The ecological and evolutionary impact of cane toads
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Phillips, B., G. P. Brown, and R. Shine. 2003. Assessing the potential impact of cane toads (Bufo marinus) on Australian snakes. Conservation Biology 17:1738-1747.
In this paper, we look at which species of Australian snake are likely to be at risk from toads, based on their geographic distributions and whether or not they eat frogs (and hence, are likely to try to eat toads). We also show that most (but not all) Aussie snakes are very sensitive to toad poisons. We conclude that a high proportion of Australian snake species might be at risk from toads.
Phillips, B., and R. Shine. 2004. Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proceedings of the National Academy of Sciences (USA) 101:17150-17155.
If you are a frog-eating snake and toxic cane toads arrive, the best chance of survival may be if you are a big snake with a small head. In this way, you simply cannot open your mouth wide enough to eat a toad large enough to kill you. Ben’s measurements of preserved museum specimens showed that in two frog-eating snake species, that’s exactly the pattern we see. Following toad invasion, average body size increases and relative head size decreases. In combination with some of our other results, the clear message is that Aussie ecosystems can change rapidly to deal with new challenges like the toad invasion.
Phillips, B., G. P. Brown, and R. Shine. 2004. Assessing the potential for an evolutionary response to rapid environmental change: invasive toads and an Australian snake. Evolutionary Ecology Research 6:799-811.
Is there genetic variation for traits (such as tolerance to toad poisons) that might help a population adapt to the arrival of toads? Without such variation, natural selection cannot act. We show that such variation does indeed occur in keelback snakes.
Phillips, B., and R. Shine. 2005. The morphology, and hence impact, of an invasive species (the cane toad, Bufo marinus) changes with time since colonization. Animal Conservation 8:407-413.
The risk that a cane toad poses to a predator depends on how much poison it has within its body – in turn, dependent on how big the toad is, and how big its poison-glands (parotoid glands) are. We show that both of these characteristics shift with time since toads arrived in an area. Toads at the invasion front are bigger, and have bigger toxin glands. We're not sure why these changes occur; they might be due to evolution, or be induced by some aspects of the local environment. Ben is currently running breeding trials with toads, that will answer these and other questions.
Phillips, B. L., and R. Shine. 2006. Allometry and selection in a novel predator-prey system: Australian snakes and the invading cane toad. Oikos 112:122-130.
The vulnerability of a snake predator to a toad depends on the rate that increasing body size enables a snake to eat a bigger toad; and also, the rate that the toad’s total amount of poison increases with its own body size. We measure these size-related changes, to calculate how vulnerable particular kinds of snakes are likely to be.
Phillips, B., and R. Shine. 2006. Spatial and temporal variation in the morphology (and thus, predicted impact) of an invasive species in Australia. Ecography 29:205-212.
Whether or not a predator dies when it eats a toad depends upon the size and toxicity of the toad. This paper maps the variation in space (across Qld) and time (through the year) of toad body size and toad gland size. Both of these traits are critical to the impact that a toad population can have (because body size determines both toxicity, and whether a predator can handle a toad, and gland size determines the toxicity). This paper shows that there is meaningful spatial variation in the toxicity of toads and hence their potential impact on gape-limited predators (such as snakes); toads are more toxic in some areas than in others.
Phillips, B. L., and R. Shine. 2006. An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia. Proceedings of the Royal Society B 273:1545-1550.
There are many reports of mortality of predators that attack toads. These reports mostly come from areas where toads have just invaded. Our surveys show that predator numbers can indeed fall dramatically due to toad-poisoning, but (encouragingly!) those species do not actually disappear entirely. Indeed, many become common once again (possibly within a decade), and somehow coexist with toads. We show that blacksnakes in toad-infested areas have changed (in feeding behaviour, physiology and relative head size) in ways that enable them to survive despite the toads’ presence. Mother Nature is a tough old lady, and Australian ecosystems have had to cope with many challenges over the last few million years! Toads are just one more challenge.
Smith, J. G., and B. L. Phillips. 2006. Toxic tucker: assessing the potential impact of cane toads on Australia's reptiles. Pacific Conservation Biology 12:40-49.
James and Ben followed up our earlier work on snakes, testing a range of lizards, crocodiles and turtles to see which ones could tolerate toad poisons. The results were similar to the snake work: most species of non-snake Australian reptiles also have very low resistance to toad toxin, although there appears to be much greater variation in toxin resistance between species. Perhaps the most surprising result from this work is that saltwater crocodiles appear to be quite resistant to toad toxin, whereas freshwater crocodiles are highly susceptible.
Greenlees, M. J., G. P. Brown, J. K. Webb, B. L. Phillips, and R. Shine. 2006. Effects of an invasive anuran (the cane toad, Bufo marinus) on the invertebrate fauna of a tropical Australian floodplain. Animal Conservation 9:431-438.
For his Honours year, Matt built outdoor enclosures on the edge of the floodplain, and added frogs to some, toads to others, and no amphibians at all to the remainder. He then surveyed the invertebrates within each enclosure, to actually measure the effect of toads (compared to native frogs) on the numbers and types of insects remaining. To our surprise, toads were not too different from frogs in their effects: both changed invertebrate numbers to about the same degree, though (probably because they are bigger) toads had a bit more effect.
Hagman, M., and R. Shine. 2007. Effects of invasive cane toads on Australian mosquitoes: does the dark cloud have a silver lining? Biological Invasions 9:445-452.
Several people have reported that mosquito numbers have fallen since toads arrived. Why would this happen? Adult toads rarely eat adult mosquitoes, so we thought the effect might occur in the larval stage. Thus, Mattias set up tanks with mosquito larvae either with or without cane toad tadpoles. The toad tadpoles increased mortality in one species of mosquito, and reduced body sizes at emergence in the others. Also, female mosquitoes avoided laying their eggs in ponds containing toad tadpoles. These effects are similar to those we have already shown with native frogs: it seems that mosquitoes don’t really like either frogs OR toads. This doesn't mean that toads will reduce mozzie numbers - that depends on many factors, such as whether the mosquitoes are breeding in mangroves or in freshwater ponds, etc - but it's an interesting example of the fact that invasive species have complex effects - and some people would rate some of those effects as positive, not negative.
Greenlees, M. J., G. P. Brown, J. K. Webb, B. L. Phillips, and R. Shine. 2007. Do invasive cane toads (Chaunus marinus) compete with Australian frogs (Cyclorana australis)? Austral Ecology 32:900-907.
Using the enclosures that he constructed on the floodplain fringe (see above), Matt put combinations of toads and frogs together (versus separately) to see if the presence of a toad reduced the feeding rate or activity level of a native Giant Burrowing Frog. The frogs were less active if toads were present in the arena, but the overall effect on feeding rate was pretty small. It may be that on hot humid nights in the tropics, the number of bugs is so great that there is little effective competition between frogs, or between frogs and toads. Certainly, anybody who has ever spent time out on the Adelaide River floodplain during the wet-season will testify to the fact that it is one of the buggiest places in the universe!
Webb, J. K., G. P. Brown, T. Child, M. J. Greenlees, B. L. Phillips, and R. Shine. 2008. A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid toxic cane toads. Austral Ecology 33:821-829.
It seems that one of the toads' main victims in Australia has been the quoll, a medium-sized marsupial carnivore. Quolls try to eat toads (and just about anything else that moves!), and die as a result because of the toad's toxic poisons. We wondered about smaller relatives of the quoll - small mouse-sized marsupials like the planigale. These little blokes are common on the Adelaide River floodplain - what would happen when the toads arrived? Would the planigales attack them and die, like the quolls? To our relief, planigales proved to be surprisingly smart. A few died after they attacked toads, but most did not - and the survivors rapidly learned that toads were best avoided. Thus, planigales should not be too badly affected by the toad invasion.
Letnic, M., J. K. Webb, and R. Shine. 2008. Invasive cane toads (Bufo marinus) cause mass mortality of freshwater crocodiles (Crocodylus johnstoni) in tropical Australia. Biological Conservation 141:1773-1782.
Although there are many anecdotal reports of cane toad invasion resulting in the deaths of native predators that try to eat these poisonous amphibians, there is very little real detail on population-level effects. Our surveys in upstream areas of the Daly and Victoria Rivers show a major impact of toad arrival on freshwater crocodile numbers, and on the distribution of body sizes within the crocodile population. Remarkably, cane toads have little or no effect on freshwater crocs at Fogg Dam, perhaps because the toads rarely come to the water's edge where they would meet crocs - instead, there are plenty of puddles around where the toads can rehydrate. In the drier upstream areas around the rivers, though, the toads and crocs are forced into close contact - with devastating results.
Pizzatto, L., and R. Shine. 2009. Native Australian frogs avoid the scent of invasive cane toads. Austral Ecology 34:77-82.
Frogs and toads both lose water quickly in dry conditions, so spend most of the day in shelters where they can stay moist. One way that toad invasion might affect native frogs would be to discourage them from using favoured shelter-sites if those spots are already being occupied by cane toads. Ligia tested the responses of small (newly-transformed) native frogs to various smells, and found that the little frogs avoided places that smell like adult cane toads. However, the little frogs also avoided other strong smells, so this may just be a general response not a specific cane-toad-related behaviour. And we doubt that hiding places are too hard to find, so this may not be a big issue for the local frogs unless they are restricted to the pond margins by dry weather, and so are confronted with lots of toads as neighbours.
Crossland, M. R., R. A. Alford, and R. Shine. 2009. Impact of the invasive cane toad (Bufo marinus) on an Australian frog (Opisthodon ornatus) depends on reproductive timing. Oecologia 158:625-632.
In outdoor trials in ponds, the exact time at which we added either toad eggs or tadpoles, or the eggs or tadpoles of native frogs, massively affected the numbers of baby frogs or toads that survived to emerge from the ponds. For example, if we added toad eggs to a pond already containing native tadpoles, the natives ate the eggs and many were fatally poisoned - so this reduced the numbers of metamorphs a few weeks later. But on the other hand, lower densities of tadpoles in that circumstance reduced competition for food, so the surviving tadpoles grew quicker and emerged at a larger size. That larger size might sometimes be a huge advantage - in which case, the arrival of cane toads might actually increase not decrease the numbers of frogs emerging successfully to recruit to the population!
Llewelyn, J., B. L. Phillips, and R. Shine. 2009. Sublethal costs associated with the consumption of toxic prey by snakes. Austral Ecology 34:179-184.
One of the only Australian snakes that is immune to the cane toads' poison is the keelback, a harmless species that is widely distributed in the tropics. John followed up some earlier work by Ben, showing that although keelbacks can indeed eat toads without dying, the toads are still pretty awful in terms of food quality. First, the toads' poison tends to slow the snake down - so that it takes a long time to eat a toad, and then may be almost paralysed for quite a while. This could be bad news if a predator comes along. Second, even if the snake eats the toad, there doesn't seem to be much net nutritional value - snakes fed on toads tend to lose weight, whereas snakes fed the same amount of frogs grow bigger. So, although keelbacks can eat toads, they don't get much benefit from doing so.
Shine, R., M. Greenlees, M. R. Crossland, and D. Nelson. 2009. The myth of the toad-eating frog. Frontiers in Ecology and the Environment 7:359-361.
There was a lot of publicity a few years ago when a community-group spokesperson in Darwin suggested that one of the local frogs (Litoria dahlii) could eat cane toads, and so might be a saviour for local biodiversity. It's a great story, but unfortunately our actual trials painted a different picture. This frog species was like all the others we tested - they are readily killed by the toad's poison. Fortunately, the frogs mostly learn to avoid toads quite quickly, after they become sick after eating one - and so, there isn't a huge amount of frog mortality by a year or two after the toads arrive. However, it's a good example of how a "cute" story about toads, even if it has very little factual basis, can get a lot of publicity!
Pearson, D. J., M. Greenlees, G. Ward-Fear, and R. Shine. 2009. Predicting the ecological impact of cane toads (Bufo marinus) on threatened camaenid land snails in north-western Australia. Wildlife Research 36:533-540.
Toads will eat just about anything, although they focus mostly on small ants and beetles and the like. The Western Australian wildlife management authorities were worried that toads might pose a threat by eating endangered land snails. Our lab trials showed that cane toads will indeed eat native snails quite happily, but the kinds of habitats these snails occupy are not popular with toads – they are steep rocky areas that toads tend to avoid.
Hagman, M., B. L. Phillips, and R. Shine. 2009. Fatal attraction: adaptations to prey on native frogs imperil snakes after invasion of toxic toads. Proceedings of the Royal Society B 276:2813-2818.
Death adders are large venomous snakes that have an unusual way of catching their food. The snake lies camouflaged without moving, and wriggles the tip of its tail to mimic the movements of a caterpillar or grub. Frogs and lizards that approach the lure are seized by the snake. We showed that the snake’s lure works much better to attract cane toads than to attract native frogs. Thus, the snakes are luring their own worst enemy – when a death adder bites a toxic toad, the encounter is likely to be fatal for both parties.
Beckmann, C., and R. Shine. 2009. Are Australia's birds at risk due to the invasive cane toad? Conservation Biology 23:1544-1549.
Although some community groups have been worried about toad impacts on Australia’s birds, Christa’s review is encouraging – there are very few records of birds being poisoned by toads. Most birds avoid them, or selectively eat the bits (tongue etc) that aren’t too poisonous. Birds seem to be very resistant to toad poisons anyway.
Phillips, B. L., M. J. Greenlees, G. P. Brown, and R. Shine. 2010. Predator behaviour and morphology mediates the impact of an invasive species: cane toads and death adders in Australia. Animal Conservation 13:53-59.
Ben captured death adders from our Fogg Dam area just before the toads invaded. He tested the snakes’ responses to toads in captivity (would they try to eat a toad or not?) then released them with radiotransmitters so he could check on them every day. The adders that tried to eat toads in the lab also did so after they were released, and were fatally poisoned. The snakes that ignored toads in the lab generally did the same in the field and survived. Interesting, a smaller head size (which prevent s the snake from swallowing a really big toad) also aided the snake’s survival.
Llewelyn, J., L. Schwarzkopf, R. Alford, and R. Shine. 2010. Something different for dinner? Responses of a native Australian predator (the keelback snake) to an invasive prey species (the cane toad). Biological Invasions 12:1045-1051.
Although keelback snakes can deal with the cane toad’s poisons, they don’t really like to eat them. They much prefer native frogs, probably because they are less poisonous (or taste better?).
Beckmann, C., and R. Shine. 2010. The power of myth: the (non) impact of invasive cane toads (Bufo marinus) on domestic chickens (Gallus gallus). Animal Production Science 50:847-851.
Farmers have been worried about their chickens being poisoned by eating cane toads. The story about chicken vulnerability has been around ever since toads were brought to Australia, but it’s nonsense. Our chickens either ignored toads, or gobbled them up with gusto – and suffered no ill effects even if they ate a dozen or so small toads.
Crossland, M., and R. Shine. 2010. Vulnerability of an Australian anuran tadpole assemblage to the toxic eggs of the invasive cane toad (Bufo marinus). Austral Ecology 35:197-204.
When cane toads spawn in ponds near Fogg Dam, many native tadpoles are fatally poisoned by eating the toxic eggs. We tested tadpoles of several native frog species in the lab, to see if any would refuse the toad eggs, or tolerate the poison. Unfortunately they all proved vulnerable.
Llewelyn, J., J. K. Webb, L. Schwarzkopf, R. Alford, and R. Shine. 2010. Behavioural responses of carnivorous marsupials (Planigale maculata) to toxic invasive cane toads (Bufo marinus). Austral Ecology 35:560-567.
We know from our previous studies in the Northern Territory that small carnivorous marsupials are not too badly affected by cane toad invasion. The planigales grab the first toad they see, but it makes them ill and so they leave them alone after that. A few die in the process, however. What happens in a place where the toads have been present for more than 50 years – Townsville, in Queensland? John found pretty much the same behaviour in Townsville as we found in Darwin. They tried to eat toads, got sick, and learnt not to do it again. None of the Queensland planigales died in the process of learning, though, so maybe they have evolved a higher tolerance to the toads’ poisons.
Greenlees, M. J., B. L. Phillips, and R. Shine. 2010. An invasive species imposes selection on life-history traits of a native frog. Biological Journal of the Linnean Society 100:329-336.
Baby native frogs readily try to eat baby toads – and if they manage to swallow them, are likely to die. This means that smaller baby frogs are at less risk – they learn the toad is poisonous while they hold it in their mouth, but they don’t get a full dose of poison so they survive. Bigger frogs swallow the toad, and die. So, it’s an advantage to be small if you are a baby frog when the toads arrive.
O'Donnell, S., J. K. Webb, and R. Shine. 2010. Conditioned taste aversion enhances the survival of an endangered predator imperiled by a toxic invader. Journal of Applied Ecology 47:558-565.
Steph won a prestigious international award for this paper. She trained captive-born quolls (cat-sized marsupial predators) to avoid cane toads as prey, by adding nausea-inducing chemicals to dead toads that she fed to the captive quolls. Then she released and radio-tracked the animals; and the trained quolls survived much better than their untrained brothers and sisters.
Shine, R. 2010. The ecological impact of invasive cane toads (Bufo marinus) in Australia. Quarterly Review of Biology 85:253-291.
This is a major review on the effects of cane toads. The federal government based a lot of their recent overhaul of anti-toad measures on Rick’s review.
Price-Rees, S. J., G. P. Brown, and R. Shine. 2010. Predation on toxic cane toads (Bufo marinus) may imperil bluetongue lizards (Tiliqua scincoides intermedia, Scincidae) in tropical Australia. Wildlife Research 37:166-173.
We noticed that bluetongue lizards virtually disappeared from the area around Fogg Dam soon after cane toads arrived. Sam tested bluetongue responses to toads – and sure enough, they try to eat them, and are very sensitive to the toads’ poison. So, these magnificent bluetongue lizards are major victims of toad invasion.
Pizzatto, L., C. M. Shilton, and R. Shine. 2010. Infection dynamics of the lungworm Rhabdias pseudosphaerocephala in its natural host, the cane toad Bufo marinus, and in novel hosts (Australian frogs). Journal of Wildlife Diseases 46:1152-1164.
Cane toads brought South American parasites (lungworms) with them when the toads were brought to Australia. The parasites can severely affect toads. What happens when they infect native frogs? Our lab studies showed that the parasites don’t function well inside most native frogs, suggesting that they may not pose much of a danger to the native frog fauna.
Nelson, D., M. R. Crossland, and R. Shine. 2010. Indirect ecological impacts of an invasive toad on predator-prey interactions among native species. Biological Invasions 12:3363-3369.
One of the ways that an invading species can affect native species is by changing their behaviour. David looked at how native fish learn to avoid cane toad tadpoles (which are poisonous), and how this affects the fish’s responses to native tadpoles that look like toad tadpoles. The fish were initially fooled, but soon learnt to tell the difference.
Greenlees, M., B. L. Phillips, and R. Shine. 2010. Adjusting to a toxic invader: native Australian frog learns not to prey on cane toads. Behavioral Ecology 21:966-971.
You might not think that baby frogs are very smart, but Matt showed that they are incredibly quick learners when it comes to cane toads. After one or two encounters with the poisonous toads, the baby frogs stopped trying to eat them.
Brown, G. P., B. L. Phillips, and R. Shine. 2011. The ecological impact of invasive cane toads on tropical snakes: field data do not support predictions from laboratory studies. Ecology 92:422-431.
Based on lab data on poison tolerances and feeding habits, we thought that many Australian snake species would be in big trouble when cane toads invaded. But remarkably, this hasn’t happened. One or two species of snakes at Fogg Dam may have been badly affected by toads, but most of the local snakes have actually increased not decreased in numbers since toads arrived. The reason may be that goannas (varanid lizards) often eat snakes. The goannas were killed off by the toads, so that now the snakes experience less predation.
Beckmann, C., and R. Shine. 2011. Toad's tongue for breakfast: exploitation of a novel prey type, the invasive cane toad, by scavenging raptors in tropical Australia. Biological Invasions 13:1447-1455.
Fork-tailed kits and black kites are common at Fogg Dam, and often eat road-killed frogs. They eat toads as well, and Christa conducted a series of experiments to measure how many toads were eaten, and the birds’ preferences for frogs rather than toads. Like most predators, the hawks reckon a tasty native frog makes a better meal than a poisonous toad – but in the dry season when frogs are scarce, the hawks eat plenty of toads as well (or at least, the less poisonous parts of the toads).
Nelson, D., M. R. Crossland, and R. Shine. 2011. Behavioural responses of native predators to an invasive toxic prey species. Austral Ecology 36:605–611.
David conducted lab experiments to look at what happens when native predators (fishes and frogs) first encounter toad tadpoles. The predators soon learnt to leave tadpoles alone.
Greenlees, M. J., and R. Shine. 2011. Impacts of eggs and tadpoles of the invasive cane toad (Bufo marinus) on aquatic predators in tropical Australia. Austral Ecology 36:53-58.
Matt’s lab experiments showed that cane toad tadpoles aren’t a problem for native fish and long-necked turtles – they eat the tadpoles, but spit them out immediately because they taste bad. But the same predators readily eat toad eggs as well, and don’t recognize how poisonous they are – so the predator can be killed. Toad eggs thus are more dangerous than toad tadpoles.
Llewelyn, J., B. L. Phillips, G. P. Brown, L. Schwarzkopf, R. A. Alford, and R. Shine. 2011. Adaptation or preadaptation: why are keelback snakes (Tropidonophis mairii) less vulnerable to invasive cane toads (Bufo marinus) than are other Australian snakes? Evolutionary Ecology 25:13-24.
Keelback snakes aren’t affected as much by cane toad poisons as are other Australian snakes. Is this because keelbacks have evolved to deal with the toads’ poisons, or did they inherit a resistance to those poisons from their Asian ancestors (because there are plenty of poisonous toads in Asia also)? John found that keelbacks have a high resistance to toad poison even in areas where the snakes have never met toads – so this is an ancestral characteristic of keelbacks, not an adaptation to cane toad invasion.
Ujvari, B., R. Shine, and T. Madsen. 2011. Detecting the impact of invasive species on native fauna: cane toads (Bufo marinus), frillneck lizards (Chlamydosaurus kingii), and the importance of spatial replication. Austral Ecology 36:126-130.
There have been lots of suggestions that frillneck lizards die when they eat cane toads, and that populations of these iconic lizards have declined as a result. Bea and Thomas were studying three frillneck populations near Fogg Dam when the toads arrived, and didn’t see any clear impact of toads at all. On average, the lizards were just as common after toads arrived as beforehand.
Nelson, D. W. M., M. R. Crossland, and R. Shine. 2011. Foraging responses of predators to novel toxic prey: effects of predator learning and relative prey abundance. Oikos 120:152-158.
How quickly a native predator learns to recognize cane toad tadpoles as noxious, and different from native tadpoles, is affected by issues such as how common the toads are compared to local frogs. David ran lab trials to show this.
Pizzatto, L., and R. Shine. 2011. Ecological impacts of invading species: do parasites of the cane toad imperil Australian frogs? Austral Ecology 36:954–963.
Most native frogs that Ligia tested were able to pick up the parasite from cane toads, but they generally were not badly affected by it. So, most native frogs species probably aren’t at risk from the parasite carried by toads.
Pizzatto, L., and R. Shine. 2011. The effects of experimentally infecting Australian tree frogs with lungworms (Rhabdias pseudosphaerocephala) of a newly-encountered parasite from invasive cane toads. International Journal of Parasitology 41:943–949.
But the bad news is that SOME frogs are affected by the toad’s parasite. Green tree frogs get infected, but don’t seem to experience too many problems from the lungworm. Unfortunately, magnificent tree frogs not only take up the parasite, but are likely to die as a result. Fortunately, the magnificent tree frogs mostly live in areas where they are unlikely to encounter many toads.
Beckmann, C., M. R. Crossland, and R. Shine. 2011. Responses of Australian wading birds to a novel toxic prey type, the invasive cane toad Rhinella marina. Biological Invasions 13:2925-2934.
Christa put out trays with fishes, tadpoles and so forth to see how birds like herons and egrets react to the invasive cane toad. Most birds just ignored the toads and ate the native food items; and eating a few toads didn’t seem to make them ill anyway. The birds don’t really seem to be affected much at all by toad invasion.
Somaweera, R., J. K. Webb, G. P. Brown, and R. Shine. 2011. Hatchling Australian freshwater crocodiles rapidly learn to avoid toxic invasive cane toads. Behaviour 148:501-517.
Baby crocodiles are smart! In lab trials, Ruchira’s baby crocs rapidly distinguished between frogs and toads, and soon began to eat the frogs but not the toads. None of the babies died after eating small toads, so learning will probably enable crocodile populations in Lake Argyle to withstand the toad invasion.
Webb, J. K., D. Pearson, and R. Shine. 2011. A small dasyurid predator (Sminthopsis virginiae) rapidly learns to avoid a toxic invader. Wildlife Research 38:726-731.
This paper shows that, like other small predatory marsupials, the red-cheeked dunnart from tropical Australia is very good at learning that toads make a dangerous meal. So, toad invasion probably will not greatly affect this species – they are too smart.
Somaweera, R., M. R. Crossland, and R. Shine. 2011. Assessing the potential impact of invasive cane toads on a commercial freshwater fishery in tropical Australia. Wildlife Research 38:380-385.
Catfish are a major commercial item in Lake Argyle in tropical northwestern Australia. Our experiments show that the toad invasion probably won’t have any major impact on catfish, although a few fish will be killed by eating toad eggs.
Crossland, M., G. P. Brown, and R. Shine. 2011. The enduring toxicity of road-killed cane toads (Rhinella marina). Biological Invasions 13:2135-2145.
Just because a toad is dead, doesn’t mean that it isn’t dangerous! We tested the carcasses of cane toads that had been run over, and had lain on the road for weeks or months. Remarkably, their poisons were still effective .. when we put them in water, tadpoles and fish tried to avoid the carcass – and if they couldn’t, were likely to die. This means that if large numbers of toad carcasses end up in roadside ditches, which are flooded by the first wet-season rains, the water may be dangerous for native species.
Beckmann, C., and R. Shine. 2012. How many of Australia’s ground-nesting birds are likely to be at risk from the invasive cane toad (Rhinella marina)? Emu 112:83-89.
One group of native animals that may be at risk from cane toads are the small birds – like bee-eaters – that nest on the ground. Cane toads will eat nestling birds, so could be a problem. However, our analysis suggests that it’s unlikely to be a significant issue.
Somaweera, R., and R. Shine. 2012. The (non) impact of invasive cane toads on freshwater crocodiles at Lake Argyle in tropical Australia. Animal Conservation 15:152-163.
In some places where cane toads have invaded, there has been massive mortality of freshwater crocodiles. In most places, though, the crocs have not been affected at all. We don’t really understand why this difference occurs. Ruchira’s studies show that cane toads have not had any significant effect on crocodiles in Lake Argyle – a very encouraging result, because this lake hosts the largest population of freshwater crocs in Australia. Ruchira’s data also show how community toad-busting activities can reduce toad numbers effectively for a few months, but eventually new toads move into the system and replace those that were removed.
Price-Rees, S. J., G. P. Brown, and R. Shine. 2012. Interacting impacts of invasive plants and invasive toads on native lizards. American Naturalist 179:413-422.
Native predators like blacksnakes have adapted to the cane toad invasion by evolving an increased tolerance of the toads’ poisons. Sam Price-Rees found that bluetongue lizards are also very vulnerable to cane toads, and that lizards from the east coast (where toads have been present for decades) have much higher tolerance of the poison than do lizards from Western Australia (where the toads are only now invading). We thought this was a similar case to the blacksnakes – adaptation to toads – but then we tested lizards from Sydney (where there were no toads) and found they were also very tolerant to the toads’ poison. Remarkably, a garden plant from Madagascar, called mother-of-millions, might be the reason for this puzzling situation. The plant contains poisons very similar to those of cane toads – a bizarre example of evolutionary convergence – so that lizards that eat the flowers of this plant (as bluetongues do) may have evolved to deal with the poison. So, when the toads arrived, the bluetongues were already “pre-adapted” to their poisons.
Llewelyn, J., K. Bell, L. Schwarzkopf, R. A. Alford, and R. Shine. 2012. Ontogenetic shifts in a prey’s chemical defence influence feeding responses of a snake predator. Oecologia 169:965-973.
The amount of poison in a toad changes as it grows – eggs have a lot, but then poison content decreases in older tadpoles, and doesn’t increase again until after metamorphosis, when the young toad begins to make its own poison. A snake that can tolerate toad poisons (the keelback) seems to have worked this out – the snakes selectively eat the stages of toads with the least poison (larger rather than smaller tadpoles, and smaller rather than larger baby toads).
Somaweera, R., R. Shine, J. Webb, T. Dempster, and M. Letnic. 2013. Why does vulnerability to toxic invasive cane toads vary among populations of Australian freshwater crocodiles? Animal Conservation 16:86-96.
Why do some populations of freshwater crocodiles crash when toads arrive, whether others are not affected? This study shows that it isn’t due to differences in factors such as feeding preferences or poison tolerance … so unfortunately, although we’ve managed to disprove some possibilities, it’s still a mystery!
Gonzalez-Bernal, E., M. J. Greenlees, G. P. Brown, and R. Shine. 2013. Interacting biocontrol programs: Invasive cane toads reduce rates of breakdown of cowpats by dung beetles. Austral Ecology 38:891-895.
Cane toads love to eat the dung beetles that are attracted to cowpats (cattle faeces piles). This reduces the rate at which the beetles (which were introduced to Australia to break down these cowpats) are able to do their work; and so, cane toads have reduced the effectiveness of this useful program.
Brown, G. P., B. Ujvari, T. Madsen, and R. Shine. 2013. Invader impact clarifies the roles of top-down and bottom-up effects on tropical snake populations. Functional Ecology 27:351-361.
Almost all animal species eat some other species, but themselves are eaten by others. So, the numbers of animals in a population can be determined either by how much food is available, or how many predators are out there eating them. The invasion of cane toads at Fogg Dam gave us a chance to explore this issue for keelbacks and slatey-grey snakes, because the toads killed off most of the big predators (goannas) that used to eat these snakes, but didn’t affect the numbers of frogs (a main food for the snakes).
Lettoof, D. C., M. J. Greenlees, M. Stockwell, and R. Shine. 2013. Do invasive cane toads affect the parasite burdens of native Australian frogs? International Journal for Parasitology: Parasites and Wildlife 2:155-164.
Lots of people have worried that cane toads will bring new parasites to infect native frogs; but Damian’s study in northeastern NSW showed the opposite effect: frogs actually have fewer parasites after toads invade, not more. This remarkable result probably reflects the fact that the larvae of parasites infect toads, but aren’t able to develop successfully – and so, the toads remove a lot of the parasites that otherwise would infect frogs.
Brown, G. P., M. J. Greenlees, B. L. Phillips, and R. Shine. 2013. Road transect surveys do not reveal any consistent effects of a toxic invasive species on tropical reptiles. Biological Invasions 15:1005-1015.
If cane toads had a devastating impact on native snakes, as many people think they do, then we would expect to see fewer snakes after toad arrival than before. But we don’t. Our standard surveys of snake numbers at night over several years before and after toad invasion, along three roads near Fogg Dam, showed no consistent effects of toads on snake abundance. Snake numbers decreased along a busy highway, but increased or stayed the same along other smaller roads. Highway mortality – through being run over – seems to have been more of a problem for tropical snakes than has the arrival of cane toads.
Kelehear, C., G. P. Brown, and R. Shine. 2013. Invasive parasites in multiple invasive hosts: the arrival of a new host revives a stalled prior parasite invasion. Oikos 122:1317-1324.
Crystal found a lungworm species in cane toads near Darwin. Her analyses showed that this parasite is usually only found in invasive house geckos, not native lizards or frogs – but it can live in cane toads. So, the invasion of toads has provided a new host, and will enable this lungworm to spread over a much wider area than is the case at present.
Bleach, I., C. Beckmann, G. P. Brown, and R. Shine. 2014. Effects of an invasive species on refuge-site selection by native fauna: the impact of cane toads on native frogs in the Australian tropics. Austral Ecology 39:50-59.
Our earlier laboratory studies suggested that native frogs may avoid the scent of cane toads – and so, the arrival of toads might reduce the number of burrows available for frogs to shelter in. Iris’ field studies showed that this isn’t as much of a problem as we expected. Frogs and toads tend to select different types of burrows, and the arrival of a toad in a burrow didn’t consistently cause frogs to leave.
Llewelyn, J., L. Schwarzkopf, B. L. Phillips, and R. Shine. 2014. After the crash: how do predators adjust following the invasion of a novel toxic prey type? Austral Ecology 39:190-197.
Studies in the NT and Western Australia consistently show that yellow-spotted goannas die in huge numbers when toads arrive (about 95% mortality), because these large predators are fatally poisoned when they try to eat the toxic toads. But the same goanna species is common in northeastern Queensland, where toads have been present for more than 70 years. How can goannas coexist with toads there, but not at the invasion front? John showed that goannas around Townsville refuse to eat toads (but readily eat frogs), and that behaviour enables the lizards to survive. On a nearby island where toads are absent, the goannas readily tried to eat toads. So, it looks like the goannas in Queensland have dealt with the toad invasion by evolving (or learning) an ability to ignore toads.
Shine, R. 2014. A review of ecological interactions between native frogs and invasive cane toads in Australia. Austral Ecology 39:1-16.
Common sense suggests that cane toad invasion will be bad news for native frogs –but the evidence shows otherwise. Although cane toads can eat frogs, and compete with them for food, and transmit parasites to them, these negative effects are outweighed by positive advantages. For example, toads fatally poison a lot of predators that usually eat frogs. The end result is that extensive surveys, by several different research groups, have all reached the same conclusion – cane toad invasion has no detectable effect on native frog populations.
Pearson, D. J., M. J. Greenlees, B. L. Phillips, G. S. Bedford, G. P. Brown, J. Thomas, and R. Shine. 2014. Behavioural responses of reptile predators to invasive cane toads in tropical Australia. Austral Ecology 39:448-454.
The native species that are badly impacted by cane toads are those that try to eat toads, and cannot tolerate the toads’ poison. The most reliable way to work out whether a species is vulnerable is to put it in a cage with a toad, and see what happens. We tested many native species, using specimens that had been collected for faunal surveys, and would be euthanased and preserved anyway. We found complex responses; larger species were at more risk, and some groups were at more risk than others.
Greenlees, M. J., M. R. Crossland, and R. Shine. 2014. Larval interactions with an invasive species (the cane toad Rhinella marina) affect life-history traits in an Australian anuran (the marbled frog Limnodynastes convexiusculus). Australian Zoologist 36:424-428.
Tadpoles of the marbled frog develop into smaller metamorphs if they encounter cane toad larva. Smaller size would normally be a disadvantage but in this case it is not. Smaller frogs are less likely to try to eat toxic baby toads.
Pizzatto, L., C. Both, and R. Shine. 2014. Quantifying anuran microhabitat use to judge the potential for parasite transmission between invasive cane toads and two species of Australian native frogs. PLoS One 9:e106996.
Sometimes, the worst impact of an invading species comes from the parasites it brings with it from its native home. A new type of parasite can be devastating. That’s the case with a lungworm that cane toads brought to Australia. Most native frogs are not affected by it, but at least one species dies if it is infected. The magnificent treefrog is a large animal, bright green with white flecks. As its name suggests, it’s magnificent. Our lab studies showed that the frog is very sensitive to the toad lungworms. Ligia and Camila conducted a radio-tracking study in the field, near Kununurra in the Kimberley, to see how likely it was for toads and treefrogs to come into contact – and so, spread the parasite. They found that overlap is fairly small – enough to be a problem for some treefrogs, but probably not enough to endanger the entire species.
Cabrera-Guzman, E., M. R. Crossland, D. Pearson, J. K. Webb, and R. Shine. 2015. Predation on invasive cane toads (Rhinella marina) by native Australian rodents. Journal of Pest Science 88:143-153.
Despite what many people say, some native Australian animals can tolerate the poisons of the cane toad without ill effect. So, the arrival of the toad means extra food, not a death sentence. Australia has many native rats and mice, and we showed that several species – including the introduced rats in our cities – love to eat toads for breakfast, lunch and dinner.
Cane toad research photo credits: Christa Beckmann, Haley Bowcock, Greg Brown, Elisa Cabrera-Guzman, Travis Child, Michael Crossland, Matthew Greenlees, Mattias Hagman, Crystal Kelehear, John Llewelyn, David Nelson, Stephanie O'Donnell, Ben Phillips, Ligia Pizzatto, Sam Price-Rees, Cathy Shilton, Ruchira Somaweera, Peter Street, Georgia Ward-Fear, Jonathan Webb