Ecology, 96(9), 2015, pp. 2544–2554 Ó 2015 by the Ecological Society of America Invasive toads shift predator–prey densities in animal communities by removing top predators 1,2,6,7 2 3 4 5 J. SEAN DOODY, REBEKAH SOANES, CHRISTINA M. CASTELLANO, DAVID RHIND, BRIAN GREEN, 4 6 COLIN R. MCHENRY, AND SIMON CLULOW 1Department of Ecology and Evolutionary Biology, 569 Dabney Hall, University of Tennessee, Knoxville, Tennessee 37996-1610 USA 2Department of Biological Sciences, Monash University, Clayton, Victoria 3800 Australia 3Utah’s Hogle Zoo, 2600 Sunnyside Avenue, Salt Lake City, Utah 84108 USA 4Department of Anatomy and Developmental Biology, Monash University, Clayton, Victoria 3800 Australia 5Institute for Applied Ecology, University of Canberra, Australian Capital Territory 2601 Australia 6School of Environmental and Life Sciences, University of Newcastle, Callaghan, New South Wales 2308 Australia Abstract. Although invasive species can have substantial impacts on animal communities, cases of invasive species facilitating native species by removing their predators have rarely been demonstrated across vertebrate trophic linkages. The predictable spread of the invasive cane toad (Rhinella marina), however, offered a unique opportunity to quantify cascading effects. In northern Australia, three species of predatory monitor lizards suffered severe population declines due to toad-induced lethal toxic ingestion (yellow-spotted monitor [Varanus panoptes], Mertens’ water monitor [V. mertensi], Mitchell’s water monitor [V. mitchelli]). We, thus, predicted subsequent increases in the abundance and recruitment of prey species due to the reduction of those predators. Toad-induced population-level declines in the water monitor species approached 50% over a five-year period spanning the toad invasion, apparently causing fledging success of the Crimson Finch (Neochmia phaeton) to increase from 55% to 81%. The consensus of our original and published long-term data is that invasive cane toads are causing predators to lose a foothold on top-down regulation of their prey, triggering shifts in the relative densities of predator and prey in the Australian tropical savannah ecosystem. Key words: cane toad; common tree snake; Crimson Finch; Crocodylus johnstoni; Gilbert’s dragon lizard; monitor lizard; Neochmia phaeton; Rhinella marina; top predator; trophic cascade; Varanus spp. INTRODUCTION nities and ecosystems (Terborgh and Estes 2010, Trophic downgrading, or the disappearance of top Thomsen et al. 2010). As such, there is an urgent need consumers, including apex predators, may be one of the for research to forecast the effects of trophic downgrad- most pervasive anthropogenic influences on nature, and ing on future ecosystems (Estes et al. 2011). has been linked to a plethora of processes worldwide, Invasive species are a major threat to native species including biodiversity loss, the spread of invasive via individual direct effects such as predation, compe- species, wildfire frequency, disease transmission, and tition, and poisoning (reviewed in Simberloff and alterations in water, atmosphere, and soil (Estes et al. Rejmanek [2011]). If these individual effects are partic- 2011). The loss of top predators can influence biodiver- ularly strong, they may translate into population-level sity by shifting the relative abundance of species across impacts, or even extirpations and extinctions (Blackburn trophic levels (Eisenberg 2010). Theory predicts that the et al. 2004, Doody et al. 2009). If the affected species are largest impacts of the loss of predators will be on the predators, we would predict further shifts in communi- next trophic level down, manifest as ‘‘facilitation,’’ or ties and ecosystems via facilitation. Indeed, a major type the increase in density or biomass of one species through of facilitation is predatory release, or outbreaks, in its interaction with another (Thomsen et al. 2010). species caused by declines in top predators (Soule´et al. Facilitation is a recent addition to ecological theory, 1988). Although there are numerous examples of despite its ubiquity and importance for ecological and predatory release, there are few demonstrated cases of evolutionary processes (Bruno et al. 2003, Kikvidze and releases triggered by an invasive species across trophic Callaway 2009). At the biodiversity level, facilitation is levels of vertebrates (reviews in Rodriguez [2006], White now thought to play a major role in shaping commu- et al. [2006], Letnic et al. [2009]). Yet, invasive species that are dispersing in a predictable manner offer a unique opportunity to test predictions involving trophic Manuscript received 8 July 2014; revised 5 November 2014; cascades and trophic downgrading. accepted 18 November 2014; final version received 4 March 2015. Corresponding editor: J. B. Yavitt The (terrestrial) large mammal fauna of Australia is 7 E-mail: [email protected] depauperate relative to other continents, leaving mon- 2544 September 2015 TOADS SHIFT PREDATOR–PREY DENSITIES 2545 itor lizards to occupy a role of top or near-top predators level declines in previous studies (Letnic et al. 2008, (Johnson et al. 2007, Sutherland et al. 2010). However, Doody et al. 2009, 2014). Prey species of these predators Australian monitor lizards are evolutionarily naı¨ve to counted during these surveys were the Gilbert’s dragon the cane toad (Rhinella marina), a toxic invasive species (Lophognathus gilberti) and the common tree snake that poisons many predators that attempt to ingest it (Dendrelaphis punctulata). Five surveys were conducted (reviewed in Shine [2010]). The steady westward march annually during May–June 2009–2013 along the Ord of cane toads across tropical Australia offers an ideal River, Western Australia (15848030.0100 S, 128844015.1200 opportunity to use before-and-after studies to determine E to 128859006.2900 S, 128842014.7400 E; Fig. 1). Surveys the ecological impact of toads on native species, and were conducted under sunny conditions, and each research has revealed severe population-level declines in survey involved counts along 46 km of river during monitor lizards coincident with toad invasion (Griffiths 08:30–15:30 hours (Fig. 1). Surveys involved visual and McKay 2007, Doody et al. 2009, 2014, Ujvari and searching for target species on the shoreline, on trees Madsen 2009). Moreover, emerging from this research and logs, vegetation (terrestrial, emergent, and floating), was evidence for increases in the monitors’ prey and man-made structures (piers and docks). The boat following their demise (Doody et al. 2006, 2009, 2013, was kept between 7–10 m from the shoreline during Brown et al. 2011). surveys. There were three observers, including the Here, we address the prediction that cane toads are driver, and one scribe, who did not observe. Air and shifting the relative densities of predator and prey in water temperature were taken five times during each animal communities in the riparian ecosystem of survey at 08:30, 10:15, 12:30, 14:15, and 15:30 hours. tropical Australia, via direct impacts on monitor lizards and indirect impacts on their prey. We quantified the Crimson Finch fledging success relative abundance of predators and their prey for five To determine if toads facilitated Crimson Finches years spanning the arrival of the invasive cane toad, (Neochmia phaeton) by boosting fledging success, we including four species of predators (the monitor lizards used a snapshot nest appearance method to estimate Varanus mertensi, V. mitchelli, and V. panoptes, and the fledging success across 2011–2013 along 13 km of the freshwater crocodile Crocodylus johnstoni), and three Ord River (Fig. 1). We collected nests late in the nesting prey species of those predators (the Crimson Finch period (2011, N ¼ 42 nests; 2012, N ¼ 35 nests; 2013, N ¼ Neochmia phaeton, the Gilbert’s dragon lizard Lopho- 48 nests) and scored each nest as preyed upon or fledged, gnathus gilberti, and the common tree snake Dendrela- based on nest appearance and condition, presence of phis punctulata). We review published data for other feces or egg shells, and signs of damage, such as holes, species to update the overall ecological impact of cane tearing, or distorted entrances. toads on the vertebrate food web. To inform managers, We validated the snapshot method in 2011 by we predict future impacts of cane toads on animal comparing the estimate for each nest to its known fate; communities as they invade the last remaining toad-free the known fate was determined in an intensive study of area of tropical Australia. reproductive success of a larger sample of nests in 2011 that included the 42 nests in the above estimate (Soanes MATERIALS AND METHODS 2011). During the intensive study, visual searches for Toad surveys active finch nests among shoreline vegetation were To determine the timing of toad arrival, we conducted conducted by boat along the same 13 km of the Ord five annual 13 km long surveys of the M1 Channel Road, River used in the snapshot method (Fig. 1). When which runs parallel to the M1 Channel and stems from possible, adult birds were opportunistically followed for the Ord River, near Kununurra, Western Australia several minutes to attempt to discover their nest site, but (15841022.4100 S, 128844031.0800 Eto158470306200 S, the majority of nests were located directly, due to their 128843004.0500 E; Fig. 1, see Plate 1). Surveys were conspicuousness (in emergent Pandanus trees just above conducted by two observers and one driver on rainless water). Once located, the stage of each nest was nights at 19:30–21:00 h in late May and early June, 2009– determined (building, laying, incubation, or chick 2013, from a car travelling at 15 km/h. Surveys involved rearing) and its contents, such as the number of eggs visual searches for toads with the aid of spotlights. or chicks and chick developmental stage, were assessed. Notes on parent and chick behavior during monitoring Predator and prey surveys were also recorded. All active nests were checked by To determine direct effects of toads on the relative boat, on average, every three days until fledging or nest abundance of native predators, we used visual encounter failure occurred.