Assessing the Potential Impact of Cane Toads on Australian Snakes

Abstract:   Cane toads ( Bufo marinus ) are large, highly toxic anurans that were introduced into Australia in 1937. Anecdotal reports suggest that the invasion of toads into an area is followed by dramatic declines in the abundance of terrestrial native frog-eating predators, but quantitative studies have been restricted to nonpredator taxa or aquatic predators and have generally reported minimal impacts. Will toads substantially affect Australian snakes? Based on geographic distributions and dietary composition, we identified 49 snake taxa as potentially at risk from toads. The impact of these feral prey also depends on the snakes' ability to survive after ingesting toad toxins. Based on decrements in locomotor (swimming) performance after ingesting toxin, we estimate the LD₅₀ of toad toxins for 10 of the at-risk snake species. Most species exhibited a similar low ability to tolerate toad toxins. Based on head widths relative to sizes of toads, we calculate that 7 of the 10 taxa could easily ingest a fatal dose of toxin in a single meal. The exceptions were two colubrid taxa (keelbacks [  Tropidonophis mairii ] and slatey-grey snakes [  Stegonotus cucullatus ]) with much higher resistance to toad toxins (up to 85-fold) and one elapid (swamp snakes [  Hemiaspis signata ]) with low resistance but a small relative head size and thus low maximum prey size. Overall, our analysis suggests that cane toads threaten populations of approximately 30% of terrestrial Australian snake species.     

The ecological impact of invasive cane toads on tropical snakes: field data do not support laboratory-based predictions

Predicting which species will be affected by an invasive taxon is critical to developing conservation priorities, but this is a difficult task. A previous study on the impact of invasive cane toads (Bufo marinus) on Australian snakes attempted to predict vulnerability a priori based on the assumptions that any snake species that eats frogs, and is vulnerable to toad toxins, may be at risk from the toad invasion. We used time-series analyses to evaluate the accuracy of that prediction, based on >3600 standardized nocturnal surveys over a 138-month period on 12 species of snakes and lizards on a floodplain in the Australian wet-dry tropics, bracketing the arrival of cane toads at this site. Contrary to prediction, encounter rates with most species were unaffected by toad arrival, and some taxa predicted to be vulnerable to toads increased rather than declined (e.g., death adder Acanthophis praelongus; Children's python Antaresia childreni). Indirect positive effects of toad invasion (perhaps mediated by toad-induced mortality of predatory varanid lizards) and stochastic weather events outweighed effects of toad invasion for most snake species. Our study casts doubt on the ability of a priori desktop studies, or short-term field surveys, to predict or document the ecological impact of invasive species.     

The behavioral ecology of cannibalism in cane toads (<Emphasis Type="Italic">Bufo marinus</Emphasis>)

Laboratory studies show that predatory cane toads (Bufo marinus) exhibit specialized toe-luring behavior that attracts smaller conspecifics, but field surveys of toad diet rarely record cannibalism. Our data resolve this paradox, showing that cannibalism is common under specific ecological conditions. In the wet–dry tropics of Australia, desiccation risk constrains recently metamorphosed toads to the edges of the natal pond. Juvenile toads large enough to consume their smaller conspecifics switch to a primarily cannibalistic diet (67% of prey biomass in stomachs of larger toads). Cannibalistic attack was triggered by prey movement, and (perhaps as an adaptive response to this threat) small (edible-sized) toads were virtually immobile at night (when cannibals were active). Smaller metamorphs were consumed more frequently than were larger conspecifics. The switch from insectivory to cannibalism reflects the high dry season densities of small conspecifics (in turn, due to desiccation-imposed constraints to dispersal) and the scarcity of alternative (insect) prey during dry weather. Our study pond (102 m in circumference) supported >400 juvenile toads, which consumed many metamorphs over the course of our study. Toads appear to be low-quality food items for other toads; in laboratory trials, juvenile toads that fed only on conspecifics grew less rapidly than those that ate an equivalent mass of insects. This effect was not due to parotoid gland toxins per se. Thus, cane toads switch to intensive cannibalism only when seasonal precipitation regimes increase encounter rates between large and small toads, while simultaneously reducing the availability of alternative prey.     

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.     

Ecological and Economic Services Provided by Birds on Jamaican Blue Mountain Coffee Farms

Abstract: Coffee farms can support significant biodiversity, yet intensification of farming practices is degrading agricultural habitats and compromising ecosystem services such as biological pest control. The coffee berry borer (Hypothenemus hampei) is the world's primary coffee pest. Researchers have demonstrated that birds reduce insect abundance on coffee farms but have not documented avian control of the berry borer or quantified avian benefits to crop yield or farm income. We conducted a bird‐exclosure experiment on coffee farms in the Blue Mountains, Jamaica, to measure avian pest control of berry borers, identify potential predator species, associate predator abundance and borer reductions with vegetation complexity, and quantify resulting increases in coffee yield. Coffee plants excluded from foraging birds had significantly higher borer infestation, more borer broods, and greater berry damage than control plants. We identified 17 potential predator species (73% were wintering Neotropical migrants), and 3 primary species composed 67% of migrant detections. Average relative bird abundance and diversity and relative resident predator abundance increased with greater shade‐tree cover. Although migrant predators overall did not respond to vegetation complexity variables, the 3 primary species increased with proximity to noncoffee habitat patches. Lower infestation on control plants was correlated with higher total bird abundance, but not with predator abundance or vegetation complexity. Infestation of fruit was 1–14% lower on control plants, resulting in a greater quantity of saleable fruits that had a market value of US$44–$105/ha in 2005/2006. Landscape heterogeneity in this region may allow mobile predators to provide pest control broadly, despite localized farming intensities. These results provide the first evidence that birds control coffee berry borers and thus increase coffee yield and farm income, a potentially important conservation incentive for producers.     

Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies

Chemical defenses are widespread among animals, and the compounds involved may be either synthesized from nontoxic precursors or sequestered from an environmental source. Defensive sequestration has been studied extensively among invertebrates, but relatively few examples have been documented among vertebrates. Nonetheless, the number of described cases of defensive sequestration in tetrapod vertebrates has increased recently and includes diverse lineages of amphibians and reptiles (including birds). The best-known examples involve poison frogs, but other examples include natricine snakes that sequester toxins from amphibians and two genera of insectivorous birds. Commonalities among these diverse taxa include the combination of consuming toxic prey and exhibiting some form of passive defense, such as aposematism, mimicry, or presumptive death-feigning. Some species exhibit passive sequestration, in which dietary toxins simply require an extended period of time to clear from the tissues, whereas other taxa exhibit morphological or physiological specializations that enhance the uptake, storage, and/or delivery of exogenous toxins. It remains uncertain whether any sequestered toxins of tetrapods bioaccumulate across multiple trophic levels, but multitrophic accumulation seems especially likely in cases involving consumption of phytophagous or mycophagous invertebrates and perhaps consumption of poison frogs by snakes. We predict that additional examples of defensive toxin sequestration in amphibians and reptiles will be revealed by collaborations between field biologists and natural product chemists. Candidates for future investigation include specialized predators on mites, social insects, slugs, and toxic amphibians. Comprehensive studies of the ecological, evolutionary, behavioral, and regulatory aspects of sequestration will require teams of ecologists, systematists, ethologists, physiologists, molecular biologists, and chemists. The widespread occurrence of sequestered defenses has important implications for the ecology, evolution, and conservation of amphibians and reptiles.     

Foraging tactics of an ambush predator: the effects of substrate attributes on prey availability and predator feeding success

The foraging sites selected by an ambush forager can strongly affect its feeding opportunities. Foraging cane toads (Rhinella marina) typically select open areas, often under artificial lights that attract insects. We conducted experimental trials in the field, using rubber mats placed under lights, to explore the influence of substrate color and rugosity on prey availability (numbers, sizes, and types of insects) and toad foraging success. A mat's color (black vs. white) and rugosity (smooth vs. rough) did not influence the numbers, sizes, or kinds of insects that were attracted to it, but toads actively preferred to feed on rugose white mats (50% of prey-capture events, vs. a null of 25%). White backgrounds provided better visual contrast of the (mostly dark) insects, and manipulations of prey color in the laboratory showed that contrast was critical in toad foraging success. Insects landing on rugose backgrounds were slower to leave, again increasing capture opportunities for toads. Thus, cane toads actively select backgrounds that maximize prey-capture opportunities, a bias driven by the ways that substrate attributes influence ease of prey detection and capture rather than by absolute prey densities.     

Vivid birds respond more to acoustic signals of predators

Because conspicuous morphology such as colorful plumage may increase predation risk, we aimed to see if variation in plumage coloration could explain variation in avian anti-predator behavior. We included several measures of plumage coloration: human perception of vividness from images in field guides, total intensity from reflectance spectra of museum skins, contrasts calculated from physiological models of these spectra parameterized for both raptors and humans, chroma, and spectral saturation. We investigated how well these measurements predicted risk assessment in ten species of birds in St. John, U.S. Virgin Islands. We quantified how each species responded to playbacks of a predator’s calls and compared this response to that elicited by songs from a non-predatory, sympatric bird. We found that human-determined measures of vividness best predicted anti-predator responses of birds—more vividly colored species responded more to predators than duller species. No spectrophotometric variable explained variation in species reactions to a predator call. Our results suggest that vivid birds may compensate for their conspicuousness by being more responsive to the sound of predators and that more work is needed to better evaluate how animal coloration is quantified in comparative studies.     

Amphibian myiasis. Blowfly larvae (Lucilia bufonivora,Diptera: Calliphoridae) coping with the poisonous skin secretion of the common toad (Bufo bufo)

The blowfly Lucilia bufonivora shows high host specificity for toads despite the host’s toxic skin secretion, which consists mainly of bufadienolides. These toxins are effective blockers of the Na⁺, K⁺-ATPase, an enzyme that is essential for many physiological processes in animals. Whereas common toad (Bufo bufo) toxins were identified in the larvae of the fly, few toxins were found in the pupae and empty puparia as trace amounts, while adult flies were entirely free of these toxic compounds. Similar results were obtained when larvae of generalist necrophagous blowflies (L. sericata, Calliphora vicina) fed on toad carcasses. Analysis of the Na⁺, K⁺-ATPase gene revealed no amino acid substitution at positions known to mediate resistance to bufadienolides in other systems. Alternative mechanisms of resistance such as efficient excretion of the compounds may enable the flies to use this poisonous food source.     

Consistent Ecological Selectivity through Time in Pacific Island Avian Extinctions

Abstract: Understanding the ecological mechanisms that lead to extinction is a central goal of conservation. Can understanding ancient avian extinctions help to predict extinction risk in modern birds? I used classification trees trained on both paleoecological and historical data from islands across the Pacific to determine the ecological traits associated with extinction risk. Intrinsic traits, including endemism, large body size, and certain feeding guilds, were tightly linked with avian extinction over the past 3500 years. Species ecology and phylogeny were better predictors of extinction risk through time than extrinsic or abiotic factors. Although human impacts on birds and their habitats have changed over time, modern endangered birds share many of the same ecological characteristics as victims of previous extinction waves. My use of detailed predictions of extinction risk to identify species potentially in need of conservation attention demonstrates the utility of paleoecological knowledge for modern conservation biology.     

Landscape constraints on functional diversity of birds and insects in tropical agroecosystems

In this paper, we analyzeatabases on birds and insects to assess patterns of functional diversity in human-dominated landscapes in the tropics. A perspective from developed landscapes is essential for understanding remnant natural ecosystems, because most species experience their surroundings at spatial scales beyond the plot level, and spillover between natural and managed ecosystems is common. Agricultural bird species have greater habitat and diet breadth than forest species. Based on a global data base, bird assemblages in tropical agroforest ecosystems were composed of disproportionately more frugivorous and nectarivorous, but fewer insectivorous bird species compared with forest. Similarly, insect predators of plant-feeding arthropods were more diverse in Ecuadorian agroforest and forest compared with rice and pasture, while, in Indonesia, bee diversity was also higher in forested habitats. Hence, diversity of insectivorous birds and insect predators as well as bee pollinators declined with agricultural transformation. In contrast, with increasing agricultural intensification, avian pollinators and seed dispersers initially increase then decrease in proportion. It is well established that the proximity of agricultural habitats to forests has a strong influence on the functional diversity of agroecosystems. Community similarity is higher among agricultural systems than in natural habitats and higher in simple than in complex landscapes for both birds and insects, so natural communities, low-intensity agriculture, and heterogeneous landscapes appear to be critical in the preservation of beta diversity. We require a better understanding of the relative role of landscape composition and the spatial configuration of landscape elements in affecting spillover of functionally important species across managed and natural habitats. This is important for data-based management of tropical human-dominated landscapes sustaining the capacity of communities to reorganize after disturbance and to ensure ecological functioning.     

Absence of Blood Parasites in Indigenous and Introduced Birds from the Cook Islands, South Pacific

Abstract: We found no protozoan parasites in 79 blood smears of birds from the Cook Islands, South Pacific. Our sample consisted of 55 smears from nine indigenous species of land and aquatic birds, and 24 smears from one introduced land bird The absence or scarcity of avian hematozoa in the Cook Islands is probably due to a very low prevalence of infection among introduced and naturally colonizing species of birds, rather than a scarcity of insect vectors. On one hand, the apparent absence or extreme scarcity of avian hematozoa, particularly the malaria-causing Plasmodium spp., is fortunate from a conservation standpoint, considering the devastating impact that Plasmodium from human-introduced mosquitoes and birds has had on the indigenous avifauna of Hawaii during the past century. On the other hand, our results suggest that the indigenous birds of the Cook Islands, much like those of Hawaii, would have little natural resistance to avian malaria should it be introduced. Thus precautions should be taken to prohibit the introduction of potentially infected nonnative birds or mosquitoes in the Cook Islands and elsewhere in Polynesia     

Responses of Seed‐Dispersing Birds to Amount of Rainforest in the Landscape around Fragments

Habitat loss and fragmentation alter the composition of bird assemblages in rainforest. Because birds are major seed dispersers in rainforests, fragmentation‐induced changes to frugivorous bird assemblages are also likely to alter the ecological processes of seed dispersal and forest regeneration, but the specific nature of these changes is poorly understood. We assessed the influence of fragment size and landscape forest cover on the abundance, species composition, and functional properties of the avian seed disperser community in an extensively cleared, former rainforest landscape of subtropical Australia. Bird surveys of fixed time and area in 25 rainforest fragments (1–139 ha in size across a 1800 km² region) provided bird assemblage data which were coupled with prior knowledge of bird species’ particular roles in seed dispersal to give measurements of seven different attributes of the seed disperser assemblage. We used multimodel regression to assess how patch size and surrounding forest cover (within 200 m, 1000 m, and 5000 m radii) influenced variation in the abundance of individual bird species and of functional groups based on bird species’ responses to fragmentation and their roles in seed dispersal. Surrounding forest cover, specifically rainforest cover, generally had a greater effect on frugivorous bird assemblages than fragment size. Amount of rainforest cover within 200 m of fragments was the main factor positively associated with abundances of frugivorous birds that are both fragmentation sensitive and important seed dispersers. Our results suggest a high proportion of local rainforest cover is required for the persistence of seed‐dispersing birds and the maintenance of seed dispersal processes. Thus, even small rainforest fragments can function as important parts of habitat networks for seed‐dispersing birds, whether or not they are physically connected by vegetation. Respuestas de Aves Dispersoras de Semillas al Incremento de Selvas en el Paisaje Alrededor de Fragmentos     

To flee or not to flee: predator avoidance by cheetahs at kills

Mammalian carnivores are unusual because their primary competitors for food are often their primary predators. This relationship is most evident at persistent kills where dominant competitors are attracted to both the carcass (as a free meal) and to the killers (as potential prey). Cheetahs (Acinonyx jubatus) are frequent victims of kleptoparasitism, and cubs, and sometimes adults, are killed by lions (Panthera leo) or spotted hyenas (Crocuta crocuta). Between 1980 and 2002, we observed 639 kills made by cheetahs in Serengeti National Park, Tanzania. These kills were often visited by scavengers, including relatively innocuous species such as vultures and jackals and potentially dangerous species, like spotted hyenas and lions. We used cheetah behavior at kills to test a number of predictions about how cheetahs should minimize risk at kill sites given they face an increased risk of predation of themselves or their cubs. In particular, we examined the propensity of cheetahs of different age/sex classes to hide carcasses after making a kill, vigilance at kills, and the delay in leaving after finishing feeding with respect to ecological factors and scavenger presence. The behavior of single females at kills did not suggest that they were trying to avoid being killed, but the behavior of males, often found in groups, was in line with this hypothesis. In contrast, the behavior of mother cheetahs at kills appeared to be influenced greatly by the risk of cubs being killed. Our results suggest that cheetahs use several behavioral counterstrategies to avoid interspecific predation of self or cubs.     

Ecosystem-based management of predator-prey relationships: piscivorous birds and salmonids.

Predator-prey relationships are often altered as a result of human activities. Where prey are legally protected, conservation action may include lethal predator control. In the Columbia River basin (Pacific Northwest, USA and Canada), piscivorous predators have been implicated in contributing to a lack of recovery of several endangered anadromous salmonids (Oncorhynchus spp.), and lethal and nonlethal control programs have been instituted against both piscine and avian species. To determine the consequences of avian predation, we used a bioenergetics approach to estimate the consumption of salmonid smolts by waterbirds (Common Merganser, California and Ring-billed Gull, Caspian Tern, Double-crested Cormorant) found in the mid-Columbia River from April through August, 2002-2004. We used our model to explore several predator-prey scenarios, including the impact of historical bird abundance, and the effect of preserving vs. removing birds, on smolt abundance. Each year, <1% of the estimated available salmonid smolts (interannual range: 44,830-109,209; 95% CI = 38,000-137,000) were consumed, 85-98% away from dams. Current diet data combined with historical gull abundance at dams suggests that past smolt consumption may have been 1.5-3 times current numbers, depending on the assumed distribution of gulls along the reaches. After the majority (80%) of salmonid smolts have left the study area, birds switch their diet to predominantly juvenile northern pikeminnow (Ptychocheilus oregonensis), which as adults are significant native salmonid predators in the Columbia River. Our models suggest that one consequence of removing birds from the system may be increased pikeminnow abundance, which--even assuming 80% compensatory mortality in juvenile pikeminnow survival--would theoretically result in an annual average savings of just over 180,000 smolts, calculated over a decade. Practically, this suggests that smolt survival could be maximized by deterring birds from the river when smolts are present, allowing bird presence after the diet switch to act as a tool for salmonid-predator control, and conducting adult-pikeminnow control throughout. Our analysis demonstrates that identifying the strength of ecosystem interactions represents a top priority when attempting to manage the abundance of a particular ecosystem constituent, and that the consequences of a single-species view may be counterintuitive, and potentially counterproductive.     

苏州工业园区不同生境鸟类群落结构及季节动态

2012年5月至2013年4月,在苏州工业园区选择了4种生境,设置了17条样线、24个样点,逐月对鸟类群落进行了研究。共记录到鸟类130种,隶属12目41科,雀形目鸟类占主要地位,其中留鸟、夏候鸟、冬候鸟和旅鸟分别占鸟类总种数的26.15%、25.38%、27.69%和20.77%。区系以广布种和古北界种类为主,兼有东洋界种类,具有南北过渡的明显特征。从季节动态变化上看,园区鸟种数由多到少表现为春季冬季秋季夏季;密度由高到低表现为冬季秋季春季夏季。湿地生境鸟类种数最多,分布均匀;道路生境鸟类种数最少,分布不均,但优势种突出,以常见的伴人雀形目鸟类为主。聚类结果显示,环境条件是影响鸟类组成的重要因素。     

Quantifying the global threat to native birds from predation by non-native birds on small islands

Although invasive non-native species can adversely affect biodiversity in many ways, predation of native species by non-native species on islands can be severely damaging. Results of numerous studies document non-native birds preying on birds on islands, but our understanding of the number and type of species affected has been limited by the lack of a global review of these impacts. I identified the non-native bird species that have been recorded preying on birds, the locations where this predation occurred, and the bird species affected. Because the impacts of non-native birds can be particularly severe on small islands, I then identified the islands <500 km² around the world that are occupied by predatory non-native birds. By taking into account their life-history traits and predation history, I also identified the near-threatened and threatened bird species on these islands that they may prey on. The results indicated that predation by non-native birds was primarily a concern for threatened bird conservation on small islands; almost all predation impacts (91%) on near-threatened and threatened birds were recorded on islands, and median island size was 106 km². I also found non-native bird predation was a poorly known and widespread potential threat to avian biodiversity; worldwide, 194 islands of <500 km² were occupied by predatory non-native birds, but information on their impacts was unavailable for most of these islands. On them, where the impacts of non-native species can be severe, non-native birds may be preying on approximately 6% of the world's near-threatened and threatened bird species. Four non-native bird species I identified have been successfully eradicated from islands. If they were eradicated from the small islands they occupy, 70% of the near-threatened and threatened bird species I identified would no longer be affected by nest predation by non-native birds on small islands.     

Effects of learning and adaptation on population viability

Cultural adaptation is one means by which conservationists may help populations adapt to threats. A learned behavior may protect an individual from a threat, and the behavior can be transmitted horizontally (within generations) and vertically (between generations), rapidly conferring population-level protection. Although possible in theory, it remains unclear whether such manipulations work in a conservation setting; what conditions are required for them to work; and how they might affect the evolutionary process. We examined models in which a population can adapt through both genetic and cultural mechanisms. Our work was motivated by the invasion of highly toxic cane toads (Rhinella marina) across northern Australia and the resultant declines of endangered northern quolls (Dasyurus hallucatus), which attack and are fatally poisoned by the toxic toads. We examined whether a novel management strategy in which wild quolls are trained to avoid toads can reduce extinction probability. We used a simulation model tailored to quoll life history. Within simulations, individuals were trained and a continuous evolving trait determined innate tendency to attack toads. We applied this model in a population viability setting. The strategy reduced extinction probability only when heritability of innate aversion was low (<20%) and when trained mothers trained >70% of their young to avoid toads. When these conditions were met, genetic adaptation was slower, but rapid cultural adaptation kept the population extant while genetic adaptation was completed. To gain insight into the evolutionary dynamics (in which we saw a transitory peak in cultural adaptation over time), we also developed a simple analytical model of evolutionary dynamics. This model showed that the strength of natural selection declined as the cultural transmission rate increased and that adaptation proceeded only when the rate of cultural transmission was below a critical value determined by the relative levels of protection conferred by genetic versus cultural mechanisms. Together, our models showed that cultural adaptation can play a powerful role in preventing extinction, but that rates of cultural transmission need to be high for this to occur.     

Optimal fire histories for biodiversity conservation

Fire is used as a management tool for biodiversity conservation worldwide. A common objective is to avoid population extinctions due to inappropriate fire regimes. However, in many ecosystems, it is unclear what mix of fire histories will achieve this goal. We determined the optimal fire history of a given area for biological conservation with a method that links tools from 3 fields of research: species distribution modeling, composite indices of biodiversity, and decision science. We based our case study on extensive field surveys of birds, reptiles, and mammals in fire‐prone semi‐arid Australia. First, we developed statistical models of species’ responses to fire history. Second, we determined the optimal allocation of successional states in a given area, based on the geometric mean of species relative abundance. Finally, we showed how conservation targets based on this index can be incorporated into a decision‐making framework for fire management. Pyrodiversity per se did not necessarily promote vertebrate biodiversity. Maximizing pyrodiversity by having an even allocation of successional states did not maximize the geometric mean abundance of bird species. Older vegetation was disproportionately important for the conservation of birds, reptiles, and small mammals. Because our method defines fire management objectives based on the habitat requirements of multiple species in the community, it could be used widely to maximize biodiversity in fire‐prone ecosystems. Historiales de Incendios Óptimos para la Conservación de la Biodiversidad     

Targeted gene flow and rapid adaptation in an endangered marsupial

Targeted gene flow is an emerging conservation strategy. It involves translocating individuals with favorable genes to areas where they will have a conservation benefit. The applications for targeted gene flow are wide-ranging but include preadapting native species to the arrival of invasive species. The endangered carnivorous marsupial, the northern quoll (Dasyurus hallucatus), has declined rapidly since the introduction of the cane toad (Rhinella marina), which fatally poisons quolls that attack them. There are, however, a few remaining toad-invaded quoll populations in which the quolls survive because they know not to eat cane toads. It is this toad-smart behavior we hope to promote through targeted gene flow. For targeted gene flow to be feasible, however, toad-smart behavior must have a genetic basis. To assess this, we used a common garden experiment, comparing offspring from toad-exposed and toad-naïve parents raised in identical environments, to determine whether toad-smart behavior is heritable. Offspring from toad-exposed populations were substantially less likely to eat toads than those with toad-naïve parents. Hybrid offspring showed similar responses to quolls with 2 toad-exposed parents, indicating the trait may be dominant. Together, these results suggest a heritable trait and rapid adaptive response in a small number of toad-exposed populations. Although questions remain about outbreeding depression, our results are encouraging for targeted gene flow. It should be possible to introduce toad-smart behavior into soon to be affected quoll populations.