Search

Spatial sorting on invasion fronts drives the evolution of dispersive phenotypes, and in doing so can push phenotypes in the opposite direction to natural selection. The invasion of cane toads (Rhinella marina) through tropical Australia has accelerated over recent decades because of the accumulation of dispersal-enhancing traits at the invasion front, driven by spatial sorting. One such trait is the length of the forelimbs: invasion-front toads have longer arms (relative to body length) in comparison with populations 10-20 years after invasion. Such a shift likely has fitness consequences: an increase of forearm length would decrease the strength with which a male could cling to a female during amplexus and so render such a male less competitive in competition for mates, compared to short-armed conspecifics. Our laboratory trials of attachment strength confirmed that males with relatively longer arms were easier to displace, and competition trials show higher duration of amplexus for males with shorter arms. Together with the sharp cline in limb length observed behind the invasion front, these results imply an opposition of selective forces: spatial sorting optimizes dispersal, but as this force wanes behind the invasion front, we see the primacy of natural selection reassert itself.

In many species of anurans, males produce advertisement calls that function to attract reproductively active females. Rival males may use the public information in these calls to optimize their own tactics for acquiring mates. To see whether male cane toads, Rhinella marina, modify their mate-searching and amplexus behaviours in response to conspecific calls, we monitored toads in outdoor enclosures while playing recordings of advertisement calls, a biologically irrelevant stimulus with similar acoustic properties or silence. Male toads were seven times more likely to engage in amplexus and moved twice as much during a toad chorus than during the control sound or silence. Nonacoustic cues also influenced propensity to initiate amplexus, with males five to 16 times more likely to amplect a moving target than a stationary one (regardless of the sex of the animal being amplexed). Our study shows that male toads dramatically alter their behaviour in response to acoustic and visual information from conspecifics, suggesting that this public information holds substantial value to them as they seek to fine-tune their own reproductive tactics.

Increased dispersal propensity often evolves on expanding range edges due to the Olympic Village effect, which involves the fastest and fittest finding themselves together in the same place at the same time, mating, and giving rise to like individuals. But what happens after the range's leading edge has passed and the games are over? Although empirical studies indicate that dispersal propensity attenuates following range expansion, hypotheses about the mechanisms driving this attenuation have not been clearly articulated or tested. Here, we used a simple model of the spatiotemporal dynamics of two phenotypes, one fast and the other slow, to propose that dispersal attenuation beyond preexpansion levels is only possible in the presence of trade‐offs between dispersal and life‐history traits. The Olympic Village effect ensures that fast dispersers preempt locations far from the range's previous limits. When trade‐offs are absent, this preemptive spatial advantage has a lasting impact, with highly dispersive individuals attaining equilibrium frequencies that are strictly higher than their introduction frequencies. When trade‐offs are present, dispersal propensity decays rapidly at all locations. Our model's results about the postcolonization trajectory of dispersal evolution are clear and, in principle, should be observable in field studies. We conclude that empirical observations of postcolonization dispersal attenuation offer a novel way to detect the existence of otherwise elusive trade‐offs between dispersal and life‐history traits.

© 2017 by The University of Chicago Press. All rights reserved. Our best hope of developing innovative methods to combat invasive species is likely to come from the study of high-profile invaders that have attracted intensive research not only into control, but also basic biology. Here we illustrate that point by reviewing current thinking about novel ways to control one of the world’s most well-studied invasions: that of the cane toad in Australia. Recently developed methods for population suppression include more effective traps based on the toad’s acoustic and pheromonal biology. New tools for containing spread include surveillance technologies (e.g., eDNA sampling and automated call detectors), as well as landscape-level barriers that exploit the toad’s vulnerability to desiccation— a strategy that could be significantly enhanced through the introduction of sedentary, rangecore genotypes ahead of the invasion front. New methods to reduce the ecological impacts of toads include conditioned taste aversion in free-ranging predators, gene banking, and targeted gene flow. Lastly, recent advances in gene editing and gene drive technology hold the promise of modifying toad phenotypes in ways that may facilitate control or buffer impact. Synergies between these approaches hold great promise for novel and more effective means to combat the toad invasion and its consequent impacts on biodiversity.

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.

The rapid evolution of increased dispersal rate during a population's range expansion provides a unique opportunity to detect trade-offs between dispersal and reproduction. If a high reproductive rate slows down an individual's dispersal, vanguard individuals should exhibit a lower reproductive output than conspecifics from long-colonized areas. In the present study, we demonstrate a reduction in reproductive rate in highly dispersive invasion-front populations of cane toads in tropical Australia.

Summary1. The ability to disperse along a consistent compass heading strongly affects the rate andefficiency of an animal’s displacement, and thus is under selection at the expanding edge of abiological invasion.2. We used radiotelemetry to assess whether the dispersal direction of cane toads (Rhinellamarina) changed as a function of time since invasion, by comparing (i) toads at a single sitemonitored annually for 10 years subsequent to toad arrival; (ii) toads collected from sitesacross the species’ invaded range in Australia, and radiotracked at a common site; and (iii) theoffspring of those transported toads that were reared in captivity under common-garden condi-tions.3. The first of these data sets showed non-random directionality, indicating strong spatialsorting operating on this trait: toads moved in a north-westerly direction for the first 6 yearspost-invasion, but in random directions thereafter. Despite the evidence for trait sorting, noconsistent directionality was seen in toads relocated from populations with different invasionhistories nor in their offspring. Why do we see no evolutionary shifts?4. Dispersal directionality of the offspring was not correlated with that of their parents, argu-ing against a genetic basis to this behavioural trait. Thus, while an expanding invasion frontcreates an evolutionary pressure for animals to move in a specific direction, evolution of thistrait has not occurred in this system because directionality is not heritable.5. The observed north-westerly movements of toads at the invasion front were due to simpledensity differentials: in the first few years, most toads arriving at our study site originated fromearlier-colonized (and hence denser) populations to the south-east.Key-words: Bufo marinus, dispersal, invasive species, orientation, range expansion, spatialsortingIntroduction

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.

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-naive) preda- tory 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.

The ability of a native predator to adjust to a dangerously toxic invasive species is key to avoiding an ongoing suppression of the predator's population and the trophic cascade of effects that can result. Many species of anurophagous predators have suffered population declines due to the cane toad's (Rhinella marina: Bufonidae) invasion of Australia; these predators can be fatally poisoned from attempting to consume the toxic toad. We studied one such toad-vulnerable predator, the yellow-spotted monitor (Varanus panoptes: Varanidae), testing whether changes to the predator's feeding behaviour could explain how the species persists following toad invasion. Wild, free-roaming lizards from (1) toad-naive and (2) toad-exposed populations were offered non-toxic native frogs and slightly toxic cane toads (with parotoid glands removed) in standardized feeding trials. Toad-naive lizards readily consumed both frogs and toads, with some lizards displaying overt signs of illness after consuming toads. In contrast, lizards from toad-exposed populations consumed frogs but avoided toads. Repeated encounters with toads did not modify feeding responses by lizards from the toad-naive populations, suggesting that aversion learning is limited (but may nonetheless occur). Our results suggest that this vulnerable predator can adjust to toad invasion by developing an aversion to feeding on the toxic invader, but it remains unclear as to whether the lizard's toad-aversion arises via adaptation or learning.

Spatial heterogeneity in environmental conditions may restrict the spread of invasive species to narrow corridors between extensive patches of suitable habitat; thus, we may be able to curtail invasions by identifying such corridors, and focusing control efforts in these areas. Invasive cane toads Rhinella marina have spread rapidly through northern Australia, but to invade further into Western Australia, the toads must traverse a narrow arid corridor where artificial waterbodies may serve as critical stepping stones for range expansion. We focus on the cane toads' imminent expansion into north-western Australia and use stochastic simulation to identify areas in which removal of artificial waterbodies would be most effective at stopping their spread. Our model predicts that toads will spread from the Kimberley to the Pilbara regions of Western Australia through a narrow coastal corridor, but that they will depend upon artificial waterbodies to do so. Importantly, excluding toads from artificial waterbodies is predicted to prevent toads from colonizing c. 268200km2 of their potential range in Western Australia. We identified three locations where closure of a relatively small subset of artificial waterbodies is predicted to halt the spread of toads. Synthesis and applications. We present a modelling framework that can be used to focus management activities within invasion corridors. Our analyses suggest that strategic removal of potential invasion hubs along such corridors can halt the spread of an invasive species.

Effects of perturbations to wildlife often are measured by changes in rates of encounter with animals during standardised surveys, such as along roads. Previous work has predicted that the invasion of toxic cane toads (Rhinella marina) through the Australian tropics will cause massive mortality of anuran-eating snakes, and influence abundances of other native species. We surveyed three adjacent road transects for nocturnal snakes and lizards, beginning shortly before toads arrived at this site near Darwin, in the Northern Territory. In the wet-seasons of four successive years, we conducted surveys on 591 nights; on 302 of these nights, all three transects were surveyed. We recorded 8,880 live cane toads and 3,365 live reptiles. Toad numbers increased over time on all three transects but encounters with 13 species of native reptiles varied inconsistently. Eight of the 13 species of native reptile showed no significant change in encounter rates following the arrival of toads. Of the five species that did change in encounter rates, only one taxon (the bluetongue skink, Tiliqua scincoides intermedia) declined across all three transects. Encounter rates of the other four species often increased on at least one transect but decreased on at least one other. Thus, either the impact of cane toads on counts of reptiles differed between nearby sites, or (more likely) other factors had more influence on reptile numbers. A consistent decrease in reptile numbers on the busiest road over the study period suggests that local snake populations were affected more by road-kill than by invasive toads. Without spatial replication, this decrease could have been interpreted as an impact of toad invasion.

In an invasive species, selection for increased rates of dispersal at the expanding range front may favor the evolution of reduced investment into any trait that does not contribute to more rapid dispersal. Thus, populations at the invasion front may exhibit reduced investment into the immune system. To test this prediction, cane toads (Rhinella marina) from parents collected from populations across the toads' invasion history in tropical Australia were raised in a standard environment. When their immune systems were challenged by injection of bacterial lipopolysaccharide, the toads' metabolic rates rose by up to 40%. The magnitude of elevation in metabolic rate was lower in toads derived from the invasion front than in those from long-established populations. Our results support the hypothesis that an animal's investment in immune defenses can be modified by selective forces that arise in the course of a biological invasion.

In classical evolutionary theory, traits evolve because they facilitate organismal survival and/or reproduction. We discuss a different type of evolutionary mechanism that relies upon differential dispersal. Traits that enhance rates of dispersal inevitably accumulate at expanding range edges, and assortative mating between fast-dispersing individuals at the invasion front results in an evolutionary increase in dispersal rates in successive generations. This cumulative process (which we dub “spatial sorting”) generates novel phenotypes that are adept at rapid dispersal, irrespective of how the underlying genes affect an organism's survival or its reproductive success. Although the concept is not original with us, its revolutionary implications for evolutionary theory have been overlooked. A range of biological phenomena (e.g., acceleration of invasion fronts, insular flightlessness, preadaptation) may have evolved via spatial sorting as well as (or rather than) by natural selection, and this evolutionary mechanism warrants further study.

Because of their small size and fragility, larvae of many amphibian species are difficult to mark unambiguously for experimental studies. This constraint limits our ability to run experiments in which individual interactions matter and so limits our ability to study how social behaviors affect individual fitness. We anesthetized small ( 30 days and had only minimal effects on tadpole growth, survival, and swimming performance. Marking the membrane of a tadpole tail fin provides a cost-effective method for cohort marking with minimal equipment and training. It also provides the opportunity to gather extra data on an individual (such as DNA) with minimal further stress to the animal.

Loss of dispersal typifies island biotas, but the selective processes driving this phenomenon remain contentious. This is because selection via, both indirect (e.g. relaxed selection or island syndromes) and direct (e.g. natural selection or spatial sorting) processes may be involved, and no study has yet convincingly distinguished between these alternatives. Here, we combined observational and experimental analyses of an island lizard, the Komodo dragon (Varanus komodoensis, the world's largest lizard), to provide evidence for the actions of multiple processes that could contribute to island dispersal loss. In the Komodo dragon, concordant results from telemetry, simulations, experimental translocations, mark-recapture, and gene flow studies indicated that despite impressive physical and sensory capabilities for long-distance movement, Komodo dragons exhibited near complete dispersal restriction: individuals rarely moved beyond the valleys they were born/captured in. Importantly, lizard site-fidelity was insensitive to common agents of dispersal evolution (i.e. indices of risk for inbreeding, kin and intraspecific competition, and low habitat quality) that consequently reduced survival of resident individuals. We suggest that direct selection restricts movement capacity (e.g. via benefits of spatial philopatry and increased costs of dispersal) alongside use of dispersal-compensating traits (e.g. intraspecific niche partitioning) to constrain dispersal in island species.

Most evolutionary theory does not deal with populations expanding or contracting in space. Invasive species, climate change, epidemics, and the breakdown of dispersal barriers, however, all create populations in this kind of spatial disequilibrium. Importantly, spatial disequilibrium can have important ecological and evolutionary outcomes. During continuous range expansion, for example, populations on the expanding front experience novel evolutionary pressures because frontal populations are assorted by dispersal ability and have a lower density of conspecifics than do core populations. These conditions favor the evolution of traits that increase rates of dispersal and reproduction. Additionally, lowered density on the expanding front eventually frees populations on the expanding edge from specialist, coevolved enemies, permitting higher investment into traits associated with dispersal and reproduction rather than defense against pathogens. As a result, the process of range expansion drives rapid life-history evolution, and this seems to occur despite ongoing serial founder events that have complex effects on genetic diversity at the expanding front. Traits evolving on the expanding edge are smeared across the landscape as the front moves through, leaving an ephemeral signature of range expansion in the life-history traits of a species across its newly colonized range. Recent studies suggest that such nonequilibrium processes during recent population history may have contributed to many patterns usually ascribed to evolutionary forces acting in populations at spatial equilibrium.

As well as their direct ecological impacts on native taxa, invasive species can impose selection on phenotypic attributes (morphology, physiology, behaviour, etc.) of the native fauna. In anurans, body size at metamorphosis is a critical life-history trait: for most challenges faced by post-metamorphic anurans, larger size at metamorphosis probably enhances survival. However, our studies on Australian frogs (Limnodynastes convexiusculus) show that this pattern can be reversed by the arrival of an invasive species. When metamorph frogs first encounter invasive cane toads (Bufo marinus), they try to eat the toxic invader and, if they are able to do so, are likely to die from poisoning. Because frogs are gape-limited predators, small metamorphs cannot ingest a toad and thus survive long enough to disperse away from the natal pond (and thus from potentially deadly toads). These data show that larger size at metamorphosis can reduce rather than increase anuran survival rates, because larger metamorphs are more easily able to ingest (and thus be poisoned by) metamorph cane toads. Our results suggest that patterns of selection on life-history traits of native taxa (such as size and age at metamorphosis, seasonal timing of breeding and duration of pondside aggregation prior to dispersal) can be modified by the arrival of an invasive species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 329‐336.

Biological invasions provide opportunities to study novel behavioral interactions between predators and their prey. To withstand detrimental effects from a potentially lethal invader, a native taxon must somehow adjust to the invader’s presence. Cane toads (Bufo marinus) are highly toxic to native Australian anurans and constitute a major threat if consumed. We recorded the responses of Australian marbled frogs (Limnodynastes convexiusculus) during their first encounters with edible-sized cane toads. The frogs exhibited rapid avoidance learning: toad-exposed frogs were less likely to attack subsequently encountered cane toads (and hence more likely to survive). Among-clutch variance in learning rates and in physiological tolerance to toad toxins was low, suggesting that genetically based adaptive changes to frog feeding responses will be slow (especially given that rapid learning reduces mortality and thus reduces the fitness decrement of initial willingness to attack a toad). Hence, rapid taste aversion learning is the primary mechanism enabling marbled frogs to persist in the presence of a potentially fatal invader. In combination with previous work, our study shows that some native predators adjust to the threat posed by cane toad invasion via taste aversion learning, whereas others show genetically based modification of feeding responses. More generally, both learning and adaptation enable vulnerable native taxa to survive the arrival of a toxic invasive species. Key words: behavior, Bufo marinus, frog, invasive species, learning, predator. [Behav Ecol]

Cane toads (Bufo marinus) are now moving about 5 times faster through tropical Australia than they did a half-century ago, during the early phases of toad invasion. Radio-tracking has revealed higher daily rates of displacement by toads at the invasion front compared to those from long-colonised areas: toads from frontal populations follow straighter paths, move more often, and move further per displacement than do toads from older (long-established) populations. Are these higher movement rates of invasion-front toads associated with modified locomotor performance (e.g. speed, endurance)? In an outdoor raceway, toads collected from the invasion front had similar speeds, but threefold greater endurance, compared to conspecifics collected from a long-established population. Thus, increased daily displacement in invasion-front toads does not appear to be driven by changes in locomotor speed. Instead, increased dispersal is associated with higher endurance, suggesting that invasion-front toads tend to spend more time moving than do their less dispersive conspecifics. Whether this increased endurance is a cause or consequence of behavioural shifts associated with rapid dispersal is unclear. Nonetheless, shifts in endurance between frontal and core populations of this invasive species point to the complex panoply of traits affected by selection for increased dispersal ability on expanding population fronts.

Costs of plant defences to herbivores have been extensively studied, but costs of chemical defences to carnivores are less well understood.We examine the costs to Australian keelback snakes (Tropidonophis mairii, Gray 1841) of consuming cane toads (Bufo (Rhinella) marinus Linnaeus 1758). Cane toads (an invasive species in Australia) are highly toxic. Although keelbacks can consume toads without dying (unlike most Australian snakes), we show that cane toads are poor quality prey for keelbacks. Toads are of low net nutritional value, take longer to consume than do native frogs and reduce the snake's locomotor performance for up to 6 h after ingestion of a meal. These latter effects may increase a snake's vulnerability to predation. Nutritional content of vertebrate prey is not the only factor driving the evolution of foraging behaviour; other more subtle costs, such as risk of predation, may be widespread.

Immediately after their transition from aquatic to terrestrial life, juveniles of many anuran species are restricted to the margins of natal ponds. Understanding the factors determining the duration of that pondside aggregation has direct management ramifications in the case of the invasive cane toad (Bufo marinus) in tropical Australia. Previous work suggests that dispersal confers biotic advantages (reduced risk of cannibalism, enhanced feeding opportunities) to juvenile toads, but desiccation risk constrains these small animals to the moist margins of the pond. If so, juvenile dispersal should be sensitive to fluctuating hydric conditions on a diel and seasonal cycle. We tested this prediction with field observations (monitoring of dispersal to and from the pond) and field experiments (manipulating hydric regimes). Our results support a dynamic model of juvenile distribution, with a primary role for temporal variations in desiccation risk as the primary factor driving dispersal. During the dry season, strong diel cycles in desiccation risk generate a ‘tidal’ flow of juveniles, dispersing out in the moist morning but retreating to the pond margins at midday. Dispersal rates were enhanced by artificial watering during the dry season, and by the onset of the wet season.

Interactions between invasive species and native fauna afford a unique opportunity to examine inter- specific encounters as they first occur, without the complications introduced by coevolution. In northern Aus- tralia, 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 naive 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 subse- quently 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.

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.

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.

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.

Background Individual movement is critical to organismal fitness and also influences broader population processes such as demographic stochasticity and gene flow. Climatic change and habitat fragmentation render the drivers of individual movement especially critical to understand. Rates of movement of free-ranging animals through the landscape are influenced both by intrinsic attributes of an organism (e.g., size, body condition, age), and by external forces (e.g., weather, predation risk). Statistical modelling can clarify the relative importance of those processes, because externally-imposed pressures should generate synchronous displacements among individuals within a population, whereas intrinsic factors should generate consistency through time within each individual. External and intrinsic factors may vary in importance at different time scales. Results In this study we focused on daily displacement of an ambush-foraging snake from tropical Australia (the Northern Death Adder Acanthophis praelongus), based on a radiotelemetric study. We used a mixture of spectral representation and Bayesian inference to study synchrony in snake displacement by phase shift analysis. We further studied autocorrelation in fluctuations of displacement distances as “one over f noise”. Displacement distances were positively autocorrelated with all considered noise colour parameters estimated as >0. We show how the methodology can reveal time scales of particular interest for synchrony and found that for the analysed data, synchrony was only present at time scales above approximately three weeks. Conclusion We conclude that the spectral representation combined with Bayesian inference is a promising approach for analysis of movement data. Applying the framework to telemetry data of A. praelongus, we were able to identify a cut-off time scale above which we found support for synchrony, thus revealing a time scale where global external drivers have a larger impact on the movement behaviour. Our results suggest that for the considered study period, movement at shorter time scales was primarily driven by factors at the individual level; daily fluctuations in weather conditions had little effect on snake movement. Electronic supplementary material The online version of this article (doi:10.1186/s40462-015-0038-5) contains supplementary material, which is available to authorized users.

Determining the factors that influence the rate of spread of invasive species is an important goal for conservation biology. If invasive species utilize specific landscape features as dispersal corridors, control programs can target such corridors. Radio-telemetry was used to determine landscape level factors that influence dispersal of an introduced anuran species (the cane toad) at an invasion front in tropical Australia. Most radio-tracked toads moved along roads and cleared fencelines, avoiding heavily vegetated habitat; they typically sheltered overnight close to these open corridors, returning to the road each evening to recommence dispersal. Surveys of the compass orientation of dispersing toads on roads showed that most animals were oriented along the main axis of the road (and thus, travelling along the road) rather than moving across it. To test the hypothesis that use of roads enables toads to disperse more rapidly than would be possible across more thickly vegetated sites, locomotor performance of toads was quantified under field conditions. As predicted, toads rapidly slowed down in dense roadside vegetation but continued to move rapidly through open areas. These results suggest that simple habitat manipulations of roadside verges might help to reduce the rate of dispersal of cane toads across tropical Australia. © 2006 Elsevier Ltd. All rights reserved.

Successful invasive species often exhibit high phenotypic lability. Even when intuition suggests that their genetic diversity has been reduced by strong founder effects, many successful invasive species still exhibit adaptive change in response to their new environment. To understand the probable long-term ecological impacts of a particular invader, we need to quantify long-term changes in the invader's phenotype, as these changes may well influence the level of impact the invader has on native species. Here we examine morphological change, as a consequence of time since colonisation and other spatial factors, in the cane toad (Bufo marinus). Cane toads are highly toxic and have killed many Australian native predators since they were introduced in 1935. The amount of toxin to which a predator is exposed will depend upon (1) the body size of the toad and (2) the relative toxicity of the toad (here measured by the relative size of the toad's parotoid glands). Using multiple regression and a model-selection approach, we show that both toad size and relative toxicity have decreased with time since colonisation. Thus toads (like many other successful invasives) exhibit phenotypic lability. Importantly, this result strongly suggests that toads will exert their maximal impact on native predators when they first arrive in an area; the level of impact will then decline over time.

Reproductive isolation between sympatric taxa can be maintained by specific mate-recognition behaviours or by ecological divergence that reduces interspecific contact during reproduction. Common garter snakes, Thamnophis sirtalis (L., 1758), and plains garter snakes, Thamnophis radix (Baird and Girard, 1853), are sympatric over large areas, but morphological data suggest that the prezygotic isolation between these two species partially breaks down in a severely cold part of their joint range in Manitoba. Courtship trials show that male T. radix court intensely over a narrower range of (higher) ambient temperatures than do male T. sirtalis. Males selectively court females of their own species, but male T. radix are less choosy than male T. sirtalis. Hexane extracts of female skin lipids also elicited species-specific courtship. Although this male preference for species-specific pheromones contributes to species isolation, it is not strong enough to completely separate the two taxa. The absence of hybridization over most of the sympatric range may depend on the timing of mating (early spring, near the hibernation den). Differences between the species in hibernation-site selection and the timing of spring emergence break down in central Manitoba because severely cold winter temperatures force both species together into the few available hibernation (and thus, mating) sites, and the short warm season reduces temporal separation in emergence (and thus, mating) seasons.

Camera trapping has evolved into an efficient technique for gathering presence/absence data for many species; however, smaller mammals such as rodents are often difficult to identify in images. Identification is inhibited by co-occurrence with similar-sized small mammal species and by camera set-ups that do not provide adequate image quality. Here we describe survey procedures for identification of two small, threatened rodent species – smoky mouse (Pseudomys fumeus) and New Holland mouse (P. novaehollandiae) – using white-flash and infrared camera traps. We tested whether observers could accurately identify each species and whether experience with small mammals influenced accuracy. Pseudomys fumeus was ~20 times less likely to be misidentified on white-flash images than infrared, and observer experience affected accuracy only for infrared images, where it accounted for all observer variance. Misidentifications of P. novaehollandiae were more common across both flash types: false positives (>0.21) were more common than false negatives (

Increased dispersal propensity often evolves on expanding range edges due to the Olympic Village effect, which involves the fastest and fittest finding themselves together in the same place at the same time, mating, and giving rise to like individuals. But what happens after the range’s leading edge has passed and the games are over? Although empirical studies indicate that dispersal propensity attenuates following range expansion, hypotheses about the mechanisms driving this attenuation have not been clearly articulated or tested. Here we use a simple model of the spatiotemporal dynamics of two phenotypes, one fast and the other slow, to propose that dispersal attenuation beyond pre-expansion levels is only possible in the presence of trade-offs between dispersal and life-history traits. The Olympic Village effect ensures that fast dispersers pre-empt locations far from the range’s previous limits. When trade-offs are absent, this pre-emptive spatial advantage has a lasting impact, with highly dispersive individuals attaining equilibrium frequencies that are strictly higher than their introduction frequencies. When trade-offs are present, dispersal propensity decays rapidly at all locations. Our model’s results about the post-colonization trajectory of dispersal evolution are clear and, in principle, should be observable in field studies. We conclude that empirical observations of post-colonization dispersal attenuation offer a novel way to detect the existence of otherwise elusive trade-offs between dispersal and life-history traits.

Summary The history of biological invasions, and of attempts to combat them, is dominated by stories of futility. Especially in the case of invasive species that have a high public profile, like the cane toad ( Rhinella marina ) in Australia, the voices of scientists often have been drowned out in the roar of populist political debate. There have been many failures by science as well, beginning with the initial importation of toads for biocontrol, and extending through failed attempts to predict future patterns of toad colonisation and impact, or to devise practical means to ameliorate that impact. In our (highly biased) opinion, progress in understanding such issues and in developing effective means of toad control emerged only from detailed ecological research on toad biology, rather than enthusiastic but poorly informed attempts to find better ways to slaughter toads. The story of cane toad science in Australia is a cautionary tale for our ability to predict the future, because, to date, we have done an abysmal job of doing so. ‘In the biological control of insect pests , … perhaps more than in any other [field], the path to successful achievement is strewn with the remains of optimistic attempts which have ended in abject failure. … Such a project is not to be embarked upon lightheartedly, but only after the most mature consideration, since a false step may have most disastrous … consequences through the upsetting of the whole biological balance.’ R. W. Mungomery (1934, p. 5), written the year before he brought cane toads to Australia.

At the edge of a biological invasion, evolutionary processes (spatial sorting, natural selection) often drive increases in dispersal. Although numerous traits influence an individual's displacement (e.g. speed, stamina), one of the most important is path straightness. A straight (i.e. highly correlated) path strongly enhances overall dispersal rate relative to time and energetic cost. Thus, we predict that, if path straightness has a genetic basis, organisms in the invasion vanguard will exhibit straighter paths than those following behind. Our studies on invasive cane toads ( Rhinella marina ) in tropical Australia clearly support this prediction. Radio-tracking of field-collected toads at a single site showed that path straightness steadily decreased over the first 10 years post-invasion. Consistent with an evolved (genetic) basis to that behavioural shift, path straightness of toads reared under common garden conditions varied according to the location of their parents' origin. Offspring produced by toads from the invasion vanguard followed straighter paths than did those produced by parents from long-established populations. At the individual level, offspring exhibited similar path straightness to their parents. The dramatic acceleration of the cane toad invasion through tropical Australia has been driven, in part, by the evolution of a behavioural tendency towards dispersing in a straight line.

In many anuran species, males vocalize to attract females but will grasp any female that comes within reach and retain their hold unless displaced by a rival male. Thus, female anurans may face strong selection to repel unwanted suitors, but no mechanism is known for doing so. We suggest that a defensive trait (the ability to inflate the body to ward off attack) has been co-opted for this role: by inflating their bodies, females are more difficult for males to grasp and hence, it is easier for another male to displace an already amplexed rival. Inflating a model female cane toad ( Bufo marinus ) strongly reduced a male's ability to maintain amplexus; and females who were experimentally prevented from inflating their bodies experienced no successful takeovers from rival males, in contrast to control females. Thus, the ability of a female cane toad to inflate her body may allow her to manipulate the outcome of male–male competition. This overlooked mechanism of anuran mate choice may reflect a common evolutionary pattern, whereby females co-opt defensive traits for use in sexual selection.

The impact of invasive species on biodiversity has attracted considerable study, but impacts of the invasion process on the invaders themselves remain less clear. Invading species encounter conditions different from those in their ancestral habitats and are subject to intense selection for rapid dispersal. The end result may be significant stress on individual organisms, with consequent health problems. Our studies on invasive cane toads in Australia reveal severe spinal arthritis in ≈10% of large adult toads, associated with the same factors (large body size, frequent movement, and relatively long legs) that have enabled toads to invade so rapidly across the Australian tropics.

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.

In order to investigate population history and demography in skinks endemic to the wet tropics of Australia, multiple nuclear DNA markers were sought. The utility of 72 primers (including 63 published intron-spanning 'CATS' primers) was tested.. Seven loci were characterized and shown to be single copy by single-strand conformation polymorphism analysis. Primers to five nuclear loci were developed, four with utility in skinks and three with utility in frogs. These observations extend the available information on intron-spanning primers for amphibians and reptiles.

Populations on the edge of an expanding range are subject to unique evolutionary pressures acting on their life-history and dispersal traits. Empirical evidence and theory suggest that traits there can evolve rapidly enough to interact with ecological dynamics, potentially giving rise to accelerating spread. Nevertheless, which of several evolutionary mechanisms drive this interaction between evolution and spread remains an open question. We propose an integrated theoretical framework for partitioning the contributions of different evolutionary mechanisms to accelerating spread, and we apply this model to invasive cane toads in northern Australia. In doing so, we identify a previously unrecognised evolutionary process that involves an interaction between life-history and dispersal evolution during range shift. In roughly equal parts, life-history evolution, dispersal evolution and their interaction led to a doubling of distance spread by cane toads in our model, highlighting the potential importance of multiple evolutionary processes in the dynamics of range expansion.

Lee (1) suggests that spatial sorting will be important only under limited circumstances, that it may often affect traits also subject to natural selection, and that it will enhance the effectiveness of selection by increasing phenotypic variance via positive assortative mating. These points build on the arguments advanced in our original paper, and we broadly agree with him.

Predicting which species will be affected by an invasive taxon is critical to developing conservation priorities, but this is a difficult task. A previous study on the impact of invasive cane toads (Bufo marinus) on Australian snakes attempted to predict vulnerability a priori based on the assumptions that any snake species that eats frogs, and is vulnerable to toad toxins, may be at risk from the toad invasion. We used time-series analyses to evaluate the accuracy of that prediction, based on >3600 standardized nocturnal surveys over a 138-month period on 12 species of snakes and lizards on a floodplain in the Australian wet-dry tropics, bracketing the arrival of cane toads at this site. Contrary to prediction, encounter rates with most species were unaffected by toad arrival, and some taxa predicted to be vulnerable to toads increased rather than declined (e.g., death adder Acanthophis praelongus; Children's python Antaresia childreni). Indirect positive effects of toad invasion (perhaps mediated by toad-induced mortality of predatory varanid lizards) and stochastic weather events outweighed effects of toad invasion for most snake species. Our study casts doubt on the ability of a priori desktop studies, or short-term field surveys, to predict or document the ecological impact of invasive species.

Darwin's naturalization hypothesis predicts that the success of alien invaders will decrease with increasing taxonomic similarity to the native community. Alternatively, shared traits between aliens and the native assemblage may preadapt aliens to their novel surroundings, thereby facilitating establishment (the preadaptation hypothesis). Here we examine successful and failed introductions of amphibian species across the globe and find that the probability of successful establishment is higher when congeneric species are present at introduction locations and increases with increasing congener species richness. After accounting for positive effects of congeners, residence time, and propagule pressure, we also find that invader establishment success is higher on islands than on mainland areas and is higher in areas with abiotic conditions similar to the native range. These findings represent the first example in which the preadaptation hypothesis is supported in organisms other than plants and suggest that preadaptation has played a critical role in enabling introduced species to succeed in novel environments.

Aim Invasive species often exhibit a highly non-random suite of traits relative to non-invasive taxa, and these biases reflect strong selection at a series of steps along the invasion pathway.Here we investigate traits that are favoured in thefirst of these steps: the introduction of species outside their native geographic range.We use the global introduction of amphibians as our case study. Location Global. Methods We examined whether taxonomy, body size and attributes of the native geographicrangepredictthelikelihoodof anintroductioneventinamphibians.We then determined whether these characteristics differed between amphibian species that have been introduced intentionally and those that have been introduced unintentionally (i.e. stowaways). Results Comparisons of introduced and non-introduced amphibians reveal significant biases with respect to taxonomic position (c. 50% of all introduced species originate from only 5% of all families), and characteristics of the native geographic range (most introduced species originate from the Northern Hemisphere,occupy a wide geographic range and are sympatric with high densities of humans). Many of thesebiasespresumablyreflecttheeaseandlikelihoodofcapturingandtransporting such animals.Additionally, intentionally introduced species are of larger than average body size,occupy higher elevations in their native ranges,and are more likely to originate from the Northern Hemisphere than unintentionally introduced species. Main conclusions Introduced amphibian species are not a random subset of the global amphibian fauna with respect to taxonomic affiliation and biogeography, and this restricts our ability to make robust generalizations regarding the ecological determinants of introduction success. Nevertheless, many of our findings are similar to those revealed by previous analyses of vertebrate and invertebrate introductions. Thus, our study suggests that biases in the anthropogenic mechanisms involved in transporting species around the globe are surprisingly consistent across broadly divergent taxa.

Adaptations that enhance fitness in one situation can become liabilities if circumstances change. In tropical Australia, native snake species are vulnerable to the invasion of toxic cane toads. Death adders ( Acanthophis praelongus ) are ambush foragers that (i) attract vertebrate prey by caudal luring and (ii) handle anuran prey by killing the frog then waiting until the frog's chemical defences degrade before ingesting it. These tactics render death adders vulnerable to toxic cane toads ( Bufo marinus ), because toads elicit caudal luring more effectively than do native frogs, and are more readily attracted to the lure. Moreover, the strategy of delaying ingestion of a toad after the strike does not prevent fatal poisoning, because toad toxins (unlike those of native frogs) do not degrade shortly after the prey dies. In our laboratory and field trials, half of the death adders died after ingesting a toad, showing that the specialized predatory behaviours death adders use to capture and process prey render them vulnerable to this novel prey type. The toads' strong response to caudal luring also renders them less fit than native anurans (which largely ignored the lure): all toads bitten by adders died. Together, these results illustrate the dissonance in behavioural adaptations that can arise following the arrival of invasive species, and reveal the strong selection that occurs when mutually naive species first interact.

Current approaches to modeling range advance assume that the distribution describing dispersal distances in the population (the "dispersal kernel") is a static entity. We argue here that dispersal kernels are in fact highly dynamic during periods of range advance because density effects and spatial assortment by dispersal ability ("spatial selection") drive the evolution of increased dispersal on the expanding front. Using a spatially explicit individual-based model, we demonstrate this effect under a wide variety of population growth rates and dispersal costs. We then test the possibility of an evolved shift in dispersal kernels by measuring dispersal rates in individual cane toads (Bufo marinus) from invasive populations in Australia (historically, toads advanced their range at 10 km/year, but now they achieve55 km/year in the northern part of their range). Under a common-garden design, we found a steady increase in dispersal tendency with distance from the invasion origin. Dispersal kernels on the invading front were less kurtotic and less skewed than those from origin populations. Thus, toads have increased their rate of range expansion partly through increased dispersal on the expanding front. For accurate long-range forecasts of range advance, we need to take into account the potential for dispersal kernels to be evolutionarily dynamic.

A mechanistic understanding of factors influencing the dispersal behavior of metamorph cane toads (Bufo marinus) has direct conservation relevance in Australia. These invasive anurans are toxic to native predators, and if we can predict their distribution across the landscape, we can also predict (and perhaps, manage) the scale of their impact. We propose that the major drivers of metamorph distribution are the risk of dehydration (restricting the young toads to moist substrates near pond margins) and biotic advantages to dispersal away from the pond (especially, less risk of cannibalism). To test this model, we investigated the influence of abiotic and biotic cues on the behavior of individual toads in the laboratory. Substrate moisture levels strongly influenced metamorph activity levels and habitat selection: dry substrates induced most metamorphs to remain near water. The only biotic cue to influence metamorph dispersal was proximity of a larger (cannibalistic) conspecific; a cannibal's presence at the pond margin caused most metamorphs to spend less time there, and as a consequence, to dehydrate more rapidly. Our results suggest that the spatial and temporal distribution of metamorph cane toads reflects a trade-off between competing risks: the danger of desiccation tends to keep young toads close to the pond margin in dry conditions, whereas the danger of cannibalism stimulates dispersal.

The wMel infection of Drosophila melanogaster was successfully transferred into Aedes aegypti mosquitoes where it has the potential to suppress dengue and other arboviruses. The infection was subsequently spread into two natural populations at Yorkeys Knob and Gordonvale near Cairns, Queensland in 2011. Here we report on the stability of the infection following introduction and we characterize factors influencing the ongoing dynamics of the infection in these two populations. While the Wolbachia infection always remained high and near fixation in both locations, there was a persistent low frequency of uninfected mosquitoes. These uninfected mosquitoes showed weak spatial structure at both release sites although there was some clustering around two areas in Gordonvale. Infected females from both locations showed perfect maternal transmission consistent with patterns previously established pre-release in laboratory tests. After >2 years under field conditions, the infection continued to show complete cytoplasmic incompatibility across multiple gonotrophic cycles but persistent deleterious fitness effects, suggesting that host effects were stable over time. These results point to the stability of Wolbachia infections and their impact on hosts following local invasion, and also highlight the continued persistence of uninfected individuals at a low frequency most likely due to immigration., Author Summary The wMel infection is a Wolbachia infection introduced into Aedes aegypti mosquito populations; wMel can provide potential suppression of dengue if the infection persists in populations. We show that the infection has persisted at a high frequency since its initial introduction into two natural populations in North Queensland, Australia. The infection, which is inherited through females, appears perfectly transmitted to offspring in the field. It has continued to produce a high level of incompatibility when infected males are mated with uninfected females; these females are likely to enter populations at a low frequency as migrants. These features ensure that the infection will stay at a high frequency in populations, but costs prevent its rapid spread.

Pathogen spread can cause population declines and even species extinctions. Nonetheless, in the absence of tailored monitoring schemes, documenting pathogen spread can be difficult. In the case of worldwide amphibian declines the best present understanding is that the chytrid fungus Batrachochytrium dendrobatidis (Bd) has recently spread, causing amphibian declines and extinction in the process. However, good evidence demonstrating pathogen arrival followed by amphibian decline is rare, and analysis of putative evidence is often inadequate. Here we attempt to examine the relationship between Bd arrival and amphibian decline across north-eastern Australia, using sites where a wave-like pattern of amphibian decline was first noticed and at which intensive research has since been conducted. We develop an analytical framework that allows rigorous estimation of pathogen arrival date, which can then be used to test for a correlation between the time of pathogen arrival and amphibian decline across sites. Our results show that, with the current dataset, the earliest possible arrival date of Bd in north-eastern Australia is completely unresolved; Bd could have arrived immediately before sampling commenced or may have arrived thousands of years earlier, the present data simply cannot say. The currently available data are thus insufficient to assess the link between timing of pathogen arrival and population decline in this part of the world. This data insufficiency is surprising given that there have been decades of research on chytridiomycosis in Australia and that there is a general belief that the link between Bd arrival and population decline is well resolved in this region. The lack of data on Bd arrival currently acts as a major impediment to determining the role of environmental factors in driving the global amphibian declines, and should be a major focus of future research.