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New Weapons in the Toad Toolkit: a Review of Methods to Control and Mitigate the Biodiversity Impacts of Invasive Cane

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New Weapons in the Toad Toolkit: a Review of Methods to Control and Mitigate the Biodiversity Impacts of Invasive Cane See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/316915049 New Weapons in the Toad Toolkit: A Review of Methods to Control and Mitigate the Biodiversity Impacts of Invasive Cane... Article in The Quarterly Review of Biology · June 2017 DOI: 10.1086/692167 CITATIONS READS 2 207 13 authors, including: Reid Tingley Robert J Capon University of Melbourne University of Queensland 47 PUBLICATIONS 1,042 CITATIONS 359 PUBLICATIONS 5,007 CITATIONS SEE PROFILE SEE PROFILE Richard Shine University of Sydney 1,087 PUBLICATIONS 40,853 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Accounting for imperfect detection in environmental DNA surveys View project Novel P-glycoprotein substrates and inhibitors in application to Multidrug Resistance View project All content following this page was uploaded by Simon Clulow on 14 May 2017. The user has requested enhancement of the downloaded file. Volume 92, No. 2 June 2017 THE QUARTERLY REVIEW of Biology NEW WEAPONS IN THE TOAD TOOLKIT: A REVIEW OF METHODS TO CONTROL AND MITIGATE THE BIODIVERSITY IMPACTS OF INVASIVE CANE TOADS (RHINELLA MARINA) Reid Tingley School of BioSciences, University of Melbourne Melbourne, Victoria 3010 Australia e-mail: [email protected] Georgia Ward-Fear School of Life and Environmental Sciences, University of Sydney Sydney, New South Wales 2006 Australia e-mail: [email protected] Lin Schwarzkopf College of Science and Engineering, James Cook University Townsville, Queensland 4811 Australia e-mail: [email protected] Matthew J. Greenlees School of Life and Environmental Sciences, University of Sydney Sydney, New South Wales 2006 Australia e-mail: [email protected] The Quarterly Review of Biology, June 2017, Vol. 92, No. 2 Copyright © 2017 by The University of Chicago Press. All rights reserved. 0033-5770/2017/9202-0001$15.00 123 124 THE QUARTERLY REVIEW OF BIOLOGY Volume 92 Benjamin L. Phillips School of BioSciences, University of Melbourne Melbourne, Victoria 3010 Australia e-mail: [email protected] Gregory Brown School of Life and Environmental Sciences, University of Sydney Sydney, New South Wales 2006 Australia e-mail: [email protected] Simon Clulow School of Environmental and Life Sciences, University of Newcastle Callaghan, New South Wales 2308 Australia e-mail: [email protected] Jonathan Webb School of Life Sciences, University of Technology Sydney Sydney, New South Wales 2007 Australia e-mail: [email protected] Robert Capon Institute for Molecular Bioscience, University of Queensland St. Lucia, Queensland 4072 Australia e-mail: [email protected] Andy Sheppard CSIRO Canberra, Australian Capital Territory 2601 Australia e-mail: [email protected] Tanja Strive CSIRO Canberra, Australian Capital Territory 2601 Australia e-mail: [email protected] Mark Tizard Australian Animal Health Laboratory, CSIRO Geelong, Victoria 3220 Australia e-mail: [email protected] June 2017 NEW WEAPONS IN THE TOAD TOOLKIT 125 Richard Shine School of Life and Environmental Sciences, University of Sydney Sydney, New South Wales 2006 Australia e-mail: [email protected] keywords Bufo marinus, conditioned taste aversion, containment, genome engineering, mitigation, suppression abstract Our best hope of developing innovative methods to combat invasive species is likely to come from the study of high-profile invaders that have attracted intensive research not only into control, but also basic biology. Here we illustrate that point by reviewing current thinking about novel ways to control one of the world’s most well-studied invasions: that of the cane toad in Australia. Recently developed methods for population suppression include more effective traps based on the toad’s acoustic and pheromonal biology. New tools for containing spread include surveillance technologies (e.g., eDNA sampling and automated call detectors), as well as landscape-level barriers that exploit the toad’s vulnerability to des- iccation—a strategy that could be significantly enhanced through the introduction of sedentary, range- core genotypes ahead of the invasion front. New methods to reduce the ecological impacts of toads in- clude conditioned taste aversion in free-ranging predators, gene banking, and targeted gene flow. Lastly, recent advances in gene editing and gene drive technology hold the promise of modifying toad pheno- types in ways that may facilitate control or buffer impact. Synergies between these approaches hold great promise for novel and more effective means to combat the toad invasion and its consequent impacts on biodiversity. Introduction fundamental biology of invaders by review- PREVENTING nonnative species from ing current ideas (most of them developed reaching new areas via quarantine is very recently) on ways to control and re- typically the most effective strategy to com- duce the ecological impact of the world’s bat biological invasions, although eradicating most intensively studied amphibian invasion: newly established populations can be feasi- the deliberate release and subsequent spread ble with intensive effort (Simberloff 2003). of the cane toad (Rhinella marina, formerly Once an invader begins to spread, however, Bufo marinus) in Australia (Figure 1). eradication success declines markedly, and Native to Latin America, these exception- substantial population reductions may be dif- ally large (up to more than 1 kg) and highly ficult to achieve. Effective control methods toxic anurans were released along the north- may take decades to develop and, with a few eastern coast of Australia in 1935 in a futile exceptions (Shanmuganathan et al. 2010), attempt to control insect pests in commer- are unlikely to succeed (Saunders et al. 2010). cial sugarcane plantations (Turvey 2013). Nonetheless, the potentially devastating eco- The toads have since spread at an increas- logical impacts of invasive species (Kraus 2015; ing rate across more than 1.2 million km2 Bellard et al. 2016) mean that we urgently of tropical and subtropical Australia (Urban need to develop and apply new control and et al. 2008), and have not yet filled their fun- mitigation methods. Our best hope of suc- damental niche, either in Australia (Kearney cess may come with high-profile pest spe- et al. 2008) or globally (Tingley et al. 2014). cies that have attracted intensive research Over the course of their Australian invasion, not only into control, but also basic biology cane toads have had devastating impacts on (Simberloff 2003). In this paper, we illus- native biodiversity (Shine 2010). In particu- trate the importance of understanding the lar, large anuran-eating predators (such as 126 THE QUARTERLY REVIEW OF BIOLOGY Volume 92 Figure 1. A Male Cane Toad From the Northern Territory, Australia Photo by Ben Phillips. See the online edition for a color version of this figure. marsupial quolls, freshwater crocodiles, var- ter et al. 2008, 2011), other viral-based, gene anid and scincid lizards, and elapid snakes) deletion and RNAi-based control strategies are fatally poisoned when they ingest the (Shanmuganathan et al. 2010), and sex-bias- toxic invaders. In many areas, toad invasion ing mechanisms (Koopman 2006; Mahony has caused precipitous declines in predator and Clulow 2006) have been considered and abundance (Letnic et al. 2008; Doody et al. occasionally (in the case of virally vectored 2009, 2014; Shine 2010; Jolly et al. 2015; strategies) extensively investigated (Hyatt et al. Fukuda et al. 2016). These declines have, in 2008). Their likelihood and context of suc- turn, had flow-on effects to other species cess for managing toads have also been ana- via trophic cascades (Brown et al. 2011b; lyzed (McCallum 2006; Thresher and Bax Doody et al. 2013, 2015). 2006), but technical obstacles (and concerns Despite considerable financial investment about unintended consequences) prevented (e.g., more than $20 million from 1986– their successful development and implemen- 2009; Commonwealth of Australia 2011), tation (Hyatt et al. 2008; Shannon and Bayliss the spread of cane toads across Australia has 2008). continued unabated. Initial control efforts in Consequently, when the state of efforts to the wet-dry tropics of northern Australia fo- control cane toads was last reviewed by the cused on manually collecting adult toads and Australian Federal Government in 2011, it have been largely unsuccessful. The feasi- seemed likely that the species would fully bility of more sophisticated genetic-based colonize its potential range before any suit- biocontrol methods, such as virally vectored able technology for broad-scale control be- autoimmunity (Robinson et al. 2006; Pallis- came available (Commonwealth of Australia June 2017 NEW WEAPONS IN THE TOAD TOOLKIT 127 2011). In its threat abatement plan, the Aus- trapping of adults to chemical suppression tralian Commonwealth therefore decided of larval development. to move away from broad-scale control and eradication, and focus instead on the pro- manual removal tection of key biodiversity assets, such as off- shore islands and priority native species and The earliest terrestrial stages of the cane ecological communities (Commonwealth toad are largely diurnal, and restricted to the of Australia 2011). Suitable approaches for margins of natal ponds during dry weather achieving that aim were largely unavailable conditions, particularly in the wet-dry tropics at the time, but a recent
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