Mechanisms of competition between tadpoles of Australian frogs (Litoria spp.) and invasive cane toads (Rhinella marina)

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Competing tadpoles: Australian native frogs affect invasive cane toads (Rhinella marina) in natural waterbodies

The cane toad (Rhinella marina) is one of the most successful invasive species worldwide, and has caused significant negative impacts on Australian fauna. Experimental work in the laboratory and in mesocosms has shown that tadpoles of native frogs can affect survival, size at metamorphosis and duration of larval period of cane toad tadpoles. To test if these effects occur in nature, we conducted a field experiment using two temporary ponds where we set up enclosures with tadpoles of native green tree frogs (Litoria caerulea) and cane toads in treatments with a range of densities and combinations. The presence of green tree frog tadpoles significantly decreased the growth rate of toad tadpoles and increased the duration of their larval period in both ponds; in one pond, frog tadpoles also significantly reduced the body length and mass of metamorph toads. Toad tadpoles did not have any significant negative effects on green tree frog tadpoles, but there was strong intraspecific competition within the latter species: increased frog tadpole density resulted in increased larval period and reduced survival, growth rate and size at metamorphosis for frogs at one or both ponds. Our results are encouraging for the possibility of using native frogs as one component of an integrated approach to the biological control of cane toads.     

Moving south: effects of water temperatures on the larval development of invasive cane toads (Rhinella marina) in cool‐temperate Australia

The distributional limits of many ectothermic species are set by thermal tolerances of early‐developmental stages in the life history; embryos and larvae often are less able to buffer environmental variation than are conspecific adults. In pond‐breeding amphibians, for example, cold water may constrain viability of eggs and larvae, even if adults can find suitable thermal conditions in terrestrial niches. Invasive species provide robust model systems for exploring these questions, because we can quantify thermal challenges at the expanding range edge (from field surveys) and larval responses to thermal conditions (in the laboratory). Our studies on invasive cane toads (Rhinella marina) at the southern (cool‐climate) edge of their expanding range in Australia show that available ponds often average around 20°C during the breeding period, 10°C lower than in many areas of the toads’ native range, or in the Australian tropics. Our laboratory experiments showed that cane toad eggs and larvae cannot develop successfully at 16°C, but hatching success and larval survival rates were higher at 20°C than in warmer conditions. Lower temperatures slowed growth rates, increasing the duration of tadpole life, but also increased metamorph body mass. Water temperature also influenced metamorph body shape (high temperatures reduced relative limb length, head width, and body mass) and locomotor performance (increased speed from intermediate temperatures, longer hops from high temperatures). In combination with previous studies, our data suggest that lower water temperatures may enhance rather than reduce recruitment of cane toads, at least in areas where pond temperatures reach or exceed 20°C. That condition is fulfilled over a wide area of southern Australia, suggesting that the continuing expansion of this invasive species is unlikely to be curtailed by the impacts of relatively low water temperatures on the viability of early life‐history stages.     

Skin resistance to water gain and loss has changed in cane toads (Rhinella marina) during their Australian invasion

The water‐permeable skin of amphibians renders them highly sensitive to climatic conditions, and interspecific correlations between environmental moisture levels and rates of water exchange across the skin suggest that natural selection adapts hydroregulatory mechanisms to local challenges. How quickly can such mechanisms shift when a species encounters novel moisture regimes? Cutaneous resistance to water loss and gain in wild‐caught cane toads (Rhinella marina) from Brazil, USA (Hawai''i) and Australia exhibited strong geographic variation. Cutaneous resistance was low in native‐range (Brazilian) toads and in Hawai''ian populations (where toads were introduced in 1932) but significantly higher in toads from eastern Australia (where toads were introduced in 1935). Toads from recently invaded areas in western Australia exhibited cutaneous resistance to water loss similar to the native‐range populations, possibly because toads are restricted to moist sites within this highly arid landscape. Rates of rehydration exhibited significant but less extreme geographic variation, being higher in the native range than in invaded regions. Thus, in less than a century, cane toads invading areas that impose different climatic challenges have diverged in the capacity for hydroregulation.     

Sex and age differences in habitat use by invasive cane toads (Rhinella marina) and a native anuran (Cyclorana australis) in the Australian wet–dry tropics

Although generalized habitat use may contribute to the success of invasive taxa, even species that are typically described as habitat generalists exhibit non‐random patterns of habitat use. We measured abiotic and biotic factors in 42 plots (each 100 × 10 m) along a 4.2‐km long unpaved road in tropical Australia, at a site that had been invaded by cane toads (Rhinella marina Bufonidae) seven years previously. We also counted anurans at night in each of these plots on 103 nights during the tropical wet season, over a five‐year period, beginning soon after the initial toad invasion. Spatial distributions differed significantly among adult male toads (n = 1047), adult female toads (n = 1222), juvenile toads (n = 342) and native frogs (Cyclorana australis Hylidae, n = 234). Adult male toads were closely associated with water bodies used as calling and/or spawning sites, whereas adult female toads and native frogs were most commonly encountered in drier forested areas on sloping ground. Juvenile toads used the margins of the floodplain more than conspecific adults did, but the floodplain itself was rarely used. Understanding which components of the habitat are most important to specific age and sex classes within a population, or how invasive species differ from native species in this respect, can clarify issues such as the spatial and temporal location of ecological impact by an invader, and the most effective places for control of the invader with minimal collateral effects on the native biota.     

Field trials of chemical suppression of embryonic cane toads (Rhinella marina) by older conspecifics

1. Laboratory experiments have shown that the viability of embryos of the invasive cane toad (Rhinella marina) can be reduced by exposure to chemical cues from older conspecific larvae. These effects (very strong in laboratory trials) may offer an exciting new approach to controlling this problematic invasive species in Australia. However, the degree to which the method works in natural environments has yet to be assessed.
2. Our experiments in the laboratory and in seminatural outdoor waterbodies show that chemical cues from tadpoles do indeed suppress the growth, development, and survival of conspecific larvae that are exposed as embryos and do so in a dose‐dependent manner; higher tadpole densities cause greater suppression of embryos.
3. In seminatural outdoor waterbodies, suppressor‐exposed tadpoles were less than half as likely to survive to metamorphosis as were controls, and were much smaller when they did so and hence, less likely to survive the metamorph stage. Additionally, female cane toads were less likely to oviposit in a waterbody containing free‐ranging (but not cage‐enclosed) tadpoles, suggesting that the presence of tadpoles (rather than the chemical cues they produce) may discourage oviposition.
4. Broadly, our results suggest that the suppression effect documented in laboratory studies does indeed occur in the field also, and hence that we may be able to translate that approach to develop new and more effective ways to reduce rates of recruitment of peri‐urban populations of cane toads in their invasive range.

     

Exploiting intraspecific competitive mechanisms to control invasive cane toads (Rhinella marina)

If invasive species use chemical weapons to suppress the viability of conspecifics, we may be able to exploit those species-specific chemical cues for selective control of the invader. Cane toads (Rhinella marina) are spreading through tropical Australia, with negative effects on native species. The tadpoles of cane toads eliminate intraspecific competitors by locating and consuming newly laid eggs. Our laboratory trials show that tadpoles find those eggs by searching for the powerful bufadienolide toxins (especially, bufogenins) that toads use to deter predators. Using those toxins as bait, funnel-traps placed in natural waterbodies achieved near-complete eradication of cane toad tadpoles with minimal collateral damage (because most native (non-target) species are repelled by the toads' toxins). More generally, communication systems that have evolved for intraspecific conflict provide novel opportunities for invasive-species control.     

Invader immunology: invasion history alters immune system function in cane toads (Rhinella marina) in tropical Australia

Because an individual's investment into the immune system may modify its dispersal rate, immune function may evolve rapidly in an invader. We collected cane toads (Rhinella marina) from sites spanning their 75‐year invasion history in Australia, bred them, and raised their progeny in standard conditions. Evolved shifts in immune function should manifest as differences in immune responses among the progeny of parents collected in different locations. Parental location did not affect the offspring's cell‐mediated immune response or stress response, but blood from the offspring of invasion‐front toads had more neutrophils, and was more effective at phagocytosis and killing bacteria. These latter measures of immune function are negatively correlated with rate of dispersal in free‐ranging toads. Our results suggest that the invasion of tropical Australia by cane toads has resulted in rapid genetically based compensatory shifts in the aspects of immune responses that are most compromised by the rigours of long‐distance dispersal.     

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.     

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.     

Stress and immunity at the invasion front: a comparison across cane toad (Rhinella marina) populations

At an invasion front, energetic and physiological trade‐offs may differ from those at the range‐core as a result of selection for enhanced dispersal, combined with a low density of conspecifics (which reduces pathogen transmission and competition for food). We measured traits related to energy stores and immunity in wild cane toads (Rhinella marina) across a 750‐km transect from their invasion front in tropical Australia, back into sites colonized 21 years earlier. Several traits were found to vary with population age; some linearly and others in a curvilinear manner. The relative size of spleens and fat bodies was highest in the oldest and newest populations, where rates of lungworm infection were lowest. Toads from older populations produced more corticosterone in response to a standardized stressor, and had higher lymphocyte counts (but lower basophil counts). The amount of skin swelling elicited by phytohaemagglutinin injection did not vary geographically, although recruitment of leukocytes to the injected tissue was higher in toads from long‐colonized areas. Because this was a field‐based study, we cannot differentiate the effects of population age, toad density or pathogen pressure on our measures of stress and immune responses, nor can we distinguish whether the causation involves hard‐wired adaptive processes or phenotypically plastic responses. Nonetheless, our data demonstrate substantial variation in immune systems among toads at varying distances from an invasion front, showing that a biological invasion imposes strong pressures on physiological systems of the invader.     

Spawning site selection by feral cane toads (Bufo marinus) at an invasion front in tropical Australia

Abstract Spawning sites are a critical and often scarce resource for aquatic‐breeding amphibians, including invasive species such as the cane toad (Bufo marinus). If toads select spawning sites based on habitat characteristics, we can potentially manipulate those characteristics to either enhance or reduce their suitability as breeding sites. We surveyed 25 spawning sites used by cane toads, and 25 adjacent unused sites, in an area of tropical Australia recently invaded by these feral anurans. Water chemistry (pH, conductivity, salinity, turbidity) was virtually identical between the two sets of waterbodies, but habitat characteristics were very different. Toads selectively oviposited in shallow pools with gradual rather than steep slopes, and with open (unvegetated) gradually sloping muddy banks. They avoided flowing water, and pools with steep surrounds. In these respects, cane toads broadly resemble previously studied toad species in other parts of the world, as well as conspecifics within their natural range in South America.     

The role of biotic and abiotic cues in stimulating aggregation by larval cane toads (Rhinella marina)

Tadpoles of the cane toad (Rhinella marina) form dense aggregations in the field, but the proximate cues eliciting this behavior are not well understood. We sampled water‐bodies in the Northern Territory of Australia, finding that the density of cane toad tadpoles increased with increasing temperature. Furthermore, we conducted laboratory experiments to explore the roles of biotic factors (attraction to conspecifics; chemical cues from an injured conspecific; food) and spatially heterogeneous abiotic factors (light levels, water depth, physical structure) to identify the cues that induce tadpole aggregation. Annulus and binary choice trials demonstrated weak but significant attraction between conspecifics. Tadpoles decreased swimming speeds, but did not increase grouping in response to cues from an injured conspecific. Larvae aggregated in response to abiotic cues (high levels of illumination and proximity to physical structures) and were strongly attracted to feeding conspecifics. Overall, aggregation by cane toad tadpoles is likely driven by weak social attraction coupled with a shared preference for specific abiotic features, creating loose aggregations that are then reinforced by movement toward feeding conspecifics.     

The accelerating invasion: dispersal rates of cane toads at an invasion front compared to an already-colonized location

Evolutionary theory predicts that individuals at an expanding range edge will disperse faster than conspecifics in long-colonized locations, but direct evidence is rare. Previous reports of high rates of dispersal of cane toads (Rhinella marina) at the invasion front have been based on studies at a single site in the Northern Territory. To replicate the earlier work, we radio-tracked free-ranging toads in the Kimberley region of northwestern Australia (at the westward-spreading invasion front) and 500 km northeast, on the Adelaide River floodplain of the Northern Territory (where toads had already been present for 6 years). For comparison, we also radio-tracked native frogs (Litoria caerulea and L. splendida) at the same sites. Consistent with the earlier reports, invasion-front cane toads travelled further per day, were more highly directional, and re-used refuge sites less frequently, than did conspecifics from an already-colonized site. In contrast, native frogs showed similar movement patterns in the two study areas. Our results confirm previous reports, and suggest that accelerated dispersal may be a common feature of individuals at the vanguard of a biological invasion.     

Behavioural responses of reptile predators to invasive cane toads in tropical Australia

The ecological impact of an invasive species can depend on the behavioural responses of native fauna to the invader. For example, the greatest risk posed by invasive cane toads (Rhinella marina Bufonidae) in tropical Australia is lethal poisoning of predators that attempt to eat a toad; and thus, a predator's response to a toad determines its vulnerability. We conducted standardized laboratory trials on recently captured (toad‐naïve) predatory snakes and lizards, in advance of the toad invasion front as it progressed through tropical Australia. Responses to a live edible‐sized toad differed strongly among squamate species. We recorded attacks (and hence, predator mortality) in scincid, agamid and varanid lizards, and in elapid, colubrid and pythonid snakes. Larger‐bodied predators were at greater risk, and some groups (elapid snakes and varanid lizards) were especially vulnerable. However, feeding responses differed among species within families and within genera. Some taxa (notably, many scincid and agamid lizards) do not attack toads; and many colubrid snakes either do not consume toads, or are physiologically resistant to the toad's toxins. Intraspecific variation in responses means that even in taxa that apparently are unaffected by toad invasion at the population level, some individual predators nonetheless may be fatally poisoned by invasive cane toads.     

Effects of an invasive species on refuge‐site selection by native fauna: The impact of cane toads on native frogs in the Australian tropics

Invasive species can induce shifts in habitat use by native taxa: either by modifying habitat availability, or by repelling or attracting native species to the vicinity of the invader. The ongoing invasion of cane toads (Rhinella marina) through tropical Australia might affect native frogs by affecting refuge‐site availability, because both frogs and toads frequently shelter by day in burrows. Our laboratory and field studies in the wet‐dry tropics show that native frogs of at least three species (Litoria tornieri, Litoria nasuta and Litoria dahlii) preferentially aggregate with conspecifics, and with (some) other species of native frogs. However, the frogs rarely aggregated with cane toads either in outdoor arenas or in standardized experimental burrows that we monitored in the field. The native frogs that we tested either avoided burrows containing cane toads (or cane toad scent) or else ignored the stimulus (i.e. treated such a burrow in the same way as they did an empty burrow). Native frogs selected a highly non‐random suite of burrows as diurnal retreat sites, whereas cane toads were less selective. Hence, even in the absence of toads, frogs do not use many of the burrows that are suitable for toads. The invasion of cane toads through tropical Australia is unlikely to have had a major impact on retreat‐site availability for native frogs.     

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.     

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.     

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.     

Athletic anurans: the impact of morphology,ecology and evolution on climbing ability in invasive cane toads

Although primarily terrestrial, cane toads (Rhinella marina) sometimes climb near‐vertical surfaces (tree‐trunks, cliffs, fences) during foraging or dispersal activities. We scored climbing ability (in laboratory trials) of 288 cane toads from four regions in Australia, plus two sites on the island of Hawai'i. We found strong divergence in climbing ability associated not only with sex and relative limb length, but also population of origin. Within each population, longer‐limbed individuals (and hence, males rather than females) were better climbers, although the geographical divergence in climbing ability remained significant even when sex and limb length were included in multivariate regression models. The geographical difference in climbing ability (but not morphology) disappeared when the progeny were raised in captivity under identical conditions, without climbing opportunities. Although influenced by morphology, climbing ability in wild‐caught cane toads appears to be driven primarily by local environmental conditions that facilitate and/or reward arboreal activity.