Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia

Abstract Cane toads (Bufo marinus) are large toxic anurans that have spread through much of tropical Australia since their introduction in 1935. Our surveys of the location of the toad invasion front in 2001 to 2005, and radiotracking of toads at the front near Darwin in 2005, reveal much faster westwards expansion than was recorded in earlier stages of toad invasion through Queensland. Since reaching the wet‐dry tropics of the Northern Territory, the toads have progressed an average of approximately 55 km year⁻¹ (mean rate of advance 264 m night⁻¹ along a frequently monitored 55‐km road transect during the wet season of 2004–2005). Radiotracking suggests that this displacement is due to rapid locomotion by free‐ranging toads rather than human‐assisted dispersal; individual toads frequently moved >200 m in a single night. One radiotracked toad moved >21 800 m in a 30‐day period; the fastest rate of movement yet recorded for any anuran. Daily displacements of radiotracked toads varied with time and local weather conditions, and were highest early in the wet season on warm, wet and windy nights. The accelerated rate of expansion of the front may reflect either, or both: (i) evolved changes in toads or (ii) that toads have now entered an environment more favourable to spread. This accelerated rate of expansion means that toads will reach the Western Australian border and their maximal range in northern Australia sooner than previously predicted.     

The spatial ecology of cane toads (Bufo marinus) in tropical Australia: Why do metamorph toads stay near the water?

Abstract Cane toads (Bufo marinus) have invaded large areas of Australia, killing many native predators as they have done so. The metamorph stage of the life cycle – the first terrestrial phase, immediately after transformation from the tadpole – is critical for ecological impact (because these animals are small enough to be prey for many native predators) and for potential control of toad populations (because small body size renders metamorphs vulnerable to desiccation). To quantify the spatial and temporal distribution of metamorph toads, and the biotic and abiotic factors that might affect their distributions, we surveyed toad breeding sites in Australia's wet‐dry tropics (Adelaide River floodplain, NT) in both the wet season and the dry season. Metamorphs were concentrated close to the water's edge during the dry season, especially at midday when desiccation rates were highest. During the wet season, metamorphs were widely dispersed through the landscape. Our surveys indicate that abiotic factors (risk of desiccation) are most favourable for metamorph toads close to the pond edge, but biotic factors (food supply, and risk of competition and cannibalism) are most favourable away from the water. Operative temperatures were spatially homogeneous and sublethal, and so are unlikely to influence metamorph distribution. Desiccation risk fluctuated on a diel cycle as well as seasonally. We predict that metamorph toads benefit from dispersing as soon as desiccation risk allows them to do so, and hence the distribution of metamorph toads will shift dynamically in response to weather‐mediated changes in rates of evaporative water loss.     

Behavioural flexibility allows an invasive vertebrate to survive in a semi-arid environment

Plasticity or evolution in behavioural responses are key attributes of successful animal invasions. In northern Australia, the invasive cane toad (Rhinella marina) recently invaded semi-arid regions. Here, cane toads endure repeated daily bouts of severe desiccation and thermal stress during the long dry season (April–October). We investigated whether cane toads have shifted their ancestral nocturnal rehydration behaviour to one that exploits water resources during the day. Such a shift in hydration behaviour could increase the fitness of individual toads by reducing exposure to desiccation and thermal stress suffered during the day even within terrestrial shelters. We used a novel method (acoustic tags) to monitor the daily hydration behaviour of 20 toads at two artificial reservoirs on Camfield station, Northern Territory. Remarkably, cane toads visited reservoirs to rehydrate during daylight hours, with peaks in activity between 9.00 and 17.00. This diurnal pattern of rehydration activity contrasts with nocturnal rehydration behaviour exhibited by adult toads in their native geographical range and more mesic parts of Australia. Our results demonstrate that cane toads phase shift a key behaviour to survive in a harsh semi-arid landscape. Behavioural phase shifts have rarely been reported in invasive species but could facilitate ongoing invasion success.     

Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone

Invasive species often encounter environmental conditions well outside those found in their native geographic ranges, and thus provide ideal model systems with which to explore responses to novel abiotic challenges. Within Australia, the invasive cane toad Rhinella marina has colonized areas that are considerably more arid than those found within its native range. Has the colonization of these novel environments been accompanied by shifts in physiology and/or locomotor performance? We measured rates of evaporative water loss, water gain, and effects of desiccation on locomotor performance of cane toads from two invasion fronts: one mesic (the wet‐dry tropics) and one arid (the semi‐desert). The two populations diverged substantially. Contrary to intuition (but consistent with intra‐specific comparisons between other toad populations from mesic vs arid areas), rates of evaporative water loss were lower (not higher) in toads from the mesic population. However, arid‐zone toads gained water more rapidly through their ventral surfaces, and rates of water loss and gain were highly correlated within individual toads from the arid‐zone population. Rates of water exchange in laboratory‐acclimated toads from the semi‐arid zone did not differ from those of free‐ranging conspecifics from the same population, suggesting that divergences between mesic and semi‐arid toads reflect genetic changes that have occurred during the species’ Australian invasion. Mesic and semi‐arid toads showed similar locomotor performance (endurance, distance per hop) when fully hydrated, but locomotor performance declined much more rapidly with desiccation in the mesic toads. Thus, within the short (decades‐long) timespan of the cane toad's Australian invasion, there has been substantial population divergence in the ability to withstand desiccating conditions. If we are to accurately predict the distributions (and hence impacts) of invading organisms, we will need to include adaptation potential in risk assessment schemes.     

Effects of an invasive anuran [the cane toad (Bufo marinus)] on the invertebrate fauna of a tropical Australian floodplain

The ways in which invasive organisms influence native ecosystems remain poorly understood. For example, feral cane toads Bufo marinus have spread extensively through tropical Australia over the last 70 years, but assessments of their ecological impact remain largely anecdotal. We conducted experimental trials to examine the effect of cane toad presence on invertebrate fauna in relatively small (2.4 × 1.2 m) outdoor enclosures on a floodplain near Darwin in the wet–dry tropics. Toads significantly reduced invertebrate abundance and species richness, but only to about the same degree as did an equivalent biomass of native anurans. Thus, if toads simply replaced native anurans, the offtake of invertebrates might not be substantially different from that due to native anurans before toad invasion. However, our field surveys suggest that toads cause a massive (fourfold) increase in total amphibian biomass. The end result is that cane toads act as a massive nutrient sink in the floodplain ecosystem because they consume vast numbers of invertebrates but (unlike native frogs) are largely invulnerable to predation by frog-eating predators.     

The impact of transportation and translocation on dispersal behaviour in the invasive cane toad

Biological invasions transport organisms to novel environments; but how does the translocation process influence movement patterns of the invader? Plausibly, the stress of encountering a novel environment, or of the transport process, might induce rapid dispersal from the release site—potentially enhancing (or reducing) invader success and spread. We investigated the effect of transportation and release to novel environments on dispersal-relevant traits of one of the world’s most notorious invaders, the cane toad (Rhinella marina). We collected toads in northern New South Wales from heath and woodland habitats, manipulated the level of transport stress and either returned toads to their exact collection point (residents) or reciprocally translocated them to a novel site. Both translocation and the level of transport stress drastically altered toad dispersal rates for at least 5 days post-release. Translocated toads (depending on their level of transport stress and release habitat) moved on average two to five times further per day (mean range 67–148 m) than did residents (mean range 22–34 m). Translocated toads also moved on more days, and moved further from their release point than did resident toads, but did not move in straighter lines. A higher level of transport stress (simulating long-distance translocation) had no significant effect on movements of resident toads but amplified the dispersal of translocated toads only when released into woodland habitat. These behavioural shifts induced by translocation and transportation may affect an invader’s ability to colonise novel sites, and need to be incorporated into plans for invader control.     

Invasive cane toads might initiate cascades of direct and indirect effects in a terrestrial ecosystem

Understanding the impacts that invasive vertebrates have on terrestrial ecosystems extends primarily to invaders’ impacts on species with which they interact directly through mechanisms such as predation, competition and habitat modification. In addition to direct effects, invaders can also initiate ecological cascades via indirect population level effects on species with which they do not directly interact. However, evidence that invasive vertebrates initiate ecological cascades in terrestrial ecosystems remains scarce. Here, we ask whether the invasion of the cane toad, a vertebrate invader that is toxic to many of Australia’s vertebrate predators, has induced ecological cascades in a semi-arid rangeland. We compared activity of a large predatory lizard, the sand-goanna, and abundances of smaller lizards preyed upon by goannas in areas of high toad activity near toads’ dry season refuges and areas of low toad activity distant from toads’ dry season refuges. Consistent with the hypothesis that toad invasion has led to declines of native predators susceptible to poisoning, goanna activity was lower in areas of high toad activity. Consistent with the hypothesis that toad-induced goanna decline lead to increases in abundance the prey of goannas, smaller lizards were more abundant in areas of high toad activity. Structural equation modelling showed a positive correlation between goanna activity and distance from dry season refuge habitats used by toads. The abundances of small lizards was correlated negatively with goanna activity and distance from dry season refuges of toads. Our findings provide support for the notion that invasions by terrestrial vertebrates can trigger ecological cascades.     

Behavioural tactics used by invasive cane toads (Rhinella marina) to exploit apiaries in Australia

Behavioural flexibility plays a key role in facilitating the ability of invasive species to exploit anthropogenically‐created resources. In Australia, invasive cane toads (Rhinella marina) often gather around commercial beehives (apiaries), whereas native frogs do not. To document how toads use this resource, we spool‐tracked cane toads in areas containing beehives and in adjacent natural habitat without beehives, conducted standardized observations of toad feeding behaviour, and ran prey‐manipulation trials to compare the responses of cane toads versus native frogs to honeybees as potential prey. Toads feeding around beehives travelled shorter distances per night, and hence used different microhabitats, than did toads from nearby control sites without beehives. The toads consumed live bees from the hive entrance (rather than dead bees from the ground), often climbing on top of one another to gain access to the hive entrance. Prey manipulation trials confirm that bee movement is the critical stimulus that elicits the toads’ feeding response; and in standardized trials, native frogs consumed bees less frequently than did toads. In summary, cane toads flexibly modify their movements, foraging behaviour and dietary composition to exploit the nutritional opportunities created by commercial beehives, whereas native anurans do not.     

Desiccation risk drives the spatial ecology of an invasive anuran (Rhinella marina) in the Australian semi-desert

Some invasive species flourish in places that impose challenges very different from those faced in their native geographic ranges. Cane toads (Rhinella marina) are native to tropical and subtropical habitats of South and Central America, but have colonised extremely arid regions over the course of their Australian invasion. We radio-tracked 44 adult cane toads at a semi-arid invasion front to investigate how this invasive anuran has managed to expand its geographic range into arid areas that lie outside of its native climatic niche. As predicted from their low physiological control over rates of evaporative water loss, toads selected diurnal shelter sites that were consistently cooler and damper (and thus, conferred lower water loss rates) than nearby random sites. Desiccation risk also had a profound influence on rates of daily movement. Under wet conditions, toads that were far from water moved further between shelter sites than did conspecifics that remained close to water, presumably in an attempt to reach permanent water sources. However, this relationship was reversed under dry conditions, such that only toads that were close to permanent water bodies made substantial daily movements. Toads that were far from water bodies also travelled along straighter paths than did conspecifics that generally remained close to water. Thus, behavioural flexibility--in particular, an ability to exploit spatial and temporal heterogeneity in the availability of moist conditions--has allowed this invasive anuran to successfully colonize arid habitats in Australia. This finding illustrates that risk assessment protocols need to recognise that under some circumstances an introduced species may be able to thrive in conditions far removed from any that it experiences in its native range.     

Toads in the backyard: why do invasive cane toads (Rhinella marina) prefer buildings to bushland?

Like many invasive species, cane toads (Rhinella marina) in Australia concentrate in the disturbed habitats created by human activity, rather than in pristine areas. We surveyed cane toads in the wet–dry tropics of the Northern Territory to assess the abundances, body sizes, sexes, behaviour, hydration state and feeding rates of toads around buildings compared to those in areas remote from buildings, and conducted experimental trials to assess the effects of building-related variables (lights and increased toad densities) on the foraging success of toads. Toads around buildings were smaller than bushland conspecifics, and adult sex-ratios were female-biased. Toads were more sedentary around buildings than in the bush, but their feeding rates (based on direct observations and faeces production post-capture) were similar. That similarity, despite twofold-higher densities of competing toads around building, reflected the strong enhancement of feeding rates due to artificial lights attracting insects (in our experimental trials, a threefold increase regardless of the number of competing toads). Toads collected from around buildings were apparently in better hydric condition. Thus, access to water also may attract toads to buildings. The relative scarcity of adult male toads around buildings likely reflects waterbody-centred reproductive activities, whereas the concentration of females and juveniles around buildings is driven largely by access to the insects attracted by artificial light. We conclude that buildings enhance the persistence of cane toad populations and may facilitate their spread.     

Interacting biocontrol programmes: invasive cane toads reduce rates of breakdown of cowpats by dung beetles

Ecological interactions among invasive species can affect not only the success of the invaders, but also their impact on ecosystems in the invaded range. In Australia, both dung beetles (subfamily Scarabaeinae) and cane toads (Rhinella marina) were introduced for biocontrol: the beetles to break down bovine faeces piles (cowpats) that otherwise accumulate and reduce pasture productivity, and the cane toad to consume scarab beetles that eat sugarcane and thus reduce sugar production. The dung beetles have been a success, whereas the toads have been a failure. Our experimental studies show that as well as impacting native fauna directly, cane toads reduce the rate of cowpat breakdown by consuming dung beetles. In the laboratory, dehydrated toads actively sought out cowpats based on scent cues, and in field enclosures, the presence of a cane toad significantly reduced rates of cowpat decomposition. Although toads have benefited from agricultural activities, their spread across Australia likely has reduced the effectiveness of one of the most successful biocontrol programmes ever conducted in that continent.     

Foraging responses of predators to novel toxic prey: effects of predator learning and relative prey abundance

Learning to avoid toxic prey items may aid native predators to survive the invasion of highly toxic species, such as cane toads Bufo marinus in tropical Australia. If the predators’ initial aversion is generalized, native prey that resemble the toxic invader may receive a benefit through accidental mimicry. What ecological factors influence the acquisition of learned avoidance (and hence, the impact of invasion on both predators and native prey)? We conducted laboratory experiments to evaluate how the relative abundance of toad tadpoles compared to palatable native tadpoles (Litoria caerulea and L. rubella) affected the ability of native aquatic predators to discriminate between these two prey types. Both fish (northern trout gudgeon, Mogurnda mogurnda) and frogs (Dahl's aquatic frog, Litoria dahlii) learned to discriminate between toads and frogs within an eight‐day period. Higher abundance of toad tadpoles relative to frog tadpoles enhanced rates of predator learning, and thus reduced predation on toads and increased predation on native tadpoles. In the field, spatial and temporal variation in the relative abundance of cane toads compared to native frogs may influence the rates at which these novel toxic items are deleted from predator diets, and the duration of predator protection afforded to natives that resemble the invader.     

Toad’s tongue for breakfast: exploitation of a novel prey type,the invasive cane toad,by scavenging raptors in tropical Australia

Although interest in the ecological impacts of invasive species has largely focused on negative effects, some native taxa may benefit from invader arrival. In tropical Australia, invasive cane toads (Bufo marinus) have fatally poisoned many native predators (e.g., marsupials, crocodiles, lizards) that attempt to ingest the toxic anurans, but birds appear to be more resistant to toad toxins. We quantified offtake of dead (road-killed) cane toads by raptors (black kites (Milvus migrans) and whistling kites (Haliastur sphenurus)) at a site near Darwin, in the Australian wet-dry tropics. Raptors readily took dead toads, especially small ones, although native frogs were preferred to toads if available. More carcasses were removed in the dry season than the wet season, perhaps reflecting seasonal availability of alternative prey. Raptors appeared to recognize and avoid bufotoxins, and typically removed and consumed only the toads’ tongues (thereby minimizing toxin uptake). The invasion of cane toads thus constitutes a novel prey type for scavenging raptors, rather than (as is the case for many other native predators) a threat to population viability.     

The extra-limital spread of an invasive species via 'stowaway' dispersal: toad to nowhere?

The mechanisms by which invasive species spread through new areas can influence the spatial scale of their impact. Although previous research has focused on 'natural' dispersal rates following initial introductions, human-aided inadvertent dispersal by 'stowaways' on commercial and domestic transport is thought to be a major contributor to long-distance dispersal. Few data exist to support this assumption. Cane toads Bufo marinus were introduced to north-eastern Australia in 1935, and have since dispersed rapidly through the tropics. Based on information accumulated by community groups in Sydney, 400 km south of the cane toads' current Australian distribution, we document high rates of translocation (at least 50 toads arriving in Sydney per year). Most toads were translocated on commercial truck transport carrying landscaping and building materials from the current range of the cane toads in New South Wales and Queensland, and resulted in highly clumped locations of toad arrival reflecting primary truck transport destinations. Most introductions involved single toads (68 of 102 translocation events), but some introductions involved two to 19 animals. Adults of both sexes were represented equally but juveniles were rarely detected. High rates of translocation of adult toads of both sexes suggest that the eventual distribution of cane toads in Australia may be limited by the animals' bioclimatic tolerances rather than by an inability to reach suitable habitats, even in areas far distant from the toads' current range.     

The Interacting Effects of Ungulate Hoofprints and Predatory Native Ants on Metamorph Cane Toads in Tropical Australia

Many invasive species exploit the disturbed habitats created by human activities. Understanding the effects of habitat disturbance on invasion success, and how disturbance interacts with other factors (such as biotic resistance to the invaders from the native fauna) may suggest new ways to reduce invader viability. In tropical Australia, commercial livestock production can facilitate invasion by the cane toad (Rhinella marina), because hoofprints left by cattle and horses around waterbody margins provide distinctive (cool, moist) microhabitats; nevertheless the same microhabitat can inhibit the success of cane toads by increasing the risks of predation or drowning. Metamorph cane toads actively select hoofprints as retreat-sites to escape dangerous thermal and hydric conditions in the surrounding landscape. However, hoofprint geometry is important: in hoofprints with steep sides the young toads are more likely to be attacked by predatory ants (Iridomyrmex reburrus) and are more likely to drown following heavy rain. Thus, anthropogenic changes to the landscape interact with predation by native taxa to affect the ability of cane toads in this vulnerable life-history stage to thrive in the harsh abiotic conditions of tropical Australia.     

Out of the frying pan: Reintroduction of toad‐smart northern quolls to southern Kakadu National Park

Invasive species are a leading cause of native biodiversity loss. In Australia, the toxic, invasive cane toad Rhinella marina has caused massive and widespread declines of northern quolls Dasyurus hallucatus. Quolls are fatally poisoned if they mistakenly prey on adult toads. To prevent the extinction of this native dasyurid from the Top End, an insurance population was set up in 2003 on two toad‐free islands in Arnhem Land. In 2015, quolls were collected from one of these islands (Astell) for reintroduction. We used conditioned taste aversion to render 22 of these toad‐naïve quolls toad averse. Seven quolls received no taste aversion training. The source island was also predator‐free, so all quolls received very basic predator‐aversion training. In an attempt to re‐establish the mainland population, we reintroduced these 29 northern quolls into Kakadu National Park in northern Australia where cane toads have been established for 13 years. The difference in survival between toad‐averse and toad‐naive quolls was immediately apparent. Toad‐naive quolls were almost all killed by toads within 3 days. Toad‐averse quolls, on the other hand, not only survived longer but also were recorded mating. Our predator training, however, was far less effective. Dingo predation accounted for a significant proportion of toad‐smart quoll mortality. In Kakadu, dingoes have been responsible for high levels of quoll predation in the past and reintroduced animals are often vulnerable to predation‐mediated population extinction. Dingoes may also be more effective predators in fire degraded landscapes. Together, these factors could explain the extreme predation mortality that we witnessed. In addition, predator aversion may have been lost from the predator‐free island populations. These possibilities are not mutually exclusive but need to be investigated because they have clear bearing on the long‐term recovery of the endangered northern quoll.     

Microbial biotransformation as a source of chemical diversity in cane toad steroid toxins

The cane toad is an invasive pest that is rapidly colonising northern Australia. The cane toad parotoid gland secretes cardiotoxic steroids (bufadienolides) that are poisoning native predator species. This study reveals bufadienolide diversity within the secretions of Australian cane toads is different to cane toads from overseas, being far more structurally diverse than previously assumed. It is proposed that this variation is mediated by in situ bacterial biotransformation.     

The impact of invasive cane toads on native wildlife in southern Australia

Commonly, invaders have different impacts in different places. The spread of cane toads (Rhinella marina: Bufonidae) has been devastating for native fauna in tropical Australia, but the toads' impact remains unstudied in temperate‐zone Australia. We surveyed habitat characteristics and fauna in campgrounds along the central eastern coast of Australia, in eight sites that have been colonized by cane toads and another eight that have not. The presence of cane toads was associated with lower faunal abundance and species richness, and a difference in species composition. Populations of three species of large lizards (land mullets Bellatorias major, eastern water dragons Intellagama lesueurii, and lace monitors Varanus varius) and a snake (red‐bellied blacksnake Pseudechis porphyriacus) were lower (by 84 to 100%) in areas with toads. The scarcity of scavenging lace monitors in toad‐invaded areas translated into a 52% decrease in rates of carrion removal (based on camera traps at bait stations) and an increase (by 61%) in numbers of brush turkeys (Alectura lathami). The invasion of cane toads through temperate‐zone Australia appears to have reduced populations of at least four anurophagous predators, facilitated other taxa, and decreased rates of scavenging. Our data identify a paradox: The impacts of cane toads are at least as devastating in southern Australia as in the tropics, yet we know far more about toad invasion in the sparsely populated wilderness areas of tropical Australia than in the densely populated southeastern seaboard.     

Cane toads a threat to West Indian wildlife: mortality of Jamaican boas attributable to toad ingestion

The notorious “cane toad” (Bufo marinus) is considered to be one of the 100 worst invasive species in the world. A native of South and Central America, Mexico, and the Rio Grande Valley of the United States, this large toad was intentionally introduced to islands in the Caribbean, and subsequently throughout the southern Pacific, as a biological control agent to combat sugar cane pests. Unfortunately, the primary result of those introductions has been deleterious impacts on native biotas, primarily through competition and predation. More recently, the cane toad has devastated populations of amphibian-eating predators in Australia, through the ingestion of this highly toxic anuran. Elsewhere, however, the impact of the toad on native predators has not been documented. Here we report the first evidence that the cane toad is impacting native predators in other geographic regions. Specifically, we document death due to cane toad poisoning in the endemic and threatened Jamaican boa (Epicrates subflavus). To our knowledge, this is the first report of cane toads causing mortality in naturally occurring predators outside of Australia. Like all members of the genus, B. marinus secretes a powerful bufogenin toxin, which is often fatal if ingested by naïve species that have not co-evolved with Bufo species. Our results should therefore serve as a warning that other endemic predator species in the West Indies and elsewhere may be at risk. Thus, efforts to control the population growth and spread of cane toads may be of even greater conservation concern than previously recognized.     

Adaptation or preadaptation: why are keelback snakes (<Emphasis Type="Italic">Tropidonophis mairii</Emphasis>) less vulnerable to invasive cane toads (<Emphasis Type="Italic">Bufo marinus</Emphasis>) than are other Australian snakes?

Biological invasions can expose native predators to novel prey which may be less nutritious or detrimental to predators. The introduction and subsequent spread of cane toads (Bufo marinus) through Australia has killed many anuran-eating snakes unable to survive the toad’s toxins. However, one native species, the keelback snake (Tropidonophis mairii), is relatively resistant to toad toxins and remains common in toad-infested areas. Is the keelback’s ability to coexist with toads a function of its ancestral Asian origins, or a consequence of rapid adaptation since cane toads arrived in Australia? And does the snake’s feeding preference for frogs rather than toads reflect an innate or learned behaviour? We compared keelback populations long sympatric with toads with a population that has encountered toads only recently. Unlike toad-vulnerable snake species, sympatry with toads has not affected keelback toxin tolerances or feeding responses: T. mairii from toad-sympatric and toad-naïve populations show a similar sensitivity to toad toxin, and a similar innate preference for frogs rather than toads. Feeding responses of neonatal keelbacks demonstrate that learning plays little or no role in the snake’s aversion to toads. Thus, behavioural aversion to B. marinus as prey, and physiological tolerance to toad toxins are pre-existing innate characteristics of Australian keelbacks rather than adaptations to the cane toad’s invasion of Australia. Such traits were most likely inherited from ancestral keelbacks that adapted to the presence of bufonids in Asia. Our results suggest that the impact of invasive species on native taxa may be strongly influenced by the biogeographic histories of the species involved.