Cane toads

Predicting the impact of cane toads on native fauna: a mechanistic approach

Ben L. Phillips 1, James G. Smith 2, Matthew Greenlees 1, Greg P. Brown 1, Rick Shine 1 and Johnathan K. Webb 1.

1 School of Biological Sciences, A08, University of Sydney , NSW 2006.

2 Key Centre for Tropical Wildlife Management, Charles Darwin University , Darwin NT 0909.

Abstract

Logistical difficulties in quantifying the abundance of animals, combined with large yearly and seasonal fluctuations in population size, make the task of quantifying cane toad impacts difficult in the field. We are using a mechanistic approach to assess the likelihood of an impact from cane toads on reptile predators, frogs and invertebrates. That is, we identify a mechanism of potential impact and then test it in an experimental setting. Using this approach, we have concluded that:

1. 30% of our terrestrial snake species,59% of the Agamids, 85% of the Varanids, 50% of our crocodiles and most of our freshwater turtles are potentially at risk from cane toad poisoning;
2. Toads can reduce invertebrate abundance and modify species composition in floodplain assemblages; and
3. Strong dietary overlap between frogs and toads provides potential for competition between these species.

The mechanistic approach we outline here is cheaper than long term mark-recapture studies and, more importantly, allows us to rapidly identify which taxa we should be concerned about.

Introduction

The spread of feral cane toads across tropical Australia has raised many issues about potential impacts, and numerous research projects have been designed to clarify exactly what changes occur in natural systems due to the arrival of toads. We believe that most of these studies provide only weak evidence, because of logistical difficulties inherent in their design. In this contribution, we explain the nature of those difficulties, and review our preliminary results from an alternative (and we argue, more robust and effective) approach aimed at revealing the ecological impact of cane toads.

Before-After-Control-Impact (BACI) Designs

Quantifying animal abundance in the field poses a formidable problem. Inherent uncertainties in estimating population size, combined with large yearly and seasonal fluctuations in population sizes and animal activity make estimating abundance a difficult, and often time consuming process. Unfortunately, estimating abundance is a necessary precursor to detecting changes in population size. Additionally, proving that a reduction in population size is a consequence of a specific environmental impact (such as the arrival of an invasive species), adds more layers of difficulty: To prove that a change in abundance has been caused by a specific agent, several discrete populations (typically more than 4) need to be censured concurrently. Some of these populations have to be undisturbed and some have to be disturbed. Ideally, census data are required both before and after the impact, at all sites. Such Before-After-Control-Impact (BACI) designs are, unfortunately, the accepted approach to adequately demonstrate that a species-level impact is a consequence of the agent of interest. BACI designs are possible where study organisms are common, spatial scales are small, and the timing of the impact can be manipulated or accurately predicted. Unfortunately, none of these situations are true when we consider the impact of cane toads in Australia .

That a BACI design is likely to fail in assessing the impact of toads is evidenced by the fact that it has already been tried, producing largely ambiguous results. Between 1995-1997, CSIRO undertook an ambitious study, based on a BACI design, to determine the effects of toads on native fauna (Catling et al. 1999) . Despite some consideration of experimental design and probably for logistical/financial reasons, the final design was still insufficient to prove that changes in wildlife abundance were due to cane toads. Additionally, despite an immense survey effort, abundance data were so variable within sites that it is unlikely that any but the largest of impacts (i.e. near extinction) would have been detectable. Also, the study was insufficient to assess anything other than ecologically instantaneous population declines (i.e. declines occurring in less than 2-3 years.

Another BACI design is currently underway, using remote sensing of amphibian calls. This project has been hampered by technical difficulties and an unexpectedly rapid toad advance. Despite the study having run for more than several years and an indication that amphibian abundance has been affected, there are still insufficient data to conclusively prove that the effect is due to toads (H. McCallum, pers. comm.).

It is not our aim to criticise these studies. Arguably, they were worth trying and the latter study may yet yield enough rigorous data. Nevertheless, these two attempts show us that a BACI design is a huge logistical effort, so huge, in fact, that execution of the necessary experimental design is probably impossible within the bounds of current funding. Additionally, any results from such studies are retrospective: by the time an impact is demonstrated, it has already happened and management options have been reduced. Given that the Kimberley region is the last piece of northern Australia still cane toad free, any retrospective information will come too late.

Experimental Designs

Cane Toad impact mechanisms

An alternative to field-based studies is to examine potential impacts in an experimental setting. Experimentally investigating the potential impact of cane toads is, initially at least, a simple matter of determining the mechanisms by which the toads may have an impact and then testing whether these mechanisms work in the laboratory. Fortunately, the potential mechanisms by which toads may exert an impact are easily identifiable, Freeland (1987) identified four primary mechanisms. Cane Toads as:

• predators on native fauna;
• competitors with native fauna;
• toxic prey to native predators;
• vectors for disease.

Any of these mechanisms could have a direct impact on native species. Higher-order impacts as a consequence of changes in community structure flow from these basic four mechanisms.

With an experimental approach, we can systematically test each one of these mechanisms across many potentially impacted species. For example it is a simple question to ask, “Do toads eat native frogs?” If the answer is yes, then additional (equally tractable) questions arise. If the answer is no, then we can cross this interaction off as a potential impact. In this way we can very quickly build up an understanding of how toads have an impact and thus what their impact is likely to be.

In recent years, the focus on mechanisms of impact in an experimental setting has yielded quick leaps in our understanding of the potential impact of cane toads. For example, we know that some fish learn to avoid toads, and are rarely poisoned by them (Lawler & Hero 1997, Crossland 2001) and that aquatic invertebrates are successful predators on toad eggs and tadpoles , but that native tadpoles die when they eat toad spawn (Crossland 1998, Crossland & Alford 1998) .

Reptiles

Over the last couple of years, we have developed quantitative risk assessments for Australia ’s reptiles at risk of dying when attempting to eat cane toads. By determining how many species will share part of their range with toads and by testing representative species for their ability to tolerate toad toxin, we have derived a list of species potentially affected and, for snakes at least, an index of how badly each species may be affected.

We conclude that of our reptiles:

• 30% of Australia ’s terrestrial snakes;
• 59% of the agamids;
• 85% of the varanids;
• all of our crocodiles; and
• most of our freshwater turtles,

are potentially at risk from toad poisoning (Phillips et al. 2003, Smith & Phillips 2005) .

The species at risk in the Kimberley region are shown in Table 1. More alarmingly, almost all the reptiles we tested for resistance to toad toxin showed very low resistance levels and were easily capable of eating a toad large enough to be fatal. The exceptions to this general rule were the keelback snake (Tropidonophis mairii), the slatey-grey snake (Stegonotus cucullatus) and the saltwater crocodile (Crocodylus porosus) all of which showed relatively high resistance to toad toxins.

Native frogs, insectivores, invertebrates

Following the construction, near Darwin , of a permanent experimental facility consisting of 64 natural enclosures to investigate toad-related questions, we have been expanding our examination of the mechanisms of toad impact. This work has provided the first robust evidence that the presence of cane toads has a significant impact on both the diversity and abundance of floodplain invertebrates. Broadly, toads had a similar effect to an equivalent biomass of native frogs of the two species that we tested, Cyclorana australis and Litoria dahlii. Because cane toads can attain remarkably high population densities - much higher than those of native frogs (Freeland & Kerin 1988; van Dam et al. 2002) - the effects of these feral anurans on invertebrate communities often may be substantial. Changes in invertebrate biomass, and/or patterns of invertebrate diversity, are likely to have many flow-on effects on other native species. Reduction of food intake of other insectivores (e.g. frogs, planigales, lizards, passerine birds, larger invertebrates) and in turn, shifts in the abundance or distribution of such taxa could have yet other, secondary consequences for ecosystem processes (Spiller & Schoener 1994).

Table 1. Reptiles of the Kimberley potentially at risk from poisoning by toads. Range overlaps calculated based on the current and potential range of cane toads (data from Phillips et al. 2003; Smith & Phillips 2005). *Species with high resistance to toad toxin and which are thus unlikely to be affected.

Invertebrates are an important food source for other species (Dahl & Greenberg 1997; Park et al. 2001). However, invertebrates additionally play a diverse array of important ecological roles ranging from decomposers of organic matter (Graca 2001) through to seed dispersal agents (Wallace & Trueman 1995, Lindsey & Washok 2000). Indeed, they have been referred to as, ‘the little things that run the world’ ( Wilson 1987). The significance of ecological roles played by invertebrates, and the relative ease with which some invertebrate taxa can be sampled, has resulted in widespread use of invertebrates as bio-indicators for more generally focused management (Rosenberg et al. 1986, McGeogh 1998, Hoffmann & Andersen 2003, Andersen & Majer 2004). Our experiments suggest that invertebrates may be well suited to such a role in comparative studies of cane toad impact.

Ecological competition

Given that ecological competition is likely to be most intense between organisms that are relatively closely related, the most obvious competitors for cane toads are native frogs. We found that the presence of cane toads negatively impacts foraging success by one species of native frog (Cyclorana australis), but more information will be needed before we can evaluate the generality of this effect. We studied this locally occurring species because it is most similar to cane toads in body size and terrestrial habits; it may well be true that arboreal frogs, or those that select densely forested microhabitats that toads seldom use (Seabrook 1993) will experience less impact from toad arrival. These questions are entirely feasible for further study.

“Know the Enemy”

Our experiments demonstrate that it is feasible to explore the ecological impact of cane toads by conducting simple experiments designed to reveal the ways in which toads affect prey resources and potential competitors. Such work not only can provide objective evidence that cane toads do indeed modify natural systems, but can indicate the pathways by which such effects occur. Perhaps the most surprising aspect of the history of research on cane toads in Australia is that such studies have been delayed for so long. Military strategists have long exhorted us to, “know the enemy”, because a detailed understanding of the enemy (in this case, the cane toad) provides far better grounds for predicting future impacts, and for developing plans to mitigate such impacts, than does intuition or the simplistic assumptions that have guided control-oriented research to date. If Australian ecologists are to succeed in ameliorating the consequences of the introduction of cane toads to this continent, they are likely to do so only from a sound knowledge base about the biology of cane toads and the mechanisms by which they interact with native fauna. The experiments which we have so far conducted are an important step towards providing some of that information.

SUMMARY

 Our studies show that the mechanistic approach to investigating the impact of cane toads provides a relatively quick, cheap alternative to long-term, logistically difficult field studies. Importantly, results of experimental work can be used to predict the likely outcomes of toad invasion rather than simply provide an account of how quickly populations have declined. The results of experimental work can thus be used towards pro-active management of the cane toad threat. The best way to proceed at this point is to identify gaps in our current understanding of potential impacts and to address them. To this end, we are currently planning to experimentally investigate the effect of cane toads on small dasyurids (marsupial carnivores, eight species in the Kimberley ) that may be impacted either by attempting to eat small toads or by becoming food for larger toads. Absolutely no information is currently available regarding the effect of cane toads on this group. Generally speaking there is still very little known about the impact of cane toads as predators and competitors, and there is an excellent possibility of bringing the mechanistic approach to bear on these blank spots in our understanding.

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