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HOT TOPICS IN ECOLOGY https://www.ecolsoc.org.au/hot-topics/ecological-impacts-invasive-cane-toads Ecological impacts of invasive cane toads An invader's arrival is bad news for some native species, but good news for others Rick Shine 1. The invasion of cane toads through Australia kills many large predators, that are poisoned when they try to eat large, highly toxic toads. 2. But most native species are not affected by toads, because they soon learn not to eat them; or else have a preexisting tolerance to the toad's poison. 3. The decrease in numbers of large predators benefits many smaller species, which increase in numbers after cane toads arrive in an area. Ecological Society of Australia https://www.ecolsoc.org.au Further information about this topic contact: Prof Rick Shine [email protected] 02-9351-3772 Chair, Hot Topics Editorial Board Dr Rachel Standish Large predators like this freshwater crocodile (Crocodylus johnstoni) can be in big trouble when cane toads invade, but most smaller species are less affected by toad invasion. Indeed, the collapse of apex predator populations is good news for the species previously consumed by those predators. Photograph by G. P. Brown. Cane toads (Rhinella marina) were brought to Australia in 1935, and released in northeastern Queensland. They have since spread westwards (through Queensland, the Northern Territory, and into Western Australia) and southwards (into NSW). Concern about the toads’ impacts on wildlife spawned predictions that most native species encountering toads would be severely affected, and thus decline in abundance. Recent research is revealing a more complex picture. Toads do indeed cause precipitous population declines (of >80%) in some large-bodied predator species, due to lethal poisoning when predators attempt to eat toads. However, populations of smaller predator species are unaffected; some individuals are fatally poisoned, but most survive (because small toads contain far less toxin than large adult toads) and learn to avoid toads thereafter. Most Australian birds and rodents have inherited a tolerance of toad poison from Asian ancestors, and thus are not affected. Even for heavily impacted predators, populations might eventually recover. Simplistic predictions on the ecological impact of cane toads in Australia have not been supported by field studies - indirect impacts of toads often outweigh direct effects. For example, the abundance of native frogs appears to be unaffected by cane toads, because negative impacts (e.g. frogs being eaten by toads, poisoned by toads, competing with toads) are balanced by positive impacts (e.g. toads reducing abundance of frog-predators). Some native snake species predicted to be vulnerable to toads, have become more common since toad invasion – presumably because of the disappearance of predatory goannas. In summary, the impacts of invaders may be complex, and difficult to predict. Any disruption to one native species is likely to have indirect effects on others. Some native species are winners not losers as the toad invasion rolls across the landscape. Status: approved ; Last updated: 02/07/2014 1 HOT TOPICS IN ECOLOGY https://www.ecolsoc.org.au/hot-topics/ecological-impacts-invasive-cane-toads Ecological impacts of invasive cane toads An invader's arrival is bad news for some native species, but good news for others Rick Shine Supporting Evidence Title Aim Key Results Beckmann C. & Shine R. (2009) Are Australia's birds at risk due to the invasive cane toad? Conserv. Biol. 23, 1544–9. To determine which bird species are potentially at risk of consuming toxic toads and whether the predicted impact is real, or due to a dearth of empirical evidence 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. Thus many bird species are potentially at risk, however 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 Brown G. P., Phillips B. L. & Shine R. (2011a) The ecological impact of invasive cane toads on tropical snakes: field data do not support predictions from laboratory studies. Ecology 92, 422–31. To evaluate the accuracy of our a priori predictions of the impacts of toads on an assemblage of 12 reptile species in tropical Australia. Two main conclusions emerge from the study: (1) fewer snake species declined in abundance after toad invasion than was predicted a priori based on toxin tolerances and feeding habits; and (2) many of the shifts in snake abundance that occurred at about the time of toad invasion likely were not causally driven by toad impact Caller G. & Brown C. (2013) Evolutionary responses to invasion: cane toad sympatric fish show enhanced avoidance learning. PLoS ONE 8, e54909. To determine whether aversion learning is occurring in aquatic ecosystems by comparing cane toad naïve and sympatric populations of crimson spotted rainbow fish Cane toad sympatric fish showed reduced attacks on both cane toad tadpoles and native tadpoles which highlights evolutionary shifts in the ability of these fish to learn to recognise and subsequently avoid novel, noxious prey items. Doody J. S., Green B., Sims R., Rhind D., West P. & Steer D. (2006) Indirect impacts of invasive cane toads (Bufo marinus) on nest predation in pig-nosed turtles (Carettochelys insculpta). Wildl. Res. 33, 349–54. To quantify and understand the indirect or secondary impacts of the decline in the yellowspotted monitor lizard (Varanus panoptes) associated with the arrival of cane toads, and the predicted simultaneous impact on pig-nosed turtle nest predation by yellowspotted monitors Yellow-spotted monitors have been reduced to such low numbers that they are currently no longer a significant predator of pignosed turtle eggs Letnic M., Webb J. K. & Shine R. (2008) Invasive cane toads (Bufo marinus) cause mass mortality of freshwater crocodiles (Crocodylus johnstoni) in tropical Australia. Biol. Conserv. 141, 1773–82. To quantify the impact of this massive mortality event on the freshwater crocodile population from the Victoria River. The impact of cane toad invasion on freshwater crocodiles may increase with increasing aridity. Subadult crocodiles are particularly vulnerable to lethal toxic ingestion from eating cane toads, and with the exception of hatchlings, this size class showed the greatest decrease in abundance following the arrival of cane toads Lettoof D. C., Greenlees M. J., Stockwell M. & Shine R. (2013) Do invasive cane toads affect the parasite burdens of native Australian frogs? Int. J. Parasitol.: Parasite. Wildl. 2, 155–65. To determine if the cane toad invasion influences rates of parasitism in native frogs Contrary to initial predictions, toad invasion was associated with a reduced parasite burden in native frogs. Thus, cane toads do not appear to transfer novel parasites to native frog populations, or act as a reservoir for native parasites to ‘spill-back’ into native frogs. Instead, cane toads may reduce frog-parasite numbers by taking up native parasites that are then killed by the toad’s immune defences. O'Donnell S., Webb J. K. & Shine R. (2010) Conditioned taste aversion enhances the survival of an endangered predator imperiled by a toxic invader. J. Appl. Ecol. 47, 558–65. To investigate whether conditioned taste aversion (CTA) could be used to mitigate toad impacts by modifying quoll predatorybehaviour and enhance survival An aversion to live toads in juvenile northern quolls was successfully induced by feeding them a dead toad containing a nausea-inducing chemical (thiabendazole). In both sexes, toadsmart quolls had higher apparent survival rates than did toadnaive conspecifics Phillips B. L. & Shine R. (2006) An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia. Proc. R. Soc. B 273, 1545–50. To examine the possibility that red-belly blacksnakes display an adaptive response to the presence of cane toads Strong differences were evident between blacksnakes from toadexposed versus toad-naive populations both in their physiological resistance to toad toxin and in their willingness to eat toads. Importantly, both of these differences are in an adaptive direction i.e. there is an increased resistance to toxin and lowered preference for consuming toads in toad-exposed populations 2 HOT TOPICS IN ECOLOGY https://www.ecolsoc.org.au/hot-topics/ecological-impacts-invasive-cane-toads Ecological impacts of invasive cane toads An invader's arrival is bad news for some native species, but good news for others Rick Shine Title Aim Key Results Pizzatto L. & Shine R. (2011) Ecological impacts of invading species: do parasites of the cane toad imperil Australian frogs? Austral Ecol. 36, 954–63. To explore the risk posed by Rhabdias pseudosphaerocephala lungworms to native frogs, and to assess the effects of Rhabdias exposure on anuran survival, growth and locomotor performance Laboratory experiments showed that infective Rhabdias larvae can penetrate the body of all seven species of Australian frogs tested (five hylids: Cyclorana longipes, Litoria caerulea, Litoria dahlii, Litoria nasuta, Litoria rothii, one myobatrachid: Opisthodon ornatus, and one limnodynastid: Limnodynastes convexiusculus), but most did not host the adult worms at the end of the trials, and none showed major impairment of growth, survival or locomotor performance. One native tree-frog (L. caerulea) retained high infection levels with few ill effects, suggesting that we might be able to use this taxon as a reservoir species to build up local parasite densities for toad management. Shine R. & Doody J. S. (2011) Invasive-species control: understanding conflicts between researchers and the general community. Frontiers Ecol. Environ. 9, 400–6. To better understand the reasons for disagreements between scientists and community groups about the nature and magnitude of conservation efforts aimed at the invasive cane toad Appreciating the pressures faced by all participants engaged in conservation debates can lead to a more constructive and cooperative atmosphere Shine R. (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q. Rev. Biol. 85, 253–91. To review the ecological impacts of cane toads in Australia Overall, some Australian native species (mostly large predators) have declined due to cane toads; others, especially species formerly consumed by those predators, have benefited. For yet others, effects have been minor or have been mediated indirectly rather than through direct interactions with the invasive toads. Factors that increase a predator’s vulnerability to toad invasion include habitat overlap with toads, anurophagy, large body size, inability to develop rapid behavioral aversion to toads as prey items, and physiological vulnerability to bufotoxins as a result of a lack of coevolutionary history of exposure to other bufonid taxa. Shine R. (2014) A review of ecological interactions between native frogs and invasive cane toads in Australia. Austral Ecol. 39:1-16. To review current information on ecological interactions between cane toads and Australian anurans Overall, the interactions between native frogs and invasive toads illustrate the diverse ways in which an invader’s arrival can perturb the native fauna by both direct and indirect mechanisms, and by which the native species can curtail an invader’s success. Ward-Fear G., Brown G. P., Greenlees M. & Shine R. (2009) Maladaptive traits in invasive species: in Australia, cane toads are more vulnerable to predatory ants than are native frogs. Funct. Ecol. 23, 559–68. To determine how cane toad phenotypes differ from native frogs and then to explore the possibility that any differences might render cane toads more vulnerable to a predator (meat ant) that poses little threat to native anurans Unlike the frogs, (1) toads selected open microhabitats and were active diurnally, thus increasing encounter rates with meat ants; (2) toads failed to detect and evade approaching ants; (3) toads exhibited poor locomotor ability (short slow hops, reflecting their small size and short limbs); and (4) toads frequently relied on an ineffective defence mechanism (crypsis) when attacked. In combination, these traits rendered cane toad metamorphs far more susceptible to predation by meat ants than were any of the native frogs tested. That vulnerability presumably reflects lack of coevolution between cane toads and Australian ants. 3