Author: John Carter

Invasive species as drivers of evolutionary change: cane toads in tropical Australia PMC

We predicted a priori that yellow-spotted monitors would be more difficult to detect by active search surveys compared with lace monitors. Accordingly, cameras were deployed in sites with yellow-spotted monitors for 120 h (total 40 camera days/nights per site). In the case of invasive predators that consume native prey, selection may favor rapid adaptive responses in the endemic fauna to detect and avoid the unwelcome new arrival. For example, the arrival of mammalian predators (rats, stoats, cats, possums, etc.) may have exerted intense selection on New Zealand lizards. The absence of mammalian predators on these islands over evolutionary time presumably fashioned lizard biology in ways that reduced their vulnerability to visually hunting birds, but were ineffective against mammalian predators that use chemosensory cues for hunting (Hoare et al. 2007).

This effect can be amplified if the invader exerts disproportionally large impacts on certain functional groups within the system (e.g., predator guilds). In some cases, the negative impacts of an invasion will be short-lived [9]; but in other cases, populations of an imperilled taxon continue to decline post-invasion, eventually resulting in extinction [10, 11]. What can be concluded, overall, about the impacts of the invasive cane toad (Rhinella marina) on the abundance, diversity, and composition of Australian wildlife? Although brief, our study incorporated more spatial replication and “control” sites than have been possible in the wet–dry tropics (Doody et al. 2006, 2009, 2013; Letnic et al. 2008; Phillips et al. 2010; Brown et al. 2011, 2013b; Ujvari et al. 2011). The ability to compare faunal assemblages between areas that differ mostly in exposure to toads (rather than in environmental factors) provides convincing evidence of population‐level declines in native taxa due to toad arrival.

1. A small toad offers a nauseating but nonfatal meal that may allow aversion learning by predators, thereby ameliorating population‐level impact (O’Donnell, Webb & Shine 2010).
2. We thank Parks staff, especially Rod Hobson, for donating their time and expertise, and for assistance with field logistics.
3. Additionally, our study provides evidence of invader impact in a region that heretofore has been largely ignored.
4. Impact heterogeneity necessitates studies at multiple locations throughout an invader’s range (Parker et al. 1999; Melbourne et al. 2007).

Broadly, the sites where yellow-spotted monitors have persisted despite the presence of cane toads appear to contain unusually high availability of alternative prey. This anecdotal correlation between varanid abundance and food availability needs to be explored with more extensive surveys, that document the food-resource base as well as varanid numbers. For east coast sites, each survey consisted of a 15-min active search on foot around focal campsites (areas to which lace monitors are attracted) [16], and a 45-min search along a 5-km transect in a vehicle (paved and unpaved roads were used for transects). Morning surveys commenced from 0900 to 1200 h, afternoon surveys from 1200 to 1800 h, and nocturnal surveys from 1800 to 0100 h. In tropical Australia, yellow-spotted monitors are most active on relatively cool mornings [33]. Accordingly, at the twenty-four sites in our northern transect, morning surveys consisted of a 1-h active search on foot along a 2 km transect adjacent to focal wetlands, lakes, rivers, creeks, billabongs and floodplains (areas frequented by yellow-spotted monitors) 33.

We predicted that native fauna that prey on toads would be less abundant in toad‐invaded areas than in areas that did not contain toads. We also surveyed habitat variables to test for potential confounding factors between invaded versus uninvaded sites, and measured rates of carrion removal to test the hypothesis that this critical ecological function would be affected by toad‐induced declines of scavengers. In the present study, we provide data from a large-scale sampling of apex predator populations vulnerable to invasion by a toxic amphibian. Short-term studies have reported catastrophic population declines in larger species of the lizard genus Varanus immediately following the arrival of cane toads (Rhinella marina) [16–19], but subsequent trajectories of predator populations remain unclear.

Accordingly, we need to assess invader impacts in the context of other changes that interact synergistically or antagonistically over time [13], or affect ecosystem or species resilience [14]. For example, a warming climate may present new opportunities for non-native species to invade areas that were previously outside their thermal tolerances, increasing their impact [15]. Impacts of cane toad presence on (A) mean abundance per site (± SE) and (B) mean species richness per site (± SE) of native fauna encountered in campgrounds and surrounding bushland areas in northeastern New South Wales, Australia. Using JMP Pro 9.0, we compared the number of chicken necks removed from bait stations (both in campgrounds and in surrounding bushland) in both toad‐present and toad‐absent sites. The number of baits removed per bait station was the dependent variable, and toad exposure (two levels; toad present vs. absent) and location (two levels; campground vs. bushland) were the independent variables in a two‐way analysis of variance (ANOVA).

INVASIVE SPECIES

Impacts of cane toad presence and habitat type on mean number (± SE) of chicken necks removed from camera‐monitored bait stations in campgrounds and surrounding bushland areas in toad‐present and toad‐absent areas of northeastern New South Wales, Australia. The parallel effects on invaders and natives of biotic interactions are more clear-cut and may influence establishment success (Strauss et al. 2006b; Tingley et al. 2011) as well as subsequent adaptive shifts (Langkilde 2009). Either or both the invader and the native may be affected by competition, predation, herbivory, toxic ingestion, pathogen transfer, or hybridization between taxa (Fig. 1).

We may see evolutionary changes in the invader, in native species directly impacted by it, and in species influenced indirectly via their interactions with affected native taxa. Many systems are under simultaneous challenge from multiple invaders, adding to the complexity of response. The traits affected also are diverse, ranging through morphology, ecology, life history, physiology, and behavior. The interspecific interactions may involve relationships such as predation, herbivory, pathogen transfer, interference or exploitative competition, evolutionary traps (such as consuming a lethally toxic invader that resembles a harmless native prey species), and hybridization.

However, using simulations we have shown that a practical and cost-effective approach to control cane toads would be to strategically create “toad breaks” to disrupt the network of refuge habitats available for toads. Control of toads at invasion hubs could be conducted reactively to control established populations or prevent the spread of toads by rendering invasion hubs unsuitable for colonization ahead of the invasion front. The two varanid species are broadly similar in body sizes and general morphology (Fig 1) as well as in their general biology, including broad diet [38]. The most obvious difference between the two taxa lies in the habitats they occupy, in turn linked to climatic conditions over their distributions. The lace monitor inhabits forested areas, where ambient temperatures change seasonally and precipitation ranges from relatively aseasonal (southern regions) to seasonal (tropical regions).

Study sites

For librarians and administrators, your personal account also provides access to institutional account management. Here you will find options to view and activate subscriptions, manage institutional settings and access options, access usage statistics, and more. We thank all Traditional Owners for access to Country, and the Yawuru Country Managers, Bunuba Rangers, and Balanggarra Rangers for their assistance in the field. We thank Parks staff, especially Rod Hobson, for donating their time and expertise, and for assistance with field logistics.

They are not protected by state, federal or local laws because they are invasive and unwanted. The toads are more common in developed areas, especially near canals and freshwater retention ponds, and in agriculture communities. If that’s not gross enough, they also have large triangular glands behind their heads that excrete a highly toxic white goo when the toads are stressed or grabbed. For full access to this pdf, sign in to an existing account, or purchase an annual subscription. Shibboleth/Open Athens technology is used to provide single sign-on between your institution’s website and Oxford Academic. The poison, called bufotoxin, contains several different chemicals, such as bufagin, which affects the heart, and bufotenine, a hallucinogen.

According to this hypothesis, the impact of cane toads on apex predators has been exacerbated and prolonged by a scarcity of alternative prey. More generally, multiple anthropogenically-induced changes to natural ecosystems may have synergistic effects, intensifying the impacts beyond that expected from either threat in isolation. Cane toads (Rhinella marina) are large toxic anurans native to South and Central America, and introduced to tropical Australia in 1935 in the futile hope that they would help control insect pests in commercial sugar-cane plantations. Because Australia lacks native toads, the ecological impact of cane toads has been devastating for some species of native predators (snakes, lizards, crocodiles, marsupial carnivores) that attempt to eat toads, and are killed by the toads’ powerful poisons.

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A small toad offers a nauseating but nonfatal meal that may allow aversion learning by predators, thereby ameliorating population‐level impact (O’Donnell, Webb & Shine 2010). Importantly, our analyses suggest that the impact of an invasive species (the cane toad) on a native predator (the yellow-spotted monitor) was exacerbated by a reduction in prey availability, likely due to other anthropogenic changes to the landscape. For example, predation by cats has devastated populations of small mammals across much of tropical Australia [59]. This example highlights the interactive effects of multiple ecosystem stressors in driving population declines of native species, and in preventing recovery after population collapse [69, 70].

In this review, I will examine ideas and evidence on the evolutionary consequences of biological invasions, with a strong focus on one study system – the invasion of cane toads through tropical Australia. The destabilizing effects of biological invasions on host–parasite relationships remain a substantial challenge for future research. Other parasites may benefit from the invader’s arrival, for example, myxosporidians that occupy anuran bladders have increased in frequency among Australian frogs since the cane toad’s arrival (Hartigan et al. 2010).

Importantly for the practical application of these findings, the approaches we have devised do not impinge on the ability of livestock to obtain water, because in most situations in northern Australia livestock drink from troughs not the dams themselves. Also, the native fauna of arid Australia are arid adapted and thus unlike cane toads are not dependent or unduly impacted by exclusion from artificial water sources. Impacts of processes such as climate change, habitat degradation, and pollution can interact with invasive species to modify the direction, magnitude or duration of invader impact.

Invasive species as drivers of evolutionary change: cane toads in tropical Australia

Nonchalance among the general public appears to have had flow‐on effects for political and research priorities. Data on the three lizard taxa were assessed independently because they were identified as having declined by SIMPER. The abundance of P. porphyriacus was assessed because this species has been anecdotally reported to experience severe toad‐imposed population declines (Rayward 1974; Covacevich and Archer 1975; Fearn 2003; Phillips et al. 2003; Phillips & Fitzgerald 2004). Using JMP Pro 9.0, we compared the abundance of each species between sites where toads were present versus absent (independent variable). Because the abundance data of these individual species could not be normalized via transformation, data were analyzed using nonparametric Kruskal–Wallis analysis of variance tests (Crossland 1998; Ujvari et al. 2011; Crossland and Shine 2012). The lace monitor (Varanus varius; Fig 1, top panel) is found along the eastern coast of Australia [25], and can grow to 14 kg and exceed 2 metres in total length.