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Tolerate Thy Neighbour

cane toad

While adult cane toads are poisonous to terrestrial animals, their eggs and tadpoles are just as lethal to aquatic species. Credit: brian.gratwicke

By Georgina Caller

Cane toads have been wiping out native species, but one fish species has learnt to avoid toxic toadpoles.

For as long as humans have been moving around the world they have been taking other species with them. We have moved hundreds of thousands of vertebrates, invertebrate and microorganisms from the places they naturally evolved to new environments.

The majority of these introduced species die off after a few generations or settle into small contained populations that aren’t disruptive to their new environments. Unfortunately, a small proportion of introduced species will rapidly dominate their new environment, often wiping out any unfortunate native species they happen to compete with or prey upon. The results are dire: invasive species have a hand in 40% of all modern extinctions, with more occurring every year.

Australia has been hit particularly hard by invasive species. Due to its isolation and unique flora and fauna, invasive species often present Australia’s native organisms with threats they have never faced before. Cats and foxes have devastated populations of small native animals, and native vegetation is struggling with the introduction of hard-footed species such as cattle and horses.

However, our studies of the freshwater crimson-spotted rainbowfish have given us confidence in the capacity of native species to survive. We have found that these little fish can adapt their behaviour to the scourge of the cane toad and other potentially poisonous prey – simply by learning not to eat tadpoles.

The cane toad was introduced to Queensland in 1935, and has been a headache to conservationists ever since. It is unique among invasive species as it is dangerous to native species not by eating them, but by being eaten.

The toad’s body contains a cocktail of toxins that are devastatingly deadly to native Australian predators. Its arrival in an area is normally followed by a drop in population of every major predator that makes the lethal mistake of taking the poisonous creatures for a quick snack. The eggs and tadpoles of the cane toad are just as deadly, so even aquatic predators are not safe.

To make matters worse, the toads breed rapidly, producing thousands of eggs at a time, and have been slowly increasing their range west and south from Queensland for decades. So far no effort has succeeded in stopping them.

However, what makes invasive species so damaging to native organisms – their novelty – is also what makes the responses to them so fascinating to uncover. While many species succumb to the pressure, others adapt to the presence of the new species. By studying them we can watch evolution in motion.

Increasingly we are finding adaptation among the animals most affected by cane toads. Black snakes have developed an immunity to cane toad toxins. Other snake species are growing larger bodies and smaller heads, so that the snake’s smaller mouth is unable to consume a toad big enough to give a lethal dose of toxin to the snake’s larger body.

While these are impressive, so far all observed adaptations to the cane toad have occurred among terrestrial predators. While terrestrial predators have started adapting to adult toads, are aquatic predators likewise adapting to cane toad tadpoles?

There is evidence to support this: certain fish repeatedly fed cane toad tadpoles over several days stop trying to eat them. We set out to discover if this was occurring in natural fish populations.

We chose the crimson-spotted rainbowfish as the ideal study species. A predatory fish and keen consumer of tadpoles, its learning and memory abilities are well documented. It has a relatively short range along the east coast of Australia that partially overlaps with the range of the cane toad. This allowed us to collect two populations of rainbowfish: the northern group had been co-existing with cane toads for roughly 60 years, while the southern group came from an area free of cane toads.

We offered each fish either a cane toad tadpole or a native tadpole in a clear, perforated plastic tube. This way the tadpoles could be seen and smelt, but could pose no danger to the fish as it could not make physical contact with them.

We then recorded the behavioural responses of each fish to measure how interested each one was in tadpoles. As the fish were very curious we also offered them an empty tube so that we could determine how much of their overall interest was simply their interest in the tadpole’s enclosure.

As we predicted, the northern fish showed as much interest in the cane toad tadpoles as they did in an empty tube. In contrast, the southern fish were equally, and highly, interested in both the cane toad tadpoles and the native tadpoles.

It seemed our hypothesis was correct. The northern fish had learnt that cane toad tadpoles were not worth eating.

But something unexpected appeared in our results. While the northern fish were clearly more interested in native tadpoles than cane toad tadpoles or empty tubes, their level of interest was still much lower than that of the southern fish. This raised the question: had learning to avoid the noxious cane toad tadpoles led the northern fish to mistrust all tadpoles?

To test this we exposed some of the fish from the southern population to cane toad tadpoles once each day for 5 days. We used larger tadpoles that could not be swallowed by the fish to reduce the danger of poisoning. We recorded their behaviour throughout and found that this was not enough contact to elicit the aversion to toad tadpoles displayed by the northern fish.

After this run of toad tadpole exposure, we gave each fish a native tadpole and recorded their level of interest. For comparison, the other southern fish and the northern fish were also given native tadpoles and their responses recorded. Like the previous experiment, the interest of northern fish in native tadpoles was low while the interest of southern fish was high. However, the southern fish that had been exposed to cane toad tadpoles now showed the same level of interest as northern fish.

This was intriguing, particularly since the exposed fish had not learned to avoid cane toad tadpoles in the time they were exposed. It seemed that once the rainbowfish came across a noxious version of their regular food, all food of that type became less attractive to them, even before their rejection of the noxious food was particularly strong.

We were curious to see if living with cane toads had any deeper impacts on the northern fish that weren’t necessarily directly related to cane toad tadpoles, such as making the fish more adept at learning not to eat bad foods. To investigate this we presented both populations to a situation that echoed what would happen in the wild when cane toads first entered an area.

We took the food pellets we had been feeding the fish and soaked them in quinine, a chemical that, like cane toad tadpoles, has a distinct and unpleasant bitter taste. These pellets were then dyed a specific colour so the fish would be able to tell the difference between the quinine and the normal pellets at a glance. The fish were fed a mix of quinine pellets and normal pellets 10 times per day over 5 days, and we recorded how interested they were and how many of each pellet they ate.

The results of this experiment were complex but very interesting. First, interest in pellets for all fish dropped after the quinine pellets were introduced. This supported our theory that once a noxious version of a food type comes along, all foods of that type come under suspicion.

However, an interesting difference began to arise between the two populations. The more the southern fish were exposed to quinine pellets, the less they were interested in all pellets, non-exclusively. By contrast the northern fish grew less and less interested in only the quinine pellets, while their interest in normal pellets remained the same after the initial drop. It seemed that, having been exposed to noxious prey for a long time, this population was better at distinguishing between edible and not-so-edible food.

On top of this, the northern fish ate less of the quinine-laced pellets than the southern fish, being less likely to force themselves past a bad taste for a meal. Perhaps this was a harsh lesson learned from the past.

Introduced species present some of the greatest dangers to the continuing existence of Australian species. Their ability to change the ecology of an area can have a widespread impact that some species cannot surmount.

What is fascinating and admirable about the fauna of Australia is their ability to adapt to new situations. It seems that at least for this little fish, the cane toad tadpole is a threat that can be met.

Georgina Caller is a graduate of Macquarie University’s Behavioural Ecology and Evolution Laboratory.