Effects of invasion history on physiological responses to immune system activation in invasive Australian cane toads.
ABSTRACT: The cane toad (Rhinella marina) has undergone rapid evolution during its invasion of tropical Australia. Toads from invasion front populations (in Western Australia) have been reported to exhibit a stronger baseline phagocytic immune response than do conspecifics from range core populations (in Queensland). To explore this difference, we injected wild-caught toads from both areas with the experimental antigen lipopolysaccharide (LPS, to mimic bacterial infection) and measured whole-blood phagocytosis. Because the hypothalamic-pituitary-adrenal axis is stimulated by infection (and may influence immune responses), we measured glucocorticoid response through urinary corticosterone levels. Relative to injection of a control (phosphate-buffered saline), LPS injection increased both phagocytosis and the proportion of neutrophils in the blood. However, responses were similar in toads from both populations. This null result may reflect the ubiquity of bacterial risks across the toad's invaded range; utilization of this immune pathway may not have altered during the process of invasion. LPS injection also induced a reduction in urinary corticosterone levels, perhaps as a result of chronic stress.
Project description:Invasive species provide a robust opportunity to evaluate how animals deal with novel environmental challenges. Shifts in locomotor performance-and thus the ability to disperse-(and especially, the degree to which it is constrained by thermal and hydric extremes) are of special importance, because they might affect the rate that an invader can spread. We studied cane toads (Rhinella marina) across a broad geographical range: two populations within the species' native range in Brazil, two invasive populations on the island of Hawai'i and eight invasive populations encompassing the eastern, western and southern limits of the toad invasion in Australia. A toad's locomotor performance on a circular raceway was strongly affected by both its temperature and its hydration state, but the nature and magnitude of those constraints differed across populations. In their native range, cane toads exhibited relatively low performance (even under optimal test conditions) and a rapid decrease in performance at lower temperatures and hydration levels. At the other extreme, performance was high in toads from southern Australia, and virtually unaffected by desiccation. Hawai'ian toads broadly resembled their Brazilian conspecifics, plausibly reflecting similar climatic conditions. The invasion of Australia has been accompanied by a dramatic enhancement in the toads' locomotor abilities, and (in some populations) by an ability to maintain locomotor performance even when the animal is cold and/or dehydrated. The geographical divergences in performance among cane toad populations graphically attest to the adaptability of invasive species in the face of novel abiotic challenges.
Project description:As is common in biological invasions, the rate at which cane toads (<i>Rhinella marina</i>) have spread across tropical Australia has accelerated through time. Individuals at the invasion front travel further than range-core conspecifics and exhibit distinctive morphologies that may facilitate rapid dispersal. However, the links between these morphological changes and locomotor performance have not been clearly documented. We used raceway trials and high-speed videography to document locomotor traits (e.g. hop distances, heights, velocities, and angles of take-off and landing) of toads from range-core and invasion-front populations. Locomotor performance varied geographically, and this variation in performance was linked to morphological features that have evolved during the toads' Australian invasion. Geographical variation in morphology and locomotor ability was evident not only in wild-caught animals, but also in individuals that had been raised under standardized conditions in captivity. Our data thus support the hypothesis that the cane toad's invasion across Australia has generated rapid evolutionary shifts in dispersal-relevant performance traits, and that these differences in performance are linked to concurrent shifts in morphological traits.
Project description:Dispersal biology at an invasion front differs from that of populations within the range core, because novel evolutionary and ecological processes come into play in the nonequilibrium conditions at expanding range edges. In a world where species' range limits are changing rapidly, we need to understand how individuals disperse at an invasion front. We analyzed an extensive dataset from radio-tracking invasive cane toads (Rhinella marina) over the first 8 y since they arrived at a site in tropical Australia. Movement patterns of toads in the invasion vanguard differed from those of individuals in the same area postcolonization. Our model discriminated encamped versus dispersive phases within each toad's movements and demonstrated that pioneer toads spent longer periods in dispersive mode and displayed longer, more directed movements while they were in dispersive mode. These analyses predict that overall displacement per year is more than twice as far for toads at the invasion front compared with those tracked a few years later at the same site. Studies on established populations (or even those a few years postestablishment) thus may massively underestimate dispersal rates at the leading edge of an expanding population. This, in turn, will cause us to underpredict the rates at which invasive organisms move into new territory and at which native taxa can expand into newly available habitat under climate change.
Project description: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.
Project description:Individuals at the leading edge of expanding biological invasions often show distinctive phenotypic traits, in ways that enhance their ability to disperse rapidly and to function effectively in novel environments. Cane toads (Rhinella marina) at the invasion front in Australia exhibit shifts in morphology, physiology and behaviour (directionality of dispersal, boldness, risk-taking). We took a common-garden approach, raising toads from range-core and range-edge populations in captivity, to see if the behavioural divergences observed in wild-caught toads are also evident in common-garden offspring. Captive-raised toads from the invasion vanguard population were more exploratory and bolder (more prone to 'risky' behaviours) than toads from the range core, which suggests that these are evolved, genetic traits. Our study highlights the importance of behaviour as being potentially adaptive in invasive populations and adds these behavioural traits to the increasing list of phenotypic traits that have evolved rapidly during the toads' 80-year spread through tropical Australia.
Project description:Biological invasions can stimulate rapid shifts in organismal performance, via both plasticity and adaptation. We can distinguish between these two proximate mechanisms by rearing offspring from populations under identical conditions and measuring their locomotor abilities in standardized trials. We collected adult cane toads (Rhinella marina) from invasive populations that inhabit regions of Australia with different climatic conditions. We bred those toads and raised their offspring under common-garden conditions before testing their locomotor performance. At high (but not low) temperatures, offspring of individuals from a hotter location (northwestern Australia) outperformed offspring of conspecifics from a cooler location (northeastern Australia). This disparity indicates that, within less than 100 years, thermal performance in cane toads has adapted to the novel abiotic challenges that cane toads have encountered during their invasion of tropical Australia.
Project description:The Major Histocompatibility Complex (MHC) class I is a highly variable gene family that encodes cell-surface receptors vital for recognition of intracellular pathogens and initiation of immune responses. The MHC class I has yet to be characterised in bufonid toads (Order: Anura; Suborder: Neobatrachia; Family: Bufonidae), a large and diverse family of anurans. Here we describe the characterisation of a classical MHC class I gene in the Australian cane toad, Rhinella marina. From 25 individuals sampled from the Australian population, we found only 3 alleles at this classical class I locus. We also found large number of class I alpha 1 alleles, implying an expansion of class I loci in this species. The low classical class I genetic diversity is likely the result of repeated bottleneck events, which arose as a result of the cane toad's complex history of introductions as a biocontrol agent and its subsequent invasion across Australia.
Project description:Invasive species are an important issue worldwide but predicting invasiveness, and the underlying mechanisms that cause it, is difficult. There are several primary hypotheses to explain invasion success. Two main hypothesis based on niche spaces stand out as alternative, although not exclusive. The empty niche hypothesis states that invaders occupy a vacant niche space in the recipient community, and the niche competition hypothesis states that invaders overlap with native species in niche space. Studies on trait similarity/dissimilarity between the invader and native species can provide information on their niche overlap. Here, we use the highly invasive and well-studied cane toad (Rhinella marina) to test these two hypotheses in Australia, and assess its degree of overlap with native species in several niche dimensions. We compare extensive morphological and environmental data of this successful invader to 235 species (97%) of native Australian frogs. Our study is the first to document the significant morphological differences between the invasive cane toad and a continent-wide frog radiation: despite significant environmental overlap, cane toads were distinct in body size and shape from most Australian frog species, suggesting that in addition to their previously documented phenotypic plasticity and wide environmental and trophic niche breadth, their unique shape also may have contributed to their success as an invasive species in Australia. Thus, the invasive success of cane toads in Australia may be explained through them successfully colonizing an empty niche among Australian anurans. Our results support that the cane toad's distinct morphology may have played a unique role in the invasiveness of this species in Australia, which coupled with a broad environmental niche breadth, would have boosted their ability to expand their distribution across Australia. We also propose RLLR (Relative limb length ratio) as a potentially useful measure of identifying morphological niche uniqueness and a potential measure of invasiveness potential in anuran amphibians.
Project description:Biological invasions can induce rapid evolutionary change. As cane toads (Rhinella marina) have spread across tropical Australia over an 80-year period, their rate of invasion has increased from around 15 to 60 km per annum. Toads at the invasion front disperse much faster and further than conspecifics from range-core areas, and their offspring inherit that rapid dispersal rate. We investigated morphological changes that have accompanied this dramatic acceleration, by conducting three-dimensional morphometric analyses of toads from both range-core and invasion-front populations. Morphology of heads, limbs, pectoral girdles and pelvic girdles differed significantly between toads from the two areas, ranging from 0.5% to 16.5% difference in mean bone dimensions between populations, with invasion-front toads exhibiting wider forelimbs, narrower hindlimbs and more compact skulls. Those changes plausibly reflect an increased reliance on bounding (multiple short hops in quick succession) rather than separate large leaps. Within an 80-year period, invasive cane toads have converted the basic anuran body plan - which evolved for occasional large leaps to evade predators - into a morphotype better-suited to sustained long-distance travel.
Project description:As a population expands into novel areas (as occurs in biological invasions), the range edge becomes dominated by rapidly dispersing individuals-thereby accelerating the rate of population spread. That acceleration has been attributed to evolutionary processes (natural selection and spatial sorting), to which we add a third complementary process: behavioural plasticity. Encountering environmental novelty may directly elicit an increased rate of dispersal. When we reciprocally translocated cane toads (Rhinella marina) among study sites in southern Australia, the transported animals massively increased dispersal rates relative to residents (to an extent similar to the evolved increase between range-core versus invasion-front toad populations in Australia). The responses of these translocated toads show that even range-core toads are capable of the long-distance dispersal rates of invasion-front conspecifics and suggest that rapid dispersal (rather than evolving de novo) has simply been expanded from facultative to constitutive expression.