Shine Lab

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Scientific Publications

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Cane toad control

Phillips, B. L., C. Kelehear, L. Pizzatto, G. P. Brown, D. Barton, and R. Shine. 2010. Parasites and pathogens lag behind their host during periods of host range-advance. Ecology 91:872-881.

By dissecting hundreds of cane toads, we found that the lung parasite Rhabdias pseudosphaerocephala is lacking from the invasion-front populations. It takes a few years to catch up, probably because the worms slow toads down.

Rhabdius in toad lung

Kelehear, C., J. K. Webb, and R. Shine. 2009. Rhabdias pseudosphaerocephala infection in Bufo marinus: lung nematodes reduce viability of metamorph cane toads. Parasitology 136:919-927.

Kelehear, C., G. P. Brown, and R. Shine. 2011. Influence of lung parasites on growth rates of free-ranging and captive adult cane toads. Oecologia 165:585-592.

These studies examine the effect of the lung parasite Rhabdias pseudosphaerocephala (a nematode worm) on tiny metamorph toads in the laboratory and on much larger adult toads both in the lab and the field. In each case, the worms have strong negative effects on the toads. This is encouraging for using worms for toad control, but we have to be sure that the worms won’t also affect native frogs. We’ve been looking at this also (see Ligia’s papers on the “impact” page).

             

Pizzatto, L., and R. Shine. 2011. You are what you eat: parasite transfer in cannibalistic cane toads. Herpetologica 67:118-123.

We show that the highly cannibalistic habits of medium-sized cane toads can result in them becoming infected with the lung parasite. This could be really useful for control, because it’s these large surviving toads that we need to target.

cannibal toads


Ward-Fear, G., G. P. Brown, and R. Shine. 2010. Using a native predator (the meat ant, Iridomyrmex reburrus) to reduce the abundance of an invasive species (the cane toad, Bufo marinus) in tropical Australia. Journal of Applied Ecology 47:273-280.

Ward-Fear, G., G. P. Brown, and R. Shine. 2010. Factors affecting the vulnerability of cane toads (Bufo marinus) to predation by ants. Biological Journal of the Linnean Society 99:738-751.

             

 


Somaweera, R., N. Somaweera, and R. Shine. 2010. Frogs under friendly fire: how accurately can the general public recognize invasive species? Biological Conservation 143:1477-1484.

Our surveys of the general public at shopping centres in Darwin were designed to find out how good people are at telling the difference between frogs and cane toads. The answer is that most people are really not able to do this very well. One result is that – especially in areas where toads are scarce, or haven’t yet invaded – we should encourage people to have any “toad” identification checked by an expert. Otherwise, a lot of people will be killing native frogs in mistake for toads.

Litoria rothii


Shine, R., and J. S. Doody. 2011. Invasive-species control: understanding conflicts between researchers and the general community. Frontiers in Ecology and the Environment 9:400-406.

Sean and I wrote this paper after we attended a community meeting in Kununurra. We explore why researchers seem to end up disagreeing so often with community leaders, and conclude that it’s almost inevitable given the different pressures that the two groups are under. Scientists can afford to just try to work out what is going on, but community leaders are in a political situation where their support and funding depend upon providing simple and encouraging messages to their supporters.


Hagman, M., and R. Shine. 2009. Larval alarm pheromones as a potential control for invasive cane toads (Bufo marinus) in tropical Australia. Chemoecology 19:211-217.

             



Crossland, M. R., and R. Shine. 2011. Cues for cannibalism: cane toad tadpoles use chemical signals to locate and consume conspecific eggs. Oikos 120:327-332.

toad tadpoles eating toad eggs


Crossland, M. R., M. N. Hearnden, L. Pizzatto, R. A. Alford, and R. Shine. 2011. Why be a cannibal? The benefits to cane toad (Rhinella marina) tadpoles of consuming conspecific eggs. Animal Behaviour 82:775-782.

These two papers look at a fascinating behaviour that Michael discovered. Toad tadpoles are highly cannibalistic, and use chemical substances produced by toad egg masses to find and destroy those new eggs. If we can work out the specific chemicals involved, we might have a terrific toad-specific “bait” with which to trap toad tadpoles – without affecting the tadpoles of native frogs.

           

Cabrera-Guzmán, E., M. R. Crossland, and R. Shine. 2011. Can we use the tadpoles of Australian frogs to reduce recruitment of invasive cane toads? Journal of Applied Ecology 48:462-470.

Elisa’s laboratory experiments show that toad tadpoles are poor competitors, and experience reduced survival and growth if they have to develop in the same container as Australian native frogs. So, by encouraging frogs to breed in the ponds usually used by toads (or by adding frog tadpoles to those ponds), we can make life a lot harder for the invasive toad. The much-loved Green Tree Frog turns out to be the most effective anti-toad species.


Kelehear, C., J. K. Webb, M. Hagman, and R. Shine. 2011. Interactions between infective helminth larvae and their anuran host. Herpetologica 67:378-385.

Our behaviour studies show exactly how larval lungworm parasites enter the bodies of cane toads (mostly across the eyeball), and whether or not toads have effective strategies to avoid the parasites (they don’t).


Price-Rees, S., J. K. Webb, and R. Shine. 2011. School for skinks: Can conditioned taste aversion enable bluetongue lizards (Tiliqua scincoides) to avoid toxic cane toads (Rhinella marina) as prey? Ethology 117:749-757.

In the laboratory, we show that bluetongue lizards – a species that is imperiled by cane toad invasion – is capable of learning to recognise and avoid toads as prey.


Crossland, M. R., and R. Shine. 2012. Embryonic exposure to conspecific chemicals suppresses cane toad growth and survival. Biology Letters 8:226-229.

For a tadpole cane toad, the worst thing that can happen is for a female toad to lay her eggs in your pond – you will soon have to compete for food with thousands of younger tadpoles. Remarkably, toad tadpoles have developed a chemical weapon to reduce this threat – they produce chemicals that alter the development of the younger tadpoles, so that many of them die before finishing the tadpole stage. If we knew what this chemical was (and we don’t, unfortunately), we might be able to use it to help reduce cane toad tadpole survival.


Beckmann, C., and R. Shine. 2012. Do drivers intentionally target wildlife on roads? Austral Ecology 37:629-632.

Lots of drivers say they intentionally run over cane toads, but do they really? When Christa put out model toads and frogs and snakes on the road, drivers actually ran over all three types of animals (and other objects) at about the same rate. It is probably a good thing that people don't usually try to run over toads, because it can be difficult to tell a toad from a native frog at night when you're travelling at 100 km/hour!



Pizzatto, L., and R. Shine. 2012. Lungworm infection modifies cardiac response to exercise in cane toads. Journal of Zoology 287:150-155.

Ligia showed that cane toads that were infected with lungworms had different heartbeat rates than uninfected toads, giving us some clues as to how the lungworm actually affects toad physiology.


Kelehear, C., G. P. Brown, and R. Shine. 2012. Size and sex matter: infection dynamics of an invading parasite (the pentastome Raillietiella frenatus) in an invading host (the cane toad Rhinella marina). Parasitology 139:1596-1604.

Most of our parasite work has been with a nematode lungworm. Crystal found a different type of lungworm in invasive cane toads, and this paper shows that whether or not a toad is infected depends upon its body size (midsize toads are most vulnerable) and sex (male toads are most vulnerable).


Kelehear, C., E. Cabrera-Guzman, and R. Shine. 2012. Inadvertent consequences of community-based efforts to control invasive species. Conservation Letters 5:360-365.

Many people have put enormous effort into collecting and killing toads. In this paper we looked at the possibility that such efforts might have unintended collateral effects. For example, it seems that toad-busting activities can result in people accidentally transporting lungworm parasite larvae in wet mud on their boots, from one site to another. That process probably has moved the parasite to toad populations much earlier than would have occurred by natural processes. In another example, spraying the edges of ponds with disinfectant to kill baby toads discourages meat ants from spending time in those areas, so may have driven away native species that otherwise would have killed the baby toads. This doesn’t mean that people should stop toad-busting – it just means that we need to think carefully about exactly what we are doing, and what unintended effects we might be having on processes that influence toad numbers.


Pizzatto, L., and R. Shine. 2012. Typhoid Mary in the frogpond: can we use native frogs to disseminate a lungworm biocontrol for invasive cane toads? Animal Conservation 15:545-552.

Green Tree Frogs often breed in the same ponds as cane toads, and Ligia found that they can take up the type of lungworm that normally is only found in toads. They don’t normally take up the parasite in the field however; and although the parasite can kill toads, it doesn’t seem to affect the frogs. In this study, she showed that infected frogs are not badly affected by having the lungworm, and can continue to produce infective larvae in large numbers for long periods. So, one way to build up numbers of the toad-killing parasite might be to use Green Tree Frogs as a host.

green tree frog


Cabrera-Guzman, E., M. R. Crossland, and R. Shine. 2012. Predation on the eggs and larvae of invasive cane toads (Rhinella marina) by native aquatic invertebrates in tropical Australia. Biological Conservation 153:1-9.

Elisa showed that several species of water-bugs and water-beetles like to eat the tadpoles of cane toads – in fact, they prefer them to native tadpoles. So, declines in toad abundance in the years after toads arrive at a site might be due, at least partly, to increases in the numbers of predatory insect. The native insects may play an important role in controlling toad numbers.



Pizzatto, L., C. Kelehear, S. Dubey, D. Barton, and R. Shine. 2012. Host-parasite relationships during a biological invasion: 75 years post-invasion, cane toads and sympatric Australian frogs retain separate lungworm faunas. Journal of Wildlife Diseases 48:951-961.

When cane toads were brought to Australia in 1935, they brought with them a nematode lungworm parasite from their native range in South America. If the parasite switched to infecting native frogs, it could be a disaster. However, the news is good. Our surveys of frogs and toads, across the entire range of toads in Australia, shows that the “toad parasite” seems to be only found in toads – we never found it in frogs. Instead, native frogs have a series of species of lungworms that are related to the toad lungworm, but are not the same species.



Crossland, M. R., T. Haramura, A. A. Salim, R. J. Capon and R. Shine. 2012. Exploiting intraspecific competitive mechanisms to control invasive cane toads (Rhinella marina). Proceedings of the Royal Society B 279:3436-3442.

We can’t control cane toads by simply collecting and removing adults, because toads produce so many eggs (30,000 per clutch) that even a few remaining adult toads can repopulate an area very quickly. Somehow, we have to stop toads reproducing. In collaboration with chemists from the University of Queensland, Michael discovered that toad tadpoles are strongly attracted to a chemical that is produced by toad eggs. That chemical proved to be the toads’ poison. When we used the poison as “bait” in funnel-traps in natural waterbodies, we rapidly caught tens of thousands of toad tadpoles – and almost nothing else. So, our research has revealed a new weapon against the toads. If community groups or wildlife management authorities really want to stop toads breeding in a local area, they now have a way to do it. We think this is one of the most exciting results to emerge from TeamBufo’s research, and we are looking for more funding to continue the work.

Watch ABC News interview with Rick

 


Price-Rees, S. J., J. K. Webb, and R. Shine. 2013. Reducing the impact of a toxic invader by inducing taste-aversion in an imperilled native reptile predator. Animal Conservation 16:386-394.

We have successfully taught northern quolls not to eat cane toads, by exposing them to small toads that make them sick. Those quolls are then able to survive after we release them, because they don’t try to eat toads. Sam tried the same trick with another endangered predator, the bluetongue skink. She showed that taste-aversion training successfully increased survival rates of lizards in the wild, after toads arrived at her study site near Kununurra.


Cabrera-Guzman, E., M. R. Crossland, and R. Shine. 2013. Competing tadpoles: Australian native frogs affect invasive cane toads (Rhinella marina) in natural waterbodies. Austral Ecology: in press.

Elisa followed up her laboratory studies by raising cane toad tadpoles and native tadpoles in various combinations, in mesh containers within natural billabongs. She showed that cane toad tadpoles are suppressed by native tadpoles in nature, just as they are in the lab. So, encouraging native frogs to breed in a waterbody is a good way to make life difficult for toads.


Tingley, R., B. L. Phillips, M. Letnic, G. P. Brown, R. Shine, and S. Baird. 2013. Identifying optimal barriers to halt the invasion of cane toads Rhinella marina in northern Australia. Journal of Applied Ecology 50:129-137.

As cane toads spread west into drier and drier regions, their progress may be dependent on artificial waterbodies. Reid and Ben modelled the environment that toads are spreading into, and concluded that there may be an area where conditions are so dry that if we closed off the artificial water supplies, the toads would not be able to invade any further west. Whether or not this is actually feasible is currently under investigation; for example, occasional cyclones may be enough to provide a moist corridor that will allow toad spread.


Pizzatto, L., and R. Shine. 2013. New methods in the battle against cane toads: when should we move from research to implementation? Animal Conservation 15:557-559.

One of the big problems in tackling invasive species is the danger of collateral damage from our control efforts. At what point do we decide that the risks are worthwhile? There is no easy answer!


Cabrera-Guzman, E., M. R. Crossland, and R. Shine. 2013. Mechanisms of interspecific competition between the tadpoles of Australian frogs and of invasive cane toads (Rhinella marina). Freshwater Biology: in press.

Native tadpoles compete with toad tadpoles for food, so we might be able to use native tadpoles to help reduce the survival and growth of cane toad tadpoles. Elisa’s experiments showed that the competition is indeed all about a limited food supply, and the ability of native tadpoles to starve out the toad tadpoles.


Cabrera-Guzman, E., M. R. Crossland, E. Gonzalez-Bernal, and R. Shine. 2013. The interacting effects of ungulate hoofprints and predatory native ants on metamorph cane toads in tropical Australia. PLoS ONE: in press.

Agricultural activities are putting out “welcome” signs for invasive cane toads. One way this happens is that livestock create hoofprints in the soft mud by the edges of ponds. Those hoofprints provide moist cool retreat-sites for baby toads. But there are disadvantages too – the young toads can drown inside steep-sided hoofprints if heavy rain falls; and it may be harder for the toads to escape from predatory ants if they are attacked inside hoofprints.


Cabrera-Guzmán, E., M. R. Crossland, G. P. Brown, and R. Shine. 2013. Larger body size at metamorphosis enhances survival, growth and performance of young cane toads (Rhinella marina). PLoS ONE 8: e70121.

Several of the methods we are exploring for toad control involve stressing tadpoles – and thus, causing them to turn into toadlets at a smaller size than would otherwise be the case. Does this really affect their viability? Here, Elisa conducted studies in field enclosures to check out the long-term consequences of metamorphosing at small body sizes. She found that smaller toadlets are less likely to survive, and don’t grow as big as their siblings who metamorphose at larger sizes. This is an encouraging result for our toad-control studies.



Cabrera-Guzman, E., M. R. Crossland, D. Pearson, J. K. Webb, and R. Shine. 2014. Predation on invasive cane toads (Rhinella marina) by native Australian rodents. Journal of Pest Science: in press.

Although many people say that cane toads are deadly to all Australian predators, it’s simply not true. For example, rodents (rats and mice) are able to tolerate the toad’s poison, and eat them happily. Native and feral rats are major predators of Australian cane toads, and have played an important role in reducing the numbers of toads in many areas.


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