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.     

Evaluation of the toxicity of eggs,hatchlings and tadpoles of the introduced toad Bufo marinus (Anura: Bufonidae) to native Australian aquatic predators

Abstract The early life history stages of anurans in the Family Bufonidae often possess chemicals that are noxious or toxic to predators. Predators with no evolutionary history of exposure to bufomds may be particularly susceptible to these toxins. We conducted a series of laboratory experiments to investigate the toxic effects of eggs, hatchlings and tadpoles of the introduced toad, Bufo marinus (Linnaeus), on native Australian aquatic predators. There was considerable interspecific and intraspecific variation in these effects. Bufo marinus were highly toxic to some predator species, but were readily consumed by other species without apparent ill effect. Interspecific variation in toxic effects was not related to predator feeding mode or the number of B. marinus ingested by predators, and there was no clear pattern of distribution of vulnerability among species within higher taxa. Intraspecific variation in responses to toxins may result from individual variation in the resistance of predators to B. marinus toxins, or from individual variation in toxicity among B. marinus. Some native species adversely affected by B. marinus appeared unable to detect and avoid B. marinus toxins. This may result from a general inability to assess the toxicity of food items or from a lack of evolutionary exposure to B. marinus toxins.     

A native dasyurid predator (common planigale,Planigale maculata) rapidly learns to avoid a toxic invader

Abstract Interactions between invasive species and native fauna afford a unique opportunity to examine interspecific encounters as they first occur, without the complications introduced by coevolution. In northern Australia, the continuing invasion of the highly toxic cane toad Bufo marinus poses a threat to many frog‐eating predators. Can predators learn to distinguish the novel toxic prey item from native prey (and thus, avoid being poisoned), or are longer‐term genetically based changes to attack behaviour needed before predators can coexist with toads? To predict the short‐term impact of cane toads on native predators, we need to know the proportion of individuals that will attack toads, the proportion surviving the encounter, and whether surviving predators learn to avoid toads. We quantified these traits in a dasyurid (common planigale, Planigale maculata) that inhabits tropical floodplains across northern Australia. Although 90% of naïve planigales attacked cane toads, 83% of these animals survived because they either rejected the toad unharmed, or killed and consumed the prey snout‐first (thereby avoiding the toxin‐laden parotoid glands). Most planigales showed one‐trial learning and subsequently refused to attack cane toads for long time periods (up to 28 days). Toad‐exposed planigales also avoided native frogs for up to 9 days, thereby providing an immediate benefit to native anurans. However, the predators gradually learnt to use chemical cues to discriminate between frogs and toads. Collectively, our results suggest that generalist predators can learn to distinguish and avoid novel toxic prey very rapidly – and hence, that small dasyurid predators can rapidly adapt to the cane toad invasion. Indeed, it may be feasible to teach especially vulnerable predators to avoid cane toads before the toads invade, by deploying low‐toxicity baits that stimulate taste‐aversion learning.     

Geographical patterns of genetic variability in introduced Australian populations of the marine toad,Bufo marinus: Sorbitol dehydrogenase,Sdh

The marine toad, Bufo marinus, was introduced to Australia from Hawaii in 1935. From 1935 to 1974, the toad population expanded exponentially to occupy 584,000 km², and now has a continuous distribution from Cape York to Tweed River on the eastern coast of the continent. Genetic analysis of the population indicates a difference in allele frequency at the sorbitol dehydrogenase locus. There are two alleles segregating at the locus (NAD-Sdh^a and NAD-Sdh^b). The NAD-Sdh^aa homozygote is common in the two southern populations, but uncommon in northern populations. The north-south difference has been established in less than 25 generations.     

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.     

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.     

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.     

Cues for cannibalism: cane toad tadpoles use chemical signals to locate and consume conspecific eggs

Although animals of many species kill and consume conspecifics, most such cases probably involve serendipitous encounters between the individuals concerned. In some taxa, however, cannibalism is an active process, with predatory individuals searching out and consuming specific types of conspecific prey items. Although anuran tadpoles often have been reported to consume conspecific eggs, this behaviour has been interpreted as a by‐product of usual foraging behaviours rather than a result of targeted searching. Our field and laboratory studies in tropical Australia show that the tadpoles of invasive cane toads Bufo marinus are strongly attracted to chemical cues from conspecific eggs; the effective cues are released late in embryonic development, as the jelly coat breaks down. Tadpoles of native Australian frog species were attracted to the eggs of toads only rarely. If deployed as bait in traps, chemical cues from toad eggs could provide a way to selectively remove toad larvae from waterbodies.     

Behavioural responses of native predators to an invasive toxic prey species

One important impact of invasive species may be to modify the behaviour of native taxa. For example, the invasion of highly toxic cane toads (Bufo marinus) kills many anurophagous native predators, but other predators learn to recognize and avoid the toxic invader. We exposed native fish (northern trout gudgeons, Mogurnda mogurnda) and Dahl's aquatic frogs (Litoria dahlii) to cane toad tadpoles, then monitored the predator's responses during subsequent trials. Both the frogs and fish initially attacked toad tadpoles, but rapidly learned not to do so. Fish and adult frogs retained their aversion for at least a week, whereas recently metamorphosed frogs did not. Clearly, the spread of cane toads through tropical Australia can modify feeding responses of native aquatic predators. For predators capable of rapid avoidance learning, the primary impact of cane toads may be on foraging behaviour rather than mortality.     

Impacts of eggs and tadpoles of the invasive cane toad (Bufo marinus) on aquatic predators in tropical Australia

Invasive species affect native ecosystems in a variety of ways, and the magnitude of impact may depend upon many factors. In an invading species such as the cane toad (Bufo marinus), the multiphasic life history creates a potential for impact to differ between life history stages. Previous research on the impact of cane toads in Australia has focused on fatal poisoning of predators that ingest terrestrial stages of the toad, but aquatic stages (eggs, larvae) are toxic also. We exposed nine native Australian fish species and one native Australian turtle species to the eggs and larvae of toads. Strong species differences were evident, both in palatability (propensity to attack the egg or larva), and in subsequent responses (e.g. taste and reject the item, vs. ingest it). Toad eggs were less likely than toad tadpoles to be attacked, but also less likely to be rejected before ingestion (probably because the non‐toxic jelly coat masks the presence of toxins in the ovum). As a result, predators were far more likely to be killed by ingesting toad eggs than toad tadpoles. Fortuitously, the spatial and temporal availability of toad egg masses restricts encounter rates with predators, so that overall ecological impact may be low despite the high vulnerability of a fish or turtle that encounters such an egg mass. Understanding such ontogenetic shifts in the nature of interactions and magnitude of impact is crucial if we are to understand the overall ecological impact of invasive species.     

Do invasive cane toads (Chaunus marinus) compete with Australian frogs (Cyclorana australis)?

Abstract Despite widespread concern about the ecological impacts of invasive species, mechanisms of impact remain poorly understood. Cane toads (Chaunus [Bufo] marinus) were introduced to Queensland in 1935, and have now spread across much of tropical Australia. One plausible impact of toad invasion concerns competition between toads and native frogs, but there has been no previous experimental evaluation of this possibility. We examined interactions between toads and a morphologically similar species of native frog (Cyclorana australis) by manipulating toad and frog densities within large outdoor enclosures beside a floodplain in the wet‐dry tropics of the Northern Territory. Toads differed from frogs significantly in dietary composition and feeding rates, even in comparisons controlling for body‐size differences between these two taxa. Perhaps reflecting the abundant insect biomass, manipulating anuran densities or the presence of the putatively competing species did not influence food intake or dietary composition. However, the presence of toads suppressed activity levels of native frogs. The degree to which the invasion of cane toads influences attributes such as the activity levels, food intake and dietary composition of native frogs warrants further study, but our study suggests that competitive effects are likely to be minor compared with other pathways (such as direct poisoning during ingestion attempts) by which toads can affect frog populations.     

Skull allometry in the marine toad,Bufo marinus

Scaling predictions pioneered by A.V. Hill state that isometric changes in kinematics result from isometric changes in size. These predictions have been difficult to support because few animals display truly isometric growth. An exception to this rule is said to be the toads in the genus Bufo, which can grow over three orders of magnitude. To determine whether skull shape increases isometrically, I used linear measurements and geometric morphometrics to quantify shape variation in a size series of 69 skulls from the marine toad, B. marinus. Toads ranged in body mass from 1.8 gm to a calculated 1,558.9 gm. Of all linear measurements (S/V length, skull width, skull length, levator mass, depressor mass, adductor foramen area), only the area of the adductor foramen increased faster than body mass; the remaining variables increased more slowly. In addition, modeling the lower jaw as a lever‐arm system showed that the lengths of the closing in‐ and out‐levers scaled isometrically with body mass despite the fact that the skull itself is changing allometrically. Geometric morphometrics discerned areas of greatest variability with increasing body mass at the rear of the skull in the area of the squamosal bone and the adductor foramen. This increase in area of the adductor foramen may allow more muscle to move the relatively greater mass of the lower jaw in larger toads, although adductor mass scales with body mass. If B. marinus feeds in a similar manner to other Bufo, these results imply that morphological allometry may still result in kinematic isometry. J. Morphol. 241:115–126, 1999. © 1999 Wiley‐Liss, Inc.     

Factors affecting the vulnerability of cane toads (Bufo marinus) to predation by ants

Experimental evidence on the determinants of prey vulnerability is scarce, especially for vertebrates in the field. Invasive species offer robust opportunities to explore prey vulnerability, because the intensity of predation on or by such animals has not been eroded by coevolution. Around waterbodies in tropical Australia, native meat ants (Iridomyrmex reburrus) consume many metamorph cane toads (Bufo marinus, an invasive anuran). We document the determinants of toad vulnerability, especially the roles of toad body size and ant density. Larger metamorphs were attacked sooner (because they attracted more ants), but escaped more often. Overall, smaller toads were more likely to be killed. Ant densities influenced toad responses, as well as attack rate and success. Data on the immediate outcomes of attacks underestimate mortality: more than 73% of apparent ‘escapees’ died within 24 h. Because mortality during this period was independent of toad size, predation was less size selective than suggested by immediate outcomes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 738–751.     

Behavioural responses of carnivorous marsupials (Planigale maculata) to toxic invasive cane toads (Bufo marinus)

The arrival of a toxic invasive species may impose selection on local predators to avoid consuming it. Feeding responses may be modified via evolutionary changes to behaviour, or via phenotypic plasticity (e.g. learning, taste aversion). The recent arrival of cane toads (Bufo marinus) in the Northern Territory of Australia induced rapid aversion learning in a predatory marsupial (the common planigale, Planigale maculata). Here, we examine the responses of planigales to cane toads in north‐eastern Queensland, where they have been sympatric for over 60 years, to investigate whether planigale responses to cane toads have been modified by long‐term exposure. Responses to toads were broadly similar to those documented for toad‐naïve predators. Most Queensland planigales seized (21 of 22) and partially consumed (11 of 22) the first toad they were offered, but were likely to ignore toads in subsequent trials. However, unlike their toad‐naïve conspecifics from the Northern Territory, the Queensland planigales all survived ingestion of toad tissue without overt ill effects and continued to attack toads in a substantial proportion of subsequent trials. Our data suggest that (i) learning by these small predators is sufficiently rapid and effective that selection on behaviour has been weak; and (ii) physiological tolerance to toad toxins may be higher in planigales after 60 years (approximately 60 generations) of exposure to this toxic prey.     

Ecological impacts of invading species: Do parasites of the cane toad imperil Australian frogs?

Parasite transfer to native fauna is a potentially catastrophic impact of invasive species. Introduced cane toads in Australia frequently host the nematode lungworm Rhabdias pseudosphaerocephala, which reduces viability of metamorph toads. If native frogs are vulnerable to this South American parasite, cane toad invasion may affect native species via this route; but if the native taxa are not vulnerable, we may be able to exploit the parasites for managing toads. Our laboratory experiments show that infective larvae can penetrate the body of all seven species of Australian frogs (five hylids: Cyclorana longipes, Litoria caerulea, Litoria dahlii, Litoria nasuta, Litoria rothii, one myobatrachid: Opisthodon ornatus, and one limnodynastid: Limnodynastes convexiusculus) we tested, but most did not host the adult worms at the end of the trials, and none showed major impairment of growth, survival or locomotor performance. One native tree‐frog (L. caerulea) retained high infection levels with few ill effects, suggesting that we might be able to use this taxon as a reservoir species to build up local parasite densities for toad management. However, the interspecific variation in lungworm retention suggests that generalizations about parasite effects on native frogs will be elusive.     

Effects of invasive cane toads on Australian mosquitoes: Does the dark cloud have a silver lining?

Research on the ecological impacts of invasive organisms typically looks only for negative impacts, ignoring the possibility that the wider community might see benefits in some of these effects. To truly understand the impact of invasive species, we need to look as broadly as possible, and incorporate studies on a diversity of variables. The spread of the South American cane toad (Bufo marinus) through tropical Australia is widely viewed as an ecological catastrophe, but anecdotal reports suggest that the invasion of toads may reduce the numbers of mosquitoes (and thus, potentially, the risk they pose to human health). We conducted experiments to determine whether the presence of toad tadpoles affects survival rates, adult body sizes and/or rates of oviposition of four species of disease-carrying mosquitoes. In the laboratory, the presence of toad tadpoles significantly reduced the sizes of adult mosquitoes at emergence, and also reduced survival rates of the larvae of one mosquito species. In field trials, mosquitoes were less likely to oviposit in waterbodies containing toad tadpoles. Accordingly, these data suggest (but do not prove) that toad invasion may reduce mosquito abundance. More generally, any overall evaluation of the impact of an invasive species needs to consider possible benefits (e.g. to human health) as well as negative effects (e.g. to native species). Both types of information are essential to inform community decisions about the management of feral taxa such as the cane toad in Australia.     

Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park,Tanzania

The release of any species into a novel environment can evoke transmission of parasites that do not normally parasitize the host as well as potentially introducing new parasites into the environment. Species introductions potentially incur such risks, yet little is currently known about the parasite fauna of introduced primate species over the long term. We describe the results of long‐term monitoring of the intestinal parasite fauna of an unprovisioned, reproducing population of chimpanzees introduced 40 years earlier (1966–1969) onto Rubondo Island in Lake Victoria, Tanzania, a non‐native habitat for chimpanzees. Two parasitological surveys (March 1997–October 1998 and October 2002–December 2005) identified Entamoeba spp. including E. coli, Iodamoeba buetschlii, Troglodytella abrassarti, Chilomastix mesnili, Trichuris sp., Anatrichosoma sp., Strongyloides spp., Strongylida fam. gen. sp., Enterobius anthropopitheci, Subulura sp., Ascarididae gen. sp., and Protospirura muricola. The parasite fauna of the Rubondo chimpanzees is similar to wild chimpanzees living in their natural habitats, but Rubondo chimpanzees have a lower prevalence of strongylids (9%, 3.8%) and a higher prevalence of E. anthropopitheci (8.6%, 17.9%) than reported elsewhere. Species prevalence was similar between our two surveys, with the exception of Strongyloides spp. being higher in the first survey. None of these species are considered to pose a serious health risk to chimpanzees, but continued monitoring of the population and surveys of the parasitic fauna of the two coinhabitant primate species and other animals, natural reservoir hosts of some of the same parasites, is important to better understand the dynamics of host–parasite ecology and potential long‐term implications for chimpanzees introduced into a new habitat. Am. J. Primatol. 72:307–316, 2010. © 2009 Wiley‐Liss, Inc.     

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.