediated) environmental change. The potential for exploiting rapidly evolved traits for conservation management has been often discussed but rarely implemented. Capitalizing on a well-studied biological invasion, we here explore the idea that rapid phenotypic change in the invaders, their pathogens, and the native biota provide opportunities for managers to control invader abundance and buffer adverse impacts on native wildlife. Intensive studies of the invasion of tropical Australia by cane toads (Rhinella marina) have identified newly evolved vulnerabilities that we could exploit for toad control; and newly evolved resilience of native wildlife that we could exploit for impact reduction. For example, distinctive phenotypes of toads at the expanding range edge enhance dispersal rate but reduce reproductive output, intraspecific competitive ability, and immunocompetence; and the evolution of larval cannibalism creates opportunities not only for species-specific trapping of toad tadpoles, but also could be exploited (when allied to emerging CRISPR-Cas9 techniques) to intensify intraspecific conflict in invasive toads. That is, we could use the invasive species to control their own populations. This case study illustrates the potential of detailed basic research to identify novel approaches for conservation.

Invasive frogs show persistent physiological differences to elevation and acclimate to colder temperatures

The coqui frog (Eleutherodactylus coqui) was introduced to the island of Hawai'i in the 1980s and has spread across much of the island. Concern remains that this frog will continue to expand its range and invade higher elevation habitats where much of the island's endemic species are found. We determined whether coqui thermal tolerance and physiology change along Hawai'i’s elevational gradients. We measured physiological responses using a short-term experiment to determine baseline tolerance and physiology by elevation, and a long-term experiment to determine the coqui's ability to acclimate to different temperatures. We collected frogs from low, medium, and high elevations. After both the short and long-term experiments, we measured critical thermal minimum (CTmin), blood glucose, oxidative stress, and corticosterone levels. CTmin was lower in high elevation frogs than low elevation frogs after the short acclimation experiment, signifying that they acclimate to local conditions. After the extended acclimation, CTmin was lower in frogs acclimated to cold temperatures compared to warm-acclimated frogs and no longer varied by elevation. Blood glucose levels were positively correlated with elevation even after the extended acclimation, suggesting glucose may also be related to lower temperatures. Oxidative stress was higher in females than males, and corticosterone was not significantly related to any predictor variables. The extended acclimation experiment showed that coquis can adjust their thermal tolerance to different temperatures over a 3-week period, suggesting the expansion of coqui into higher elevation habitats may still be possible, and they may not be as restricted by cold temperatures as previously thought.

Spatial ecology of the invasive Asian common toad in Madagascar and its implications for invasion dynamics

Invasion dynamics are determined, among other aspects, by the spatial behaviour of invasive populations. The invasive toad Duttaphrynus melanostictus is spreading inland from the eastern coast of Madagascar, causing considerable ecological impacts. Understanding the basic factors determining the spread dynamics can inform management strategies and provide insights into spatial evolutionary processes. We radio-tracked 91 adult toads in three localities along the invasion gradient to determine whether spatial sorting of dispersive phenotypes is occurring, and investigate intrinsic and extrinsic determinants of spatial behaviour. Overall, toads in our study appeared as habitat generalists, and their sheltering behaviour was tied to water proximity, with toads changing shelter more frequently closer to waterbodies. Toads showed low displacement rates (mean = 4.12 m/day) and quite a philopatric behaviour but were able to perform daily movements of over 50 m. We did not detect any spatial sorting of dispersal-relevant traits nor sex- or size-biased dispersal. Our results suggest that toads are more likely to expand their range during the wet season, and that the range expansion is probably dominated by short-distance dispersal at this stage of the invasion, although a future increase in invasion speed is expected, due to the capacity for long-distance movements of this species.

Can conditioned taste aversion be deployed at a landscape level to mitigate the impact of invasive cane toads on northern quolls?

Context Animals can be taught new behaviours to mitigate threatening processes. However, it is yet to be confirmed if such teaching can be deployed in the field. Here we test this possibility using the invasion of cane toads because they are highly toxic novel prey items to many predators across northern Australia. Aims Research has shown that training predators to avoid toads, using conditioned taste aversion (CTA), significantly improves the survival rates of individuals. We sought to determine if deployment of CTA baits, in situ, could reduce cane toad impacts on a mammalian predator, the northern quoll (Dasyurus hallucatus). Methods The work was conducted in the Kimberley, Western Australia, where we treated three quoll populations with training baits from November 2015–November 2017, and kept four populations as controls. We used camera traps and Bayesian hierarchal modelling to estimate the population size of quolls on up to four occasions before, and two occasions after, cane toad arrival. Key results We observed a 65% reduction in quoll population size at control sites and a 94% reduction at treatment sites: a significant effect of aversion training, but in the direction opposite to that expected. Conclusions Two complexities – decay of aversion, and individual variation – together, may explain our result. Our trials indicate that most animals are no longer averse within 120 days post-training. Earlier studies indicating that aversion training lasts longer may have inadvertently observed innate (i.e. genetically based) aversion to cane toads. Another possibility is that our dose rate of thiabendazole within the CTA baits was, in fact, too low; or the result may be an artefact of the non-random assignment of treatment and control groups. Ultimately, there is no way of determining exactly why our outcome occurred without further laboratory/captive trails. Regardless, our study demonstrates a failure of CTA training to mitigate the impact of cane toads on northern quolls in this system. Implications Our result calls into question the value of this approach for conserving quoll populations, at least in its current form. More generally, our results point to the often-unexpected complexities encountered as ideas progress from captive trials to field deployment.