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The biology of cane toads
Hagman, M., and R. Shine. 2006. Spawning-site selection by feral cane toads (Bufo marinus) at an invasion front in tropical Australia. Austral Ecology 31:551-558.
Although many people say that toads will breed anywhere, it’s not true. Toads actively select breeding sites that are shallow ponds with long shallow edges and open ground (not thick vegetation) around the water’s edge. This may be helpful if you don't want toads to breed in your backyard pond; just make sure it has steep sides and lots of thick grass growing up to the water's edge.
Semeniuk, M., F. Lemckert, and R. Shine. 2007. Breeding-site selection by cane toads (Bufo marinus) and native frogs in northern New South Wales. Wildlife Research 34:59-66.
Because we had earlier found that toads in Kakadu actively selected particular types of ponds to lay their eggs (an obviously important issue for management, and for discouraging toad breeding), we repeated this study at the other end of the toads’ Australian range, in northeastern New South Wales. Mark found exactly the same kinds of patterns that Mattias had revealed from the Kakadu study, a very encouraging result. It seems like toads are picky about where they breed, all across Australia. Also, the toads tended to like spots quite different from those used by most of the local frogs.
Urban, M., B. L. Phillips, D. K. Skelly, and R. Shine. 2007. The cane toad's (Chaunus marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proceedings of the Royal Society B 274:1413-1419.
How far will toads eventually spread through Australia? To predict this, Mark Urban and Dave Skelly from Yale University joined forces with us to model toad distributions. The analysis suggested that toads may be adapting to Australian climates, and hence may occupy a much larger area of the continent than was originally thought. However, like all models, treat this one with healthy scepticism: other models give different results. The important point is to recognise that it not safe to assume that toads are only a problem in tropical Australia; even if you live in Sydney, they may soon be coming to a pond near you!
Hagman, M., and R. Shine. 2008. Understanding the toad code: behavioural responses of cane toad (Chaunus marinus) larvae and metamorphs. Austral Ecology 33:37-44.
Cane toads are only distantly related to Australian frogs, so perhaps they use different ways to communicate with each other? For example, lots of toad species from around the world send chemical messages to each other when they are attacked by predators. If we can work out those pathways, we might be able to influence cane toads without affecting Aussie frogs. Mattias showed that the tadpoles of cane toads do indeed use such alarm pheromones, and in other work we show that Aussie frogs don't react to them. So perhaps we can use these chemicals to drive toad tadpoles or metamorphs away from their favoured habitats, to places where they are less likely to survive.
Hagman, M., and R. Shine. 2008. Deceptive digits: the functional significance of toe-waving by cannibalistic cane toads (Chaunus marinus). Animal Behaviour 75:123-131.
Cane toads have been studied very intensively, so you don't really expect to see too many "new" behaviours that haven't already been described by other researchers. But Mattias noticed that when he fed his captive toads, they often started to wriggle the longest toes on their back feet - as if it was a lure to attract prey items. We know from field studies that bigger toads sometimes eat large numbers of smaller toads. Sure enough, we found that smaller toads were attracted to the "lure". We built an artificial toe, put it beside a freeze-dried toad, and looked at how effectively we could attract baby toads with it. The colour and movement rates of the REAL toes were ideal for attracting smaller toads to the cannibals. This behaviour is very specialised, and suggests that cannibalism may actually be a fairly important issue in the life of cane toads. One idea we are investigating at present is whether we can exploit this tendency to help use toads to control their own numbers.
Child, T., B. L. Phillips, G. P. Brown, and R. Shine. 2008. The spatial ecology of cane toads (Bufo marinus) in tropical Australia: why do metamorph toads stay near the water? Austral Ecology 33:630-640.
Travis did this study as part of his Honours year. He measured the conditions around ponds in both the wet-season and the dry-season, and looked at where the smallest toads (metamorphs, that are the first stage after the tadpole) are found. It looks as though the grass is greener for a young toad further away from water (there are more bugs to eat, and less chance that your older brother or cousin will try to eat you) but for much of the year, it's simply too dry out there. So, the young toads hang out beside the pond until it rains.
Bowcock, H., G. P. Brown, and R. Shine. 2008. Sexual communication in cane toads (Chaunus marinus): what cues influence the duration of amplexus? Animal Behaviour 75:1571-1579.
Prior to spawning, male frogs grab hold of females and stay attached until the female is ready to release her eggs. This can sometimes take days or even weeks, during which time the male clings to the female's back like a small warty jockey. Females are heavily burdened by such a male, and would benefit by convincing him to let go - but they don't seem able to do this. Male toads often grab each other by accident, and CAN convince the other male to let go by giving a special "release call". Females don't have the same kinds of vocal cords as males, because they don't have to give the loud "advertisement calls". Because they are mute, they aren't able to talk the male into letting go. This may actually end up being useful to know for control purposes - because female toads often drown if they are grabbed by more than one male at the same time, and are in deep water where they can't stay afloat.
Hagman, M., and R. Shine. 2008. Australian tadpoles do not avoid chemical cues from invasive cane toads (Bufo marinus). Wildlife Research 35:59-64.
We've shown that chemical substances from injured or crushed toad tadpoles frighten other toad tadpoles. This might be helpful for toad control, if we can force toad tadpoles into particular areas of the pond and so forth. But obviously, we need to make sure that we are not also stressing the tadpoles of native frogs. So - we exposed native tadpoles to the toad's "alarm pheromone". Fortunately, they don't seem to be at all worried by it - unlike the toads.
Child, T., B. L. Phillips, and R. Shine. 2008. Abiotic and biotic influences on the dispersal behaviour of metamorph cane toads (Bufo marinus) in tropical Australia. Journal of Experimental Zoology 309A:215-224.
When cane toads transform from aquatic life (as tadpoles) to terrestrial life (as miniature toads), they are really tiny. This makes them very vulnerable to drying out, or to attack from predators (the tiny toads have less poison than their bigger relatives). So, this "metamorph" stage is perhaps an Achilles Heel - a time in their life when toads are especially vulnerable to control efforts. Understanding where they live at this time, and why they move around to different areas, might help to target these baby toads in our efforts at control. So Travis set up a set of laboratory arenas where he changed aspects like temperature, moisture levels and so forth, to study effects on the baby toads' movements. We found that the young cane toads prefer moist sites, but are deterred from entering such places if a larger cannibal toad is present.
Pizzatto, L. and R. Shine. 2008. The behavioral ecology of cannibalism in cane toads (Bufo marinus). Behavioral Ecology and Sociobiology 63:123-133.
Adult cane toads and tiny little metamorphs mostly eat insect prey, but there's a dark side to the dietary habits of intermediate-sized (juvenile) toads. During the long dry-season when baby toads are restricted to the edge of the pond, and there's not much insect life out in the drier areas, the larger juvenile toads hang around the pond and feed mostly on their smaller brethren. About two-thirds of their diet consists of smaller toads. We recorded behaviours and distributions and numbers of the cannibals and their prey, and ran some simple experiments like dangling dead metamorph toads in front of larger toads to record feeding responses. It's very clear that any tiny toad that moves near the pond's edge at night is very likely to end up inside a larger toad's stomach!
Pizzatto, L., T. Child, and R. Shine. 2008. Why be diurnal? Shifts in activity time enable young cane toads to evade cannibalistic conspecifics. Behavioral Ecology 19:990-997.
Like most species of frogs, adult cane toads move around mostly at night - they spend the day tucked away in a safe shelter. But the tiny little metamorph toads are active by day - which seems very peculiar, since they are at risk of overheating, drying out or being grabbed by a predator at that time. Our experiments show that there is a huge benefit to this daytime activity - the young toads can thereby avoid their older cousins, who otherwise are very happy to eat them.
Dubey, S., and R. Shine. 2008. Origin of the parasites of an invading species, the Australian cane toad (Bufo marinus): are the lungworms Australian or American? Molecular Ecology 17:4418-4424.
Cane toads in Australia often have nematode worms in their lungs, and we know from other work (by Crystal Kelehear) that the worms severely affect small toads. Where did the worms come from? They might be species that evolved in Aussie frogs and have switched across to toads; or they might have come from South America with the toads. It's hard to identify nematodes by looking at them (most look very similar) so we analysed genetic material - DNA sequences - to work out what species they were. To everybody's surprise, the worms turned out to be toad-specific South American worms - so must have come to Australia with the original toads in 1935.
Crossland, M. R., G. P. Brown, M. Anstis, C. Shilton, and R. Shine. 2008. Mass mortality of native anuran tadpoles in tropical Australia due to the invasive cane toad (Bufo marinus). Biological Conservation 141:2387-2394.
We hear a lot about cane toads poisoning native snakes and lizards, and sometimes quolls, crocodiles and so forth - but nobody seems to have thought about native tadpoles. We found lots of dead native tadpoles in the waterbodies whenever toads bred in the study area; and so ran a series of trials to work out why. It turns out that most native tadpoles readily try to eat toad eggs, and the powerful poisons inside the egg are almost immediately fatal. So, most of the toads' Australian victims are tadpoles, not other vertebrates. Fortunately, tadpole numbers are so high that this mortality has very little effect on the abundance of native frogs.
Hagman, M., and R. Shine. 2008. Tadpoles of invasive cane toads (Bufo marinus) do not respond behaviourally to chemical cues from tadpoles of four species of Australian frog. Australian Journal of Zoology 56:211-213.
As part of our wide-ranging studies on the toads' alarm pheromone, we checked to see if the toad tadpoles also react to similar chemicals from Aussie frogs. They don't, confirming that the toads speak a different chemical "language" than do tadpoles of native frog species in Australia.
Hagman, M., R. Hayes, R. Capon, and R. Shine. 2009. Alarm cues experienced by cane toad tadpoles affect post-metamorphic morphology and chemical defences. Functional Ecology 23:126-132.
Cane toad tadpoles produce special chemicals when they are frightened or injured; and those chemicals cause other toad tadpoles to flee. Continued exposure to this "alarm pheromone" causes the toad tadpole to transform into an unusually small metamorph; and our analyses show that these little toads produce different poisonous chemicals than do their brothers and sisters that have not been exposed to the alarm pheromone.
Child, T., B. L. Phillips, and R. Shine. 2009. Does desiccation risk drive the distribution of metamorph cane toads (Bufo marinus) in tropical Australia? Journal of Tropical Ecology 25:193-200.
Soon after they transform from tadpoles, baby toads accumulate in high densities around the pond from which they emerged. This is especially true in the dry-season rather than the wet-season, suggesting that the little toads are restricted to the moist edges of the pond because they would dry out and die if they moved out into the wider drier world. We tested this idea in several ways, such as by wetting the ground around some sections of the pond; and sure enough, it is clear that risk of drying-out is a major determinant of the baby toad's distribution at this time of year.
Bowcock, H., G. P. Brown, and R. Shine. 2009. Beastly bondage: the costs of amplexus in cane toads (Bufo marinus). Copeia 2009:29-36.
When they are about to breed, male toads seize female toads and ride them around, clinging to the female's back. We measured the effects of that posture on the ability of male and female toads to move, swim and hop rapidly, stay afloat in the water, and so forth. It's clear that females are at substantial risk, and face substantial costs, when they are forced to carry a male around.
Hagman, M., and R. Shine. 2009. Factors influencing responses to alarm pheromones by the larvae of invasive cane toads (Bufo marinus). Journal of Chemical Ecology 35:265-271.
Before we can use larval alarm pheromones to help control cane toads (by killing some tadpoles, and dwarfing the surviving metamorphs), we need to know where and when to expose the tadpoles to these chemicals. Fortunately, our trials show that factors such as time of day and tadpole age have very little effect on how a toad tadpole responds to the alarm chemical. This should make it easier to use the pheromone for toad control.
Ward-Fear, G., G. P. Brown, M. Greenlees, and R. Shine. 2009. Maladaptive traits in invasive species: in Australia, cane toads are more vulnerable to predatory ants than are native frogs. Functional Ecology 23:559-568.
We often see native meat ants killing and eating baby cane toads, especially during the dry-season when the little toads are concentrated on the edges of ponds. Georgia conducted laboratory trials to find out why toads are so much more vulnerable to meat ants than are native frogs. She found that native frogs generally avoid places where the ants forage; and move away if they see an ant coming; and jump away if seized. In contrast, cane toads are active in open areas by day, don't avoid ants, and often just sit still when seized and let the ants tear them apart. We are investigating whether we might be able to exploit this situation to help reduce cane toad numbers.
Hagman, M., and R. Shine. 2009. Species specific communication systems in invasive toads versus Australian frogs. Aquatic Conservation 19:724-728.
We have shown that the alarm pheromone can be used to kill toad tadpoles and dwarf the survivors - but clearly, we can't use this chemical to control toads if it also affects native frogs. Fortunately, our tests on a range of native frogs suggest that most of them don't even detect the pheromone, let alone become stressed by it.
Hayes, R. A., M. R. Crossland, M. Hagman, R. J. Capon, and R. Shine. 2009. Ontogenetic variation in the chemical defences of cane toads (Bufo marinus): toxin profiles and effects on predators. Journal of Chemical Ecology 35:391-399.
Many people say that "all toads are toxic" - but nobody had ever actually measured the amount of poison in toads of different ages and sizes. We did so, in collaboration with biochemists, and found that the amounts and types of poisons in the toad change dramatically as it gets bigger. Eggs have lots of poison, as do bigger toads. The amounts are smaller in older tadpole stages and especially low around about the time of metamorphosis. This strongly affects the danger that these stages pose to predators.
Saunders, G., B. Cooke, K. McColl, R. Shine, and T. Peacock. 2010. Modern approaches for the biological control of vertebrate pests: an update on Australian research. Biological Control 52:288-295.
This paper reviews attempts to control vertebrate pests in Australia; Rick wrote the section on cane toads.
González-Bernal, E., G. P. Brown, E. Cabrera-Guzmán, and R. Shine. 2011. Foraging tactics of an ambush predator: the effects of substrate attributes on prey availability and predator feeding success. Behavioral Ecology and Sociobiology 65:1367-1375.
Edna conducted trials out in the field, looking at how toads’ feeding success is affected by the colour and roughness of the ground they are sitting on. Understanding how and why toads can feed more effectively in some places than others can tell us quite a lot about why toads succeed in some areas and fail to thrive in others.
Llewellyn, D., G. P. Brown, M. B. Thompson, and R. Shine. 2011. Behavioral responses to immune system activation in an anuran (the cane toad, Bufo marinus): field and laboratory studies. Physiological and Biochemical Zoology 84:77-86.
Brown, G. P., C. Shilton, and R. Shine. 2011. Measuring amphibian immunocompetence: validation of the phytohemagglutinin skin-swelling assay in the cane toad, Bufo marinus. Methods in Ecology and Evolution 2:341-348.
One of the exciting results from our earlier work was the discovery that invasion-front toads may have weak immune systems. This would make them potentially vulnerable to control methods that affect their immune responses. So we’ve embarked on field and lab studies to find out exactly what happens when a toad gets infected; and how we can most accurately measure the toads’ immune system capacity.
Amiel, J. J., R. Tingley, and R. Shine. 2011. Effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS ONE 6:e18277.
Tingley, R., B. L. Phillips, and R. Shine. 2011. Establishment success of introduced amphibians increases in the presence of congeneric species. American Naturalist 177:382-388.
Why have toads been such successful invaders? One way to work this out is to look at other species that haven’t succeeded. These two papers look at information on a wide range of species that have been introduced (by people) to places outside their native range. It turns out that invaders do better if the area they are brought to contains species that are their close relatives, and that species with larger brains tend to be more successful. Toads don’t fit these general patterns very well, which gives us all kinds of opportunities to ask why.
Kolbe, J. J., M. Kearney, and R. Shine. 2010. Modeling the consequences of thermal trait variation for the cane toad invasion of Australia. Ecological Applications 20:2273-2285.
One of the most amazing things about the toad invasion of Australia is that a frog that evolved in the Brazilian rainforest has been able to colonize the driest continent on earth. How do toads deal with conditions that are drier and colder than in their native range? Jason tested the ability of toads to deal with low temperatures. As you might guess, Cairns toads were not as good at dealing with cold as were toads from further south – but after a few weeks in the lab under cool conditions, even the Cairns toads became much more adept at moving about when it was cold. This adaptability is a key reason for the toads’ success in Australia.
Phillips, B. L., G. P. Brown, and R. Shine. 2010. Life-history evolution in range-shifting populations. Ecology 91:1617-1627.
Most conventional ecological theory is based on a simplifying assumption – that populations are in spatial equilibrium. This means that the species’ range is constant, not expanding or contracting. Clearly, this isn’t true for invading species like cane toads. Ben’s mathematical models, and our data on toads, show that lots of evolutionary forces are modified if a species is expanding its range.
Llewelyn, J., B. L. Phillips, R. A. Alford, L. Schwarzkopf, and R. Shine. 2010. Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area. Oecologia 162:343-348.
How do cane toads from the invasion front manage to move so much further every night than toads from Queensland? John ran toads from both areas along a raceway, and found that the invasion-front toads have much higher stamina. They just kept on going, long after the Queenslanders had given up.
Tingley, R., C. M. Romagosa, F. Kraus, D. Bickford, B. L. Phillips, and R. Shine. 2010. The frog filter: amphibian introduction bias driven by taxonomy, body size, and biogeography. Global Ecology and Biogeography 19:496-503.
Although our toad work stimulated this study, it’s actually a much broader look at what kinds of frog and salamander species have succeeded in establishing invasive populations. It turns out that whether or not an introduced frog succeeds in its new home depends upon what group it belongs to, how big it is, and where it came from.
Phillips, B. L., G. P. Brown, and R. Shine. 2010. Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads. Journal of Evolutionary Biology 23:2595-2601.
Toads move a lot faster at the invasion front than further back in areas colonized long ago. Is this because the Northern Territory is an easier place to move through than Queensland, or is it because the toads themselves have evolved to be better at dispersal? Ben raised the offspring of toads from a series of areas, and showed that the baby toads inherit their parents’’ dispersal rate. Thus, the acceleration of the toad invasion is a genuine case of evolutionary change in the toads.
Bruning, B., B. L. Phillips, and R. Shine. 2010. Turgid female toads give males the slip: a new mechanism of female mate choice in the Anura. Biology Letters 6:322-324.
In this paper, we pry into the sex lives of toads. At first sight, it doesn’t seem like a female toad can do much to choose which male she mates with – he just grabs her and hangs on until she starts producing eggs. But Bas showed that in fact, the girls are not powerless. They can inflate their bodies with air, making it harder for the males to hang on – and so, a female toad may be able to exchange an unwanted boyfriend for one she prefers.
Tingley, R., and R. Shine. 2011. Desiccation risk drives the spatial ecology of an invasive anuran (Rhinella marina) in the Australian semi-desert. PLoS One 6:e25979.
In areas of central Queensland around Longreach, cane toads are invading incredibly dry inhospitable country. Reid’s radio-tracking confirms that the toads move about in ways that give them access to water, creating distinctive patterns in the timing and location of toad activity.
Brown, G. P., C. Kelehear, and R. Shine. 2011. Effects of seasonal aridity on the ecology and behaviour of invasive cane toads (Rhinella marina) in the Australian wet-dry tropics. Functional Ecology 25:1339-1347.
How can a frog species from the Brazilian rainforest invade the driest continent on Earth? Our study area near Darwin has a short wet-season (somewhat like the conditions that occur year-round in the toads’ native range) and a long dry-season. By comparing toad ecology in those two seasons, we show that toads flexibly adjust their activity levels to prevailing conditions, and thus have no real problem in waiting out the bad times. They are incredibly flexible and resourceful animals!
Tingley, R., M. J. Greenlees, and R. Shine. 2012. Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone. Oikos 121:1959-1965.
Our measurements of water balance and activity show that toads from the Queensland semi-arid region exhibit different patterns of water permeability of the skin, and different behavioural responses to desiccation, than do toads from the wet-dry tropics. For example, the semi-desert toads will keep moving even after they are strongly desiccated - enhancing their survival in the harsh desert conditions. Toads are adaptable!
Graham, S. P., C. Kelehear, G. P. Brown, and R. Shine. 2012. Corticosterone-immune interactions during captive stress in invading Australian cane toads (Rhinella marina). Hormones and Behavior 62:146-153.
This paper looks at the immune systems of toads, to help us understand what happens physiologically when a toad encounters an infective agent.
Gonzalez-Bernal, E., M. Greenlees, G. P. Brown, and R. Shine. 2012. Cane toads on cowpats: commercial livestock production facilitates toad invasion in tropical Australia. PLOS One 7:e49351.
Livestock grazing activities cover a lot of tropical Australia, and several results of farming have made it easier for toads to invade. The provision of water sources (dams) during the dry season is the most important effect, but Edna’s experiments showed that toads also actively seek out cowpats (faeces piles); and that they can gain water by sitting on the moist surfaces. So, the abundance of cattle and buffalo faeces is a useful resource for cane toads.
Pizzatto, L., Kelehear, C., and R. Shine. 2013. Seasonal dynamics of the lungworm, Rhabdias pseudosphaerocephala, in recently colonised cane toad populations in tropical Australia. International Journal for Parasitology 43:753-761.
Ligia and Crystal surveyed the numbers of lungworms in cane toads in a variety of sites. They found many non-random patterns. One interesting bias is that lungworm infection rates were highest during the dry season, probably because toads aggregate in the few moist retreats that are available at that time, and so parasites are easily passed from one toad to another. It is harder for a lungworm to find a new host during the wet-season, when toads are widely dispersed.
Gonzalez-Bernal, E., G. P. Brown, and R. Shine. 2014. Invasive cane toads: social facilitation depends upon an individual's personality. PLoS One: in press.
Like humans, individual toads have personalities. Some are shy, some are bold. That variation may affect the way a toad population invades a new area. Edna set out lights at night to attract bugs (and thus, hungry toads). Some wild toads would only come to a light if there was another toad already there; and later trials in the lab showed that these were consistently shy animals. Other toads would feed alone at a light; these proved to be bolder.
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