The origin of species: the Australian connection
Mr Toad comes to Darwin: An evolutionary perspective on the cane toad invasion
6 March 2007
Professor Rick Shine
ARC Federation Fellow
School of Biological Sciences
University of Sydney
Professor Shine led the way in the study of reptilian ecology and evolution. His work spans evolutionary theory through to population ecology and reproductive biology. His conceptual syntheses, empirical reviews, and original studies in both laboratory and field, have used reptilian diversity to attack many questions of general importance. His work has substantially clarified the ways in which microevolutionary processes determine major changes in life history.
The Shine Lab at the University of Sydney
www.bio.usyd.edu.au/Shinelab/index.html
Herpetology at the Australian Museum
www.austmus.gov.au/herpetology/index.htm
How snakes work
http://science.howstuffworks.com/snake.htm
Information on cane toads from the Northern Territory Government
www.nt.gov.au/nreta/wildlife/animals/canetoads/index.html
Introduction
Professor Kurt Lambeck: Thank you very much for coming along this evening, and welcome to this lecture, the fifth in our series on evolution. The lecture series explores how Australian materials have contributed to the development of Charles Darwin's ideas.
Tonight's speaker is Professor Rick Shine. Rick is from the University of Sydney, where he is Professor of Evolutionary Biology. But, as some of you would know, he also has a double career now: he is also a budding TV personality. Those of you who watched Catalyst last week will recall his to-ing and fro-ing with his big brother, Professor John Shine.
I think it is fair to say that Rick is Australia's foremost authority in reptilian ecology and evolution. He has established a laboratory at Sydney whose research on the behaviour, ecology and evolution of snakes, lizards, frogs and toads covers the entire range of environments of Australia and the adjacent offshore. Tonight he is going to talk about the cane toad invasion and how those, I guess, with the longest legs jump the furthest!
I call upon Rick to tell us about the cane toad invasion in Darwin and northern Australia. Thank you Rick.
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Professor Rick Shine: Thanks very much, Kurt, and thanks very much to the Academy for inviting me to speak this evening.
Tonight's talk is basically a continuation of a story that you are all very familiar with.
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The original version by Kenneth Grahame is entitled Wind in the Willows. It is a classic children's tale about delightful little creatures in the English countryside - Rat, Mole, Badger and so on - and the central creature is Mr Toad.
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Mr Toad is an extravagant creature with a penchant for wandering. He really wants to travel. Toad's great thing in life is to move around, go to places he's never been and get there as fast as he can.
Wind in the Willows was written almost 100 years ago, and presumably the original Mr Toad has long gone to the 'swamp in the sky'. But Mr Toad's descendants, particularly the American branch of the family, are continuing to spread and travel rapidly across the globe.
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Mr Cane Toad, from the Central and South American branch of the toad family, was introduced to Australia in 1935, as an attempt at biological control. And, as we all know, Mr Cane Toad and his relatives have been spreading across the Australian tropics ever since.
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In the process, they have encountered landscapes very different from the original landscapes of Central and South America.
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Along the way, they have met lots of new 'friends', some of whom don't care very much about Mr Toad's arrival. This photograph is unposed, believe it or not, with the toad sitting up towards the back of the picture. Mr Water Python doesn't actually care very much about Mr Toad.
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The Mosquito Sisters are more interested in Mr Toad - although, we recently found that cane toad invasion reduces mosquito numbers, so it's bad news for the Mosquito Sisters.
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Some of the locals are very unfriendly. Mrs Death Adder and Mr Toad have had a pretty nasty encounter here that has had nasty consequences for both of them.
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On the other hand, some of the locals are much more friendly. Mr Giant Burrowing Frog is very fond of Mrs Toad, and is expressing his affection.
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One of the more unusual beings that Mr Toad has encountered as he has reached the suburbs of Darwin is a group that calls itself 'Team Bufo': a bunch of biologists, ecologists and evolutionary biologists that are conducting a study at Fogg Dam and its environs on the Adelaide River flood plain.
I started the work about 25 years ago and it has been going ever since. We do a lot of the things that ecologists would do when faced with the opportunity to study a biological invasion: we want to find out what toads are doing and what impact they are having. So we catch toads, strap little waistbands around them with transmitters on them and follow them around.
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But the unusual part of my group's approach, which relates to the second part of my title, is that we also take an evolutionary perspective. So Mr Toad comes to Darwin in this sense as well. We are trying to explore the possibility that there are rapid evolutionary changes, both in the toads and in the native systems that they are impacting, that are relevant to the outcomes of the invasion. If that's the case, as conservation biologists we really want to know what's going on. If the native systems are really that dynamic, we need to incorporate that.
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At first sight, that sounds like complete nonsense. Conservation biology doesn't really deal with evolution, and the reason for this is simple: there is a general feeling that evolution is a very slow process. It is very good at explaining why dinosaurs evolve, but it is very bad at explaining anything about what happens when you cut a forest down. It seems that the conservation problems and challenges that we have are so urgent that there is no way that the living systems involved can adapt quickly enough for it to really matter.
So that's the critical issue: do we have to include evolutionary thinking when dealing with conservation challenges?
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From an evolutionary perspective, any conservation challenge is just another selective force. It's an extra source of mortality - if there are individuals in the population with genes that make them less vulnerable to the new source of mortality, those genes should increase in frequency relative to the others, and the system should adapt to deal with the new challenge.
So the question becomes: can it do it fast enough?
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The stakes are really high. I have included this photo because it is the only large snake that I have caught during the last several years, and this is what snake biologists like to do - show pictures of big snakes that they catch. I will use it to come up with an allusory example of a conservation challenge and why evolution matters.
Let's suppose that every time a bunch of drunken Territorians get together and have a dinner party, they decide that they will eat an olive python. (Territorians are unusual people, so it wouldn't shock me if this sort of caught on.) And let's say that this is happening at such a rate that olive python numbers are really declining, so that we have a genuine conservation issue here. In the absence of any other process coming in, olive python numbers are going to go down and down and down.
Suppose we just change that scenario slightly. Let's say there's a gene in the olive python population that says, 'If you smell mango daiquiris on people's breath, go and hide somewhere where they can't catch you.' Then we have a scenario where some olive pythons can't be caught by drunken Territorians - they hide and survive; the other pythons get eaten but the ones that survive set up a nucleus and eventually repopulate.
The critical thing is that the information we currently have with these two scenarios is basically identical: we have a new conservation challenge.
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Something has come in to an area - it could be global warming, an invasive species, a disease, habitat destruction, it could be anything you like - and it is killing lots of native animals.
Do we need to worry about that? What priority do we give it? If you follow my first scenario, where there is no adaptive response, it's right at the top of our list. We have to put a huge amount of resources into it - and resources are scarce. If you follow my second scenario and the system is capable of adapting to it, then we can pretty much forget about it. We'd like to try and convince Territorians not to eat so many olive pythons, but it's not going to be a big issue. Ecologically, that's a problem that we can put at the bottom of our list.
If evolution can happen fast enough to make a difference, it is going to be critical to setting up our conservation priorities.
The issue is this: is it happening fast enough? Can we detect the signature of evolutionary change in real conservation problems?
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This is the villain of the piece, the cane toad, Bufo marinus. (The taxonomists have just changed it to Chaunus marinus, which doesn't sound as nice, but anyway.)
Australians always say that cane toads are ugly and strange looking but, in most of the world where frogs are found, toads are also found and they all look remarkably like cane toads. Generally, they're just a lot smaller. The shape, behaviour, even the poisons are very similar in toads all over the world.
Toads occur not only in Central and South America, but through North America, Europe, Africa and Asia. Australia is one of the only places that has frogs but doesn't have toads.
So cane toads are actually a fairly ordinary-looking animal for most people around the world - just a very big version of what they're used to. But, of course, Australia didn't have true toads until 1935.
The cane toad has a huge parotoid gland full of incredibly toxic poison that can kill you if you try to eat it. It has an unbelievable fecundity: females can produce in excess of 30,000 eggs in a single clutch - which is a ridiculous number, it's like an insect - and it makes control incredibly hard. The 30,000 eggs hatch out into little metamorphs that crawl around the edges of the pond; people have often counted many hundreds per square metre.
These guys are toxic at every stage in their life cycle, although the amount of toxicity probably varies, making them a formidable invasion machine.
These great big adult toads can eat all sorts of things, and presumably compete with native frogs. They also produce little baby toads that are about the right size for the average native predator, who would like to eat them and would die as a result.
So it looks like a really bad scenario: what have Australian scientists done in response?
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Australian society, governments and funding agencies have poured many tens of millions of dollars into research on cane toads. And almost none of that has gone towards understanding anything about toads. The focus has been very simple, with people saying things like, 'We don't want to measure toads or understand them. We just want to kill them.'
So there is a cane toad army raging through tropical Australia and we don't know what resources it needs, where it breeds, what it eats or what effect it has. Instead we spend our time and money trying to come up with ways to kill and remove, to find ways to knock out toads.
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The unusual thing about our group's approach is that we are actually trying to understand the biology of toads and understand what their effect is.
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This is Team Bufo. These are the people that have gathered most of the data that I am going to talk about this evening. They are the ones that waded through the swamps next to the crocodiles, were bitten by mosquitoes and hit by heatstroke. They are a combination of postdocs, PhD students and honours students. And having mentioned them, of course, I am now going to completely ignore them and take the credit for all the work myself!
My job is mostly to sit around for one week every month, drink mango daiquiris, get in the way and give talks like this.
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So what do we do? Well, when the invasion front first arrived at our study site - arriving from Queensland about three years ago, after 70 years travelling across country - we strapped radio transmitters on the toads at the invasion front. And we are still doing that today.
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This is Greg Brown, out and about locating the toads with transmitters.
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This is one of my other postdocs, Michael Crossland, running experiments with David Nelson. These takeaway food containers each contain a native tadpole and some of them have toad eggs as well. We want to see if the native taddies will try to eat the toad eggs, and if so, whether they'll die and whether adding alternative food changes that outcome.
So we do a lot of experimental stuff and a lot of field descriptive work. We radio-track huge numbers of predators, like death adders, and see what happens when the toads turn up. It's a big program.
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Our study is based on the Adelaide River flood plain. If you drive from Darwin out towards Kakadu, it is the first flood plain that you will hit. (It's probably now much bigger after the rain last week.)
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This little tributary is the Fogg Dam flood plain. Our work is concentrated around Fogg Dam and Beatrice Hill. It is a beautiful place, only about an hour out of Darwin. If you are ever up in Darwin and you've got a day spare, you should drop by and have a look at Fogg Dam.
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I do need to mention my sponsor. The Australian Research Council has been kind enough to support this work full time, supporting fulltime postdocs, for about 20 years, which has been a phenomenal opportunity to try to understand the ecology of a piece of tropical flood plain. We don't understand the tropics very well, even though the tropics have the greatest biodiversity and a large number of conservation problems. It has been fantastic to have 20 years to understand the dynamics of these systems. And because we know this place backwards, it is an incredible opportunity to find out what toads do, to see what effect they are having.
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The first question I want to ask is: what native species of fauna will be affected by toads? If you sit in a pub almost anywhere in Australia and you ask that question, people will tell you about Doomsday scenarios and ecological catastrophe and toads leaving a trail of death and destruction.
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Lots of people send me pictures of little 'Billy' in the backyard with the death adder that he found. The snake bit a toad and died and killed the toad at the same time.
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All manner of things go around the Internet. This image was a recent one, mostly demonstrating just how good Photoshop can be and how gullible many people can be. It creates a great temptation for toad biologists because people are so prepared to believe the worst of toads.
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Not long ago, one of my postdocs took this photo of toads with a wallaby. I was going to send it to the Northern Territory News, saying that we saw this pack of toads chasing a wallaby down and then ripping it to shreds. But the reality is that the wallaby died long ago and the toads have been attracted by the carrion-feeding beetles.
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If you think it through, most native species are not going to be directly affected by the arrival of cane toads. If you don't eat frogs, you are probably not going to try to eat a toad and that cuts out a huge number of animals that could be affected. Toads do affect the invertebrates because toads eat them and they do compete with frogs. We measured both of these and found that the effect is quite small. The toads are not a big deal in these two situations.
The big deal is toads poisoning animals that try to eat them. If you are a frog eater you are potentially at risk; if you are not a frog eater you are probably okay.
Even if you eat frogs, if you are closely related to Asian frog eaters that have experienced toads for the past few million years, you've probably still got the genetic baggage to be able to process toads and to deal with the toxins or to recognise that you shouldn't eat them. So there would be a lot of frog eaters in Australian habitats that really aren't at risk because they are closely related to Asian species and toads are very, very common in Asia.
Another group is frog eaters who don't have close Asian relatives but eat a lot of toxic frogs. They have evolved mechanisms to check out whether the prey item is poisonous before they try and eat it. And again they may be able to recognise quite rapidly: 'Here's another toxic one that we should stay away from.'
There would be quite a few native species that on first principles we wouldn't expect to be affected by toads. So what do we find?
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What we find is much like as I have just said. At Fogg Dam one of the most common snakes is the keelback. These snakes are of Asian lineage and the only natricine in Australia. They can eat toads all day without any problems.
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There are also a lot of pythons in the area. They are physiologically very susceptible to toads but in the trials that we run they just don't want to eat them. It is just not a prey item that they recognise.
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The snakes that are really in trouble are the elapids, our venomous snakes. This picture, taken in the field, shows a king brown eating a death adder, and it is in these two species that we see the highest mortality among the snakes. We see about 90 per cent mortality in goannas and also some mortality in frogs, but overall it has been very patchy.
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But there are lots of dead death adders lying next to dead toads out in the bush. As I said, we have radio-tracked about 100 death adders to see who eats what toad, where, when, and what happens.
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You might not think that frogs are vulnerable, because they don't eat other frogs. But indeed they do. For example, the lilypad frog Litoria dahlii loves to eat other frogs.
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When the toads come into an area, we find lots of dead L. dahlii floating in the water.
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On the other hand, green tree frogs, which look pretty much like a lilypad frog, seem to be fine. We can put them in with baby toads and they just ignore them or they spit them out and so they survive.
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The one group of Australian animals that the Toad Doomsday people don't talk about is the birds. In Australia, there are a lot more people watching birds than there are watching frogs, snakes or quolls, yet there are many anecdotal reports of quolls and snakes going downhill when toads arrive but there is nothing about birds.
The reason appears to be because birds don't have any problems with cane toads - probably because birds are so mobile, there is so much genetic interchange with Asian populations that they have 'tricks' for dealing with the toxic toads. And so for a bird the arrival of cane toads is probably just an extra food source and not a big deal.
But it doesn't fit the Doomsday story and so we very rarely hear that side of it. Christa Beckmann, who just started a PhD with me, is trying to look at birds versus toads to see what is really going on.
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How about the poor native predators that aren't in any of these happy categories? Can they actually detect that toads are poisonous and just refuse to eat them and thus survive?
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(Again, here is a gratuitous photo showing me with the only large fish I managed to catch in the past two or three years.)
Barramundi are a very good example. Michael Crossland put barramundi in with toad tadpoles. The barra will grab the toad taddie, spit it out, maybe do that two or three times, and after that he won't go anywhere near a toad tadpole. So it is just not a problem. They learn almost immediately that toad taddies taste bad and you shouldn't eat them.
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We have more extensive data on the common planigale. The planigale is a dasyurid, a small marsupial predator which is in the same group as the quoll. The quoll - these big predators - are the species most implicated as the victim when the cane toad arrives. The evidence for this is fairly circumstantial (there are a couple of good studies) but it really does look as if quoll populations go down when toads arrive.
Planigales are also voracious predators but they are small; they are shrew-like animals. They are very common on the flood plain but nobody has ever looked to see what happens to them when toads arrive.
Our prediction was that since they are related to quolls, and since they eat frogs, they would probably jump on a cane toad and they would probably die in agony, very quickly. It would be an ecological catastrophe.
We decided we needed to test our prediction, which meant we had to put captive planigales with cane toads, which was an awful thought. We waited till the toads had bred in our study site for the first time, when we knew that any planigale on that flood plain was going to meet a few thousand baby toads within the next few weeks of its life. We felt that under those circumstances we could put a baby toad in with a planigale.
I will now show you a couple of videos of what happens.
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Here is a planigale, sitting inside the shelter - you can see the tail out the back. We are about to throw in a cricket. These guys are dramatically fast and incredibly voracious, and bang! They will just hurl themselves at anything.
This is a native frog, boom! So it looks discouraging. I was hoping they wouldn't eat frogs, but they do.
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So we took a deep breath and we threw in a toad. The planigale pauses and you think, 'Oh goody, maybe he does recognise it,' but no. He thinks the toad is a frog and he's going to eat that toad. So he kills the toad and he starts eating it head first. At this point we thought, 'This is just awful. We are about to see 20 little planigales in 20 experiments all dying in agony.'
Only a couple of them died. The others, because of the way they were processing the toad - eating it from the nose first - got very little toxin and they survived.
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The amazing thing was, when we put toads in a second time we couldn't talk a planigale into going anywhere near them. And when we put in a native frog, we discovered that the planigale decided that anything that even looks like a toad is not a good idea.
Now, these are incredibly voracious little predators. After one trial they have learnt that toads are not to be eaten so they aren't a problem. Ecologically, toads are not a problem for planigales because the planigales learn very quickly. They are used to encountering toxic insects and frogs and they know now that toads fit into this category.
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The first insight we gained from applying evolutionary ideas to the toad invasion is that the toads are only going to affect a small proportion of the native frog-eaters, rather than creating across-the-board mayhem.
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Suppose you are a predator who is not very good at learning and you don't have any relatives from Asia; you are the 'bunny in the headlights' and you're in trouble when the toad comes. The elapid snakes, particularly our death adders, are the best example of this.
What might happen? If rapid evolutionary change could do something when toads arrive, what traits would you expect might help a snake survive?
The most obvious one is feeding responses. For example, if there is a gene that says, 'Recognise a toad and don't eat it', it should increase in frequency.
If you are a snake, the risk of being killed by a toad that you want to eat depends on how big you are compared to the toad. To cut a long story short, the best kind of snake to be is a large snake with a small head, because then you can only eat a small toad. Over time, we would expect to get a shift in body size and relative head size in snakes.
Also, physiologically we would expect that snakes would evolve to be able to tolerate the toxin of the toads.
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Our best data comes from the red-bellied blacksnake - the pinnacle of vertebrate evolution, the most glorious and interesting creature on the face of the planet. Ben Phillips did his PhD on these snakes and he took advantage of the fact that some populations of blacksnakes have been overrun by toads and others have not. By comparing toad-naïve snakes with toad-experienced snakes, we can look at traits, such as feeding responses, to see if there are any differences. Ben found wildly significant changes in all three of the variables investigated - that is genes, feeding responses and tolerance of toad toxin.
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Let's take a look at the feeding response. If you put a blacksnake from an area that has never met a toad, for example blacksnakes from around Canberra, in a cage and you throw a frog in, 100 per cent of the snakes will eat the frog. Blacksnakes really like frogs.
If you throw a toad in with these snakes - a toad about the same size as a frog - about 50 per cent of the snakes will eat the toad and they will almost certainly die. They are very vulnerable to toad toxin. They just can't handle it.
If you go to an area like Brisbane, where toads occur, and you catch a bunch of blacksnakes and test them, you find that they all eat frogs but none of them eat toads. This is almost certainly not learning. We tried to teach blacksnakes not to eat toads and we failed miserably. They just don't seem to adjust their behaviour. What seems to be happening is that when the toads arrive, the snakes that eat frogs but not toads are the only ones that survive. They then form the nucleus of the population that begins to recover.
Blacksnakes are still quite rare in areas where cane toads occur - their recovery hasn't been complete, by any means. But we do find blacksnakes happily coexisting with toads. The snakes eat lots of frogs, despite the fact that there are toads all over the place.
Blacksnakes from toad infested areas also display the shifts in physiological tolerance to the toxin and in relative head to body size.
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So, even among predators that are affected, many will recover. There are no recorded extinctions of anything in Australia due to cane toads and there are many stories about native species recovering, for example goannas in Townsville.
But we don't want to get too encouraged by these things. Some of the predators are recovering but are still quite rare. Quolls, for example, do seem to be recovering in north-eastern Queensland but they are still rare animals. However, it does seem many predators are managing to live with cane toads. That wasn't possible in the predator populations when the toads first invaded.
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Turning from the native predators to the cane toads: evolution is working on them too. And it doesn't take a lot of reflection to realise that evolution can produce changes very rapidly within toads.
This is an animal that can mature in four or five months and the females can produce 30,000 eggs. So if you put a selective force onto that system, it can adapt incredibly fast. You can kill 98 per cent of all of the toads in the population. If the remaining two per cent have a magic gene that has helped them overcome that mortality source, then next generation you are back to 30,000. The population can potentially recover incredibly fast, even from intense selection.
This is a system that should evolve very rapidly. So what do we see?
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In terms of conservation, one thing that we would like to know is how quickly the toads are going to spread.
Evolutionary thinking predicts that invading species will go faster and faster - it doesn't matter whether we are talking about cane toads, fire ants or pine trees. The reason for this: if the front is moving quite quickly, then only the fast-moving individuals, or the individuals that can disperse more rapidly, will be at the front. And only their fastest-moving progeny will be at the front and only their fastest-moving progeny will be at the front.
So there is acceleration. Any gene that slows a toad down will be left behind and the front will be composed of incredibly fast-moving, really effective dispersers - a nightmare for conservation.
Only the quickest individuals can stay at the front and that should result in the invasion front moving faster and faster as the invasion process goes on.
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What makes a toad go faster? As Kurt has already mentioned, and this is true for many amphibians, those individuals with relatively longer legs are much quicker. They hop a bit further.
Clearly there are a number of behavioural things that determine dispersal. For example, a toad that moves every day can potentially move across the landscape much faster than one that moves once a week. Also, a toad that moves in one direction, day after day, is going to move much further across the landscape than one that just meanders round in a circle.
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Let's look at leg length. (This data is from telemetry.) These axes show a residual score for leg length and a residual score for distance moved in metres over three days.
Basically, toads with really long legs move about a kilometre further over three days than toads with short legs and the same body size. It's a huge difference. These toads are sprinting through our study area. It is common for a toad to move a kilometre in a night, move every night and keep going in the same direction. It's a phenomenal invader.
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Because of that effect, the long-legged toads were the first to get to Fogg Dam. If we look at the order of arrival of the first 800 toads in the first year, we find that average leg length has decreased with time. The really fast toads in the vanguard have very long legs. So we see the evolution of leg length as an adaptation to the invasion process.
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How about behaviour? Very conveniently, we have data on Queensland populations which was done some time ago by Ross Alford and Lyn Schwarzkopf, from James Cook University. By radio-tracking toads in Queensland, they found that the toads move in any direction; it is completely random. However, our toads at the invasion front, essentially, all move north-west, straight towards Darwin.
It gets to the point, with the radio tracking, that if we let a toad go in one place we know it is going to be about a kilometre to the north-west tomorrow and another kilometre the next day. They just sprint through the study area, with ridiculously non-random directionality.
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To look at distances moved: we have here two Queensland populations. The Townsville toads have been around Townsville for probably 50 years; the Heathlands population was at the invasion front in about 1990-91 and Fogg Dam is the current invasion front. The Heathlands toads are averaging about five or six metres a day and the Fogg Dam guys are averaging almost 100 metres a day. So, in approximately 70 generations, cane toads have gone from little sedentary homebodies that just meander round in circles, to road warriors that move every day, in the same direction, and achieve displacements that are more than 10 times what they were 50 years ago.
An extraordinary toad has evolved in the process of this invasion - very different from the toads that occur in the areas that have been colonised for a long time.
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Cane toads are moving faster and faster. This map was put together by my collaborators at Yale and it shows the rates from slow to fast. The toads started out slowly and now they are racing across Australia.
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Another way to plot the same data shows that in the early years of the toad invasion the range expansion per year averaged about 10 kilometres; today, the toads are now expanding at around 60 kilometres per year.
As I said, this would be true of every invasive species, so any conservation manager who wants to anticipate what is going to happen with a biological invasion has to expect this to happen.
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It is difficult to see how toads will be able to expand faster than 60 kilometres a year. These guys are sprinting as fast as they can. But one of my grad students, Matt Greenlees, took this photo on the Arnhem Highway recently. It suggests that toads will come up with yet more ways to move faster!
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The insight from this: after they establish, invasive species are likely to go faster and faster. If you want to control them, you had better start very soon, very early in the invasion. If you let them go, they are going to be harder and harder to control.
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How far will toads make it across Australia? The conventional way to predict this is to look at the range of climatic conditions in the ancestral range, map that to find out where in Australia those conditions occurred and then predict that that is where the toads will end up. (This is akin to what climate scientists are doing with climate change modelling.)
If you are prepared to add evolution into the mix, you end up with a different prediction. Toads can adapt. What is stopping the toads from becoming good little Aussies? What is stopping them from adapting to Australian conditions so they expand their range of climatic tolerance and thus can exploit much more of Australia than you would have predicted from where they live in South America?
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Since Australia is a hot place you might expect the upper temperature limit that toads can tolerate to have increased since their arrival in Australia.
Thirty years ago, toads in Queensland had lots of areas available to them that were very hot but they didn't go into them. Now they do. They have evolved and the upper thermal tolerance has increase by a couple of degrees.
That means that the area of Australia that toads can potentially exploit is quite different from what we first thought.
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This map shows where toads are now. Everybody accepts that the toads will get through the Kimberley and invade the adjoining area. And most people tacitly assume that that will be the ultimate limit of cane toad invasion in Australia. So the process is pretty much over.
Mark Urban and Dave Skelly, from Yale, along with Ben Phillips and myself, from Team Bufo, modelled the climates in the areas where toads are currently found in Australia, as opposed to where they occur in South America, and asked: where do those conditions occur elsewhere in Australia?
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This is the scariest map you will see for a long time - the modelling predicts toads in south-western Australia, big areas of South Australia, Melbourne and patches of New South Wales. The toads are evolving to be good little Australians; they are grossly expanding their range of tolerance. Based on the areas they already occupy in the north, they should have no problems - the toad invasion has really just started.
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Invasive species will adapt, and that means it may be very difficult to predict where they are going to go, based simply on where they came from.
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The last thing I want to cover is control - if I don't mention it, it will be the first question somebody will ask me.
Does evolutionary thinking provide useful methods for controlling toads?
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A lot of money has been spent on controlling toads and some people have made a lot of money coming up with silly ways to do it. I think one of the silliest is toad-specific bullet, a given that you can walk across, bend over and pick them up.
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The first lesson from evolutionary biology is that because toads are such fantastic evolutionary machines, we cannot eradicate them from Australia. Anything we come up with will be a selective force and they will adapt to it. It doesn't matter if it involves genetic engineering or a magic trap or anything else, there will be variance. Toads can adapt rapidly. We will not eliminate toads from Australia. All we can do is begin to focus on reducing their impact.
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How might we reduce toad impact? If we sit back and ask ourselves that question in a very simple fashion, the obvious thing to do would be to say, 'Sometimes there are lots of toads in a place and sometimes there are very few toads in that place. Maybe we could just look at why that is.' And it's remarkable that nobody appears to have actually ever asked that question or tried to answer it for toads in Australia.
In particular, the story we hear from areas with toads is that toad numbers are really high when they first arrive, they stay high for a decade or two and then they decline. Why? If we could work out why they decline, maybe we could stop them being so numerous in the initial phase.
There are not many solutions that could work. One solution involves adaptation of the local predators to try and hammer the toads, but that is unlikely.
Affecting the food supply is also unlikely.
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If we look at domestic animals and humans in underdeveloped countries, we see that parasites offer opportunities to control populations. Do toads have parasites? Yes.
These are some dissected toad lungs. When we take the lungs away we discover a whole bunch of worms left behind. These are nematode lung worms, Rhabdias and they probably hopped onto toads from Australian frogs. Toads can have hundreds of them in their lungs and they create all sorts of nasty scars and so on in the lungs.
Now, think back to what I said about the invasion process, where only the fastest toads can stay at the front. It seems plausible that a toad with his lungs full of worms would be slowed down. If that was the case, the parasites would begin to lag behind. As the invasion front accelerates in toads, only the uninfected toads that can move quickly are at the front. They're bearing their progeny big, so the parasite front will move but the toad front will move faster. There will be a period of maybe a decade or two when the parasites haven't caught up with the toads.
If this is the case, and if the parasites really affect the viability of toads, this could explain why toads are so abundant for the first 10 or 20 years and then their numbers decrease.
If it is true, the corollary is that we could potentially take a bucketful of water from a pond in Townsville, dump it in a pond in Darwin and cut that initial high-density phase of toads from 20 years to six months - if it were true.
Crystal Kelehear is just finishing her honours with our team and she has shown that the worms do have an enormous affect on the viability of the toads. They also affect their locomotor speed, endurance and so on - at least in the small toads. So parasites work.
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How about the prediction that toads at the front won't have parasites and ones further back will? It is almost embarrassingly good.
Di Barton gathered these data on toads about 20 years ago but hadn't looked at them in this context. I got the data from her and re-analysed it, and sure enough, you never get lung worms at the front or anywhere near it; however, they are incredibly common in toads further back.
Crystal has just completed another sample and found that the lung worms have caught up a bit, but there is still about a 20-year period when there are no worms in any of the toads at the front.
I am not suggesting that you should go and dump worms at the invasion front, and that will take care of all our problems - I think the toad itself is a good example of biological control attempts that were done without enough forethought - but it certainly might be an incredibly cheap, effective way to have a real impact on what toads are doing. The high-tech approaches seem to have overlooked simple solutions like this.
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What other control measures might work? The trick here from an evolutionary perspective is to work out ways in which toads differ from frogs, but are similar to other toads. Many of the things we could do to toads, they could probably adapt to really quickly. We know they can change leg length, we know they can change their movement patterns - their frequency of movement, their directionality - but if we pick traits in which cane toads look like every other toad on the planet they are probably hard-wired in to being a toad. It may be much harder for them to adapt their way out of it. Are there things like that? Sure.
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Matthias Hagman, one of my PhD students, went up to the invasion front at Fogg Dam, looked at breeding sites and showed that toads love to breed in awful places: in shallow scrapes with very little vegetation round the edge. They hate deep pools, vegetation close to the edge and steep sides.
Mark Semeniuk went and did the same thing in northern New South Wales, at the other end of the toad front, and he got identical results. So toads are incredibly consistent when it comes to selecting breeding sites.
If you live in Darwin and you have a pond in your backyard and you don't want toads, you could probably spend two days planting grass around the edge of your pond. Or you could go out every night for the next 50 years with your golf club, trying to hit toads.
A simple understanding of the phylogenetically conservative nature of breeding-site choice in toads may be incredibly useful in helping people to reduce toad numbers.
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The very last example I have is behavioural and it is from work done by Matthias Hagman. We set up shallow water in trays, with grids underneath. Hospital equipment infuses fluids into one corner of each enclosure, so we can put various chemicals in and see if toad tadpoles react to the chemicals.
It turns out that they do. And it turns out that many toads have a really interesting communication system involving alarm pheromones.
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We take a toad tadpole, frighten it, or hurt it, and then gather the fluid from around that tadpole and put in a litre of water. A few drops are then added to one corner of Matthias's trays and we find that the taddies quickly move to the corner diagonally opposite. They're petrified. They hate it. They run away.
We did the same experiment with Aussie frogs and they don't react. They don't have a system of alarm pheromones and they don't react to the toad one.
So we now have a toad language. We can actually yell at toad tadpoles without the native frogs hearing us. And it works with metamorphs as well. So we can potentially start to move toad tadpoles and metamorphs around in ways that are bad for them and good for us, without affecting native frogs.
I think there are all sorts of opportunities there.
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This was the front page of the NT News when our toad-legs story came out.
The bottom line is that toads are incredibly impressive invasion machines, they are rapidly evolving to adapt to Australian conditions and they are rapidly evolving in response to the invasion process itself. At the same time, the native predators are adapting very rapidly to the presence of the toads, in ways that enable them to coexist. Unless you understand the dynamics of that system, you are not really in a position to do the most effective conservation biology.
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And this basic set of insights that can, I think, enrich conservation biology come from my own hero, Charles Darwin.
Thank you.
Discussion
Kurt Lambeck: Thanks very much, Rick, for a tremendous lecture. At least one thing I have learned from it is that many toads are poisonous. Now I know why witches put toads into their brew!
Rick Shine: Absolutely.
Question 1: Is the toad toxin a very complex mixture of chemicals? And if that is the case, what sort of mechanisms of tolerance do the predators evolve?
Rick Shine: You might think that we would understand the composition of toad toxins - but we don't. Rob Capon and his group at the University of Queensland have money to investigate this and they have started to isolate the toxins. He is also working with us on isolating the active component that scares tadpoles and so on.
But we really don't know. There is research suggesting that tiny genetic changes in some of the genes - I think they control some of the channels through the cell walls - can result in a thousand-fold difference in resistance to the toxins. So a tiny genetic change can make a toad relatively invulnerable to the main toxin, at the very least. This is probably what some of our native predators have done.
But I am not a chemist. Rob tells me that it is a crying shame that we don't actually know what toxins toads produce.
Question 2: You spoke about planigales learning not to eat toads. What impact will that have in their learning not to eat frogs and, likewise, the frogs not being eaten?
Rick Shine: What I carefully avoided mentioning was the interact effects. Suppose you take 90 per cent of the goannas out of a system. Sean Doody and his group have shown that removing these massive predators results in the survival rates of turtle eggs going through the roof.
The planigales are in trouble. What they do is switch to using scent. Normally, they use vision to jump on anything that looks like a frog. But after they've met a toad, they check out potential food by running over to it and sniffing it. If you take a cricket, rub it in toad smell and throw it into the cage, the planigale won't eat it. The planigale now has to make a complex decision and in the process of that decision, I suspect, a lot of the frogs get away into the shrubbery. So there are probably reduced predation rates on some of the local frogs because of this new planigale behaviour.
The indirect effects, the cascading effects of toad arrival, could be substantial but we don't yet understand them. And there are winners and losers.
Question 3: Is predicted climate change likely to change the distribution of places that toads can get into and their ability to cross those regions into the south-west and Adelaide and such?
Rick Shine: Yes, I think climate change could cause changes. One of the predictions is for more rainfall in tropical Australia. The southern invasion front in New South Wales seems to oscillate and I have a feeling it might be that in warm summers the toads tend to do a little bit better further south and so on. This is something we are looking at that at the moment.
I suspect that the width of the corridor along the Western Australian coast is too narrow. But what will happen is that a bunch of toads will end up sitting in somebody's agricultural equipment in the back of a ute coming from a mining camp down into Perth for the weekend party - so toads will get to Perth.
Toads come to Sydney every year and I am sure they come to Canberra every year. Toads are really good at hiding in stuff. So it will just delay the arrival of toads. But I don't think the corridors even have to be there for toads to be on the move because we move so much stuff around.
Question 4: This is probably not very significant in the overall picture of things, but has there been any research done on domesticated animals, particularly dogs? Having lived in Tully and all those areas up there, I am aware that some dogs have not been too well after coming in contact with toads, and I just wondered if it is a bit like the planigale - whether they adjust. Has there been any research in that area?
Rick Shine: I am aware of stories and one or two research papers. It seems that when the toads reached Katherine, the terriers disappeared. It seems that small dogs that like to chase moving things are the first to go but that many other dogs adapt to the presence of the toads.
There are stories of dogs that become toad-addicted - I have actually seen footage of it. The dogs disappear into the backyard and they go and lick a toad and they come back and sort of swoon around for a while and fall over. Then they get up and go down into the backyard and lick the toad again. So Lord knows.
I am sure there is substantial mortality of some of these domestic animals.
Question 5: [inaudible]
Rick Shine: There is a wave of fear that precedes the toad invasion. One glorious example was that the denizens of the Kimberley were told that one of the impacts of toad invasion would be that the unemployed youth would all start licking toads and become desperately antisocial. I am not aware that it has happened but the Territory is an unusual place.
Question 6: Concerning the plant growth around water bodies inhibiting toad breeding, is this an opportunity for you to promote the results of your research? And have you worked out a publicity plan, offering people a way of actually reducing toad incidence in their gardens, public parks and so on?
Rick Shine: We talk to a lot of people who we hope will spread the message. There are a number of community groups that were formed specifically in the face of the toad invasion and they tend to put their effort into things like traps and physical removal, which our work suggests are not going to be very effective. But I think they are starting to spread the word that there may be some relatively simple things that people can do.
The question is exactly how much of your effort you should put into promulgating that message and how much into trying to find out more about the system. I don't know that we have spread the word very well but we do try.
Question 7: Rick, how well are the toads coping with the cycle of wet and dry in tropical Australia? I note that toads reached the headwaters of the Cooper drainage but they haven't spread through it, presumably because the dynamic of wet and dry there is not suited even to their persistence. How well do they cope with the dry season in tropical Australia? Does it really knock them about and is there room for them to adapt to that?
Rick Shine: There is a dramatic reduction in body condition of toads. Toads tend to remain active through the dry season, where so many of the native frogs just go underground and shut up shop. So during this time toads tend to decline in condition.
By the time the wet season rains come, very few toads actually have the energy reserves to breed. So the rains come, the frogs breed - it's just frog sex everywhere during the wet season - but the toads are gradually building up condition as they feed. It's really at the very end of the wet season, about now, that we start to see more toads breeding, and that continues through the dry season. There is a real seasonal separation in breeding events. It may well be that a rapid cessation of wet season breeding, if the water bodies aren't there, means that there will be years when the toads are in trouble.
I would have to say that the toads are having more trouble succeeding in the Top End flood plains than I expected. We thought the flood plains would be fantastic for them but they avoid the flood plains like the plague. They go down the edges, through the woodland, but those big black-soil flood plains that you would think would be heaven for a toad, they just stay away from. But give them a while!
Question 8: This isn't facetious, although it might sound so. How do you scare a toad to produce the alarm pheromones? More importantly, how close are you to applying it in the field?
Rick Shine: We started out by macerating toadlets, then we realised we could simply pick up a taddie, rub it with our fingers and put it back in the water again. It is a very powerful signal. We are working with Rob Capon and his group at the University of Queensland, and they have narrowed it down to one of four compounds - which I think is remarkably quick. They are confident that within a month or two we will know the exact chemical composition of the toad alarm system.
The really exciting thing is with the metamorphs. Matthias has found that that chemical repels the metamorphs as well, so you can focus on them. (You may not want to control taddies, for a complex variety of reasons to do with competition among tadpoles within the ponds.) The metamorphs are very vulnerable to drying out when they leave the water body. If you could spray the chemical around the water body, in the damp zone, you could drive the metamorphs out to where they turn into crispies. That might be an effective way to do it.
So how far are we away from actually implementing it? I don't know. We are zooming along as fast as we can. It is a very simple behavioural assay and it works like a charm. So if the chemists can give us the stuff, then maybe in your local supermarket in a few years' time there will be a box of 'Toad-Off'.
This is exactly the way we should be using behavioural ecology data to contribute to conservation and I would love to see it turned into an actual mechanism that people could use.
Kurt Lambeck: I think that is an appropriate point to stop as we all go off to dinner, Rick. Once again thank you very much for a fascinating lecture. It is very much appreciated. I would like the audience to join with me in thanking Rick again.
