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In a recent paper,1 we showed that recurrent exposure to alarm pheromones reduced development time and size at metamorphosis in larval cane toads (Bufo marinus). Subsequent measurements of post-metamorphic toads revealed larger parotoid glands relative to body size and increased amounts of bufalin (a toxic bufodienalide) in animals from the experimental treatment, suggesting increased investment in chemical defenses. These findings are of interest for evolutionary theory. But the study was also part of a larger conservation-based research program of which this pheromone work was an important component in the development of a management strategy for reducing the ecological impact of invasive cane toads in Australia. For example, our study1 aimed to quantify biochemical and life-history effects as well as assess the likely longterm impact of pheromone exposure on toads. In this addendum, I discuss the conservation potential of our research, with emphasis on exploiting alarm pheromones to induce viability reducing life-history shifts.
An important precondition for the potential use of pheromones is that they must impact on cane toads specifically. Our studies2,3 of Australian tadpoles show that at least 15 native species are unaffected by exposure to toad alarm pheromones, suggesting that the chemical is specific in its activity. Thus, presumably only cane toads will detect and respond to toad pheromones, hopefully with no negative effects on native anurans. This prediction must be tested on more native anurans before any control measures can be implemented, but these preliminary results are nonetheless encouraging. If species-specificity eventually is fully confirmed these alarm pheromones offer great potential for control measures targeted at invasive toads. For example, we may be able to distribute pheromones in the field to manipulate the spatial location of toad tadpoles.4 The ability to influence tadpole behavior might be used to facilitate trapping or to disrupt thermoregulation by keeping tadpoles away from the microhabitats (such as warm shallows) in which they spend most of their time and presumably, which confer fitness advantages (via higher body temperatures, more plentiful food and so forth). Increasing the concentration of tadpoles may also escalate cannibalism and competition for resources.
A more effective control method may be to exploit pheromones to induce shifts in life-history traits. Many anurans respond to environmental cues such as predation-risk, competition and changing hydroperiods by expressing plasticity in behavioural,5–7 morphological6 and/or lifehistory traits.8,9 According to theory such plasticity should enhance fitness—but may also incur profound fitness costs such as slow growth and development.10 For example, tadpoles should escape a risky aquatic environment by metamorphosing sooner. However, they may pay the cost of small size at metamorphosis.8 Our study1 showed that it is possible to use alarm pheromones to induce shortened developmental time and smaller size at metamorphosis in cane toads, as predicted by theory. It is likely that these effects impose fitness costs.9,11,12 For example, small size might render metamorphic toads more vulnerable to predation, 13 cannibalism14 and desiccation.15 Size at metamorphosis can also affect postmetamorphic performance. For example, larger metamorphic size can persist for up to two years and has been positively correlated with both juvenile survival and with reproductive success.6,8–23 Inevitably one must ask the question if a laboratory result has ecological validity. In other words, can we extrapolate our laboratory results to the field? In order to answer that question we conducted a series of experiments in outdoor ponds.24 Interestingly we recorded up to fifty percent mortality in tadpoles and significantly smaller size at metamorphosis (Fig. 1) in the survivors when we added alarm pheromones to experimental ponds and compared them to siblings from nearby control ponds. It is unlikely that the pheromone itself was the direct cause of higher mortality in these trials. Presumably the pheromone functioned as an environmental stressor that made the tadpoles more vulnerable to parasites and invertebrate predators. Whatever the case, this work clearly showed that adding alarm pheromones to natural ponds could indeed increase mortality in tadpoles and reduce the size of metamorphosing toads.
Despite extensive research in many fields (from trap design through to genetic manipulation), we currently lack any means of controlling populations of invasive cane toads or of reducing their ecological impact.25 In this article I have discussed the prospective of using alarm pheromones for controlling invasive cane toads. The strong avoidance of alarm pheromones by toad tadpoles shows that these animals possess significant chemically mediated communication systems26 that are likely to be toad specific.2,3 Exposure to these cues induces significant life-history shifts that can reduce toad viability. 24 Thus, by purposeful use of alarm pheromones we could concentrate toads spatially4 and exploit ecological processes and life-history shifts to reduce the fitness, survival and ultimately, the ecological impact of cane toads in Australia.
I thank Richard Shine, Team Bufo and my previous collaborators at the University of Queensland, Rob Capon and Andrew Hayes. The Australian Research Council, The Department of the Environment, Water, Heritage and the Arts and the Swedish Research Council, provided funding.
Addendum to:Hagman M, Hayes RA, Capon RJ, Shine R. Alarm cues experienced by cane toad tadpoles affect post-metamorphic morphology and chemical defencesFunc Ecol200923126132 doi: 10.1111/j.1365-2435.2008.01470.x.
Previously published online: www.landesbioscience.com/journals/cib/article/11345