RESUMO
Apex predators play critical ecological roles, making their conservation a high priority. In tropical Australia, some populations of freshwater crocodiles (Crocodylus johnstoni) have plummeted by greater than 70% due to lethal ingestion of toxic invasive cane toads (Rhinella marina). Laboratory-based research has identified conditioned taste aversion (CTA) as a way to discourage consumption of toads. To translate those ideas into landscape-scale management, we deployed 2395 baits (toad carcasses with toxin removed and containing a nausea-inducing chemical) across four gorge systems in north-western Australia and monitored bait uptake with remote cameras. Crocodile abundance was quantified with surveys. Free-ranging crocodiles rapidly learned to avoid toad baits but continued to consume control (chicken) baits. Toad invasion at our sites was followed by high rates of crocodile mortality (especially for small individuals) at a control site but not at nearby treatment sites. In areas with high connectivity to other waterbodies, repeated baiting over successive years had continuing positive impacts on crocodile survival. In summary, we succeeded in buffering the often-catastrophic impact of invasive cane toads on apex predators.
Assuntos
Jacarés e Crocodilos , Espécies Introduzidas , Animais , Jacarés e Crocodilos/fisiologia , Paladar , Aprendizagem da Esquiva , Comportamento Predatório , Bufo marinus/fisiologia , Austrália OcidentalRESUMO
Natural populations can show rapid adaptive responses to intense (human-mediated) environmental change. The potential for exploiting rapidly evolved traits for conservation management has been often discussed but rarely implemented. Capitalizing on a well-studied biological invasion, we here explore the idea that rapid phenotypic change in the invaders, their pathogens, and the native biota provide opportunities for managers to control invader abundance and buffer adverse impacts on native wildlife. Intensive studies of the invasion of tropical Australia by cane toads (Rhinella marina) have identified newly evolved vulnerabilities that we could exploit for toad control; and newly evolved resilience of native wildlife that we could exploit for impact reduction. For example, distinctive phenotypes of toads at the expanding range edge enhance dispersal rate but reduce reproductive output, intraspecific competitive ability, and immunocompetence; and the evolution of larval cannibalism creates opportunities not only for species-specific trapping of toad tadpoles, but also could be exploited (when allied to emerging CRISPR-Cas9 techniques) to intensify intraspecific conflict in invasive toads. That is, we could use the invasive species to control their own populations. This case study illustrates the potential of detailed basic research to identify novel approaches for conservation.
Assuntos
Animais Selvagens , Espécies Introduzidas , Animais , Humanos , Bufo marinus/fisiologia , Austrália , Larva , FenótipoRESUMO
Bacterial assemblages on amphibian skin may play an important role in protecting hosts against infection. In hosts that occur over a range of environments, geographic variation in composition of bacterial assemblages might be due to direct effects of local factors and/or to evolved characteristics of the host. Invasive cane toads (Rhinella marina) are an ideal candidate to evaluate environmental and genetic mechanisms, because toads have evolved major shifts in physiology, morphology, and behavior during their brief history in Australia. We used samples from free-ranging toads to quantify site-level differences in bacterial assemblages and a common-garden experiment to see if those differences disappeared when toads were raised under standardised conditions at one site. The large differences in bacterial communities on toads from different regions were not seen in offspring raised in a common environment. Relaxing bacterial clustering to operational taxonomic units in place of amplicon sequence variants likewise revealed high similarity among bacterial assemblages on toads in the common-garden study, and with free-ranging toads captured nearby. Thus, the marked geographic divergence in bacterial assemblages on wild-caught cane toads across their Australian invasion appears to result primarily from local environmental effects rather than evolved shifts in the host.
Assuntos
Espécies Introduzidas , Animais , Bufo marinus/fisiologia , Austrália , FenótipoRESUMO
Animals move across a wide range of surface conditions in real-world environments to acquire resources and avoid predation. To effectively navigate a variety of surfaces, animals rely on several mechanisms including intrinsic mechanical responses, spinal-level central pattern generators, and neural commands that require sensory feedback. Muscle spindle Ia afferents play a critical role in providing sensory feedback and informing motor control strategies across legged vertebrate locomotion, which is apparent in cases where this sensory input is compromised. Here, we tested the hypothesis that spindle Ia afferents from hindlimb muscles are important for coordinating forelimb landing behavior in the cane toad. We performed bilateral sciatic nerve reinnervations to ablate the stretch reflex from distal hindlimb muscles while allowing for motor neuron recovery. We found that toads significantly delayed the onset and reduced the activation duration of their elbow extensor muscle following spindle Ia afferent ablation in the hindlimbs. However, reinnervated toads achieved similar elbow extension at touchdown to that of their pre-surgery state. Our results suggest that while toads likely tuned the activation timing of forelimb muscles in response to losing Ia afferent sensation from the hindlimbs they were likely able to employ compensatory strategies that allowed them to continue landing effectively with reduced sensory information during take-off. These findings indicate muscle spindle Ia afferents may contribute to tuning complex movements involving multiple limbs.
Assuntos
Extremidade Inferior , Fusos Musculares , Animais , Fusos Musculares/fisiologia , Membro Anterior/fisiologia , Membro Posterior/fisiologia , Bufo marinus/fisiologiaRESUMO
As an invasive organism spreads into a novel environment, it may encounter strong selective pressures to adapt to abiotic and biotic challenges. We examined the effect of water temperature during larval life on rates of survival and growth of the early life-history stages of cane toads (Rhinella marina) from two geographic regions (tropical vs. temperate) in the species' invaded range in eastern Australia. If local adaptation at the southern (cool-climate) invasion front has extended the cold-tolerance of early life-stages, we would expect to see higher viability of southern-population toads under cooler conditions. Our comparisons revealed no such divergence: the effects of water temperature on rates of larval survival and growth, time to metamorphosis, size at metamorphosis and locomotor performance of metamorphs were similar in both sets of populations. In two cases where tropical and temperate-zone populations diverged in responses to temperature, the tropical animals performed better at low to medium temperatures than did conspecifics from cooler regions. Adaptation to low temperatures in the south might be constrained by behavioural shifts (e.g., in reproductive seasonality, spawning-site selection) that allow toads to breed in warmer water even in cool climates, by gene flow from warmer-climate populations, or by phylogenetic conservatism in these traits.
Assuntos
Clima , Espécies Introduzidas , Animais , Bufo marinus/fisiologia , Larva , Filogenia , ÁguaRESUMO
This paper reports a series of tests for fore- and hind-limb preferences used by cane toads, Rhinella marina, to assist returning to the righted position after being overturned. We confirm the strong and significant right-handedness reported in this species, which under certain conditions exceeded 90% right-hand preference at the group level. Toads were tested under a variety of conditions including horizontal and inclined surfaces, with and without the opportunity for the forelimbs to grasp a support, in order to assess the effects of different vestibular and proprioceptive input on the strength and direction of fore- and hind-limb preferences. A range of behavioural strategies indicated learning effects; however, the strength or direction of limb preferences did not increase significantly with experience, even in toads retested multiple times. Comparisons with the mammalian condition for limb preferences are discussed with relevance to practice effects and established limb preferences, and to effects associated with arousal or stress. In contrast to the expectation that handedness in toads represents intentional or voluntary preferences, the presence of lateralized central pattern generators in the toads is postulated to explain the different forms of lateralization revealed by our tests.
Assuntos
Lateralidade Funcional , Mamíferos , Animais , Bufo marinus/fisiologia , Reflexo de EndireitamentoRESUMO
Invasions often accelerate through time, as dispersal-enhancing traits accumulate at the expanding range edge. How does the dispersal behaviour of individual organisms shift to increase rates of population spread? We collate data from 44 radio-tracking studies (in total, of 650 animals) of cane toads (Rhinella marina) to quantify distances moved per day, and the frequency of displacement in their native range (French Guiana) and two invaded areas (Hawai'i and Australia). We show that toads in their native-range, Hawai'i and eastern Australia are relatively sedentary, while toads dispersing across tropical Australia increased their daily distances travelled from 20 to 200 m per day. That increase reflects an increasing propensity to change diurnal retreat sites every day, as well as to move further during each nocturnal displacement. Daily changes in retreat site evolved earlier than did changes in distances moved per night, indicating a breakdown in philopatry before other movement behaviours were optimised to maximise dispersal.
Assuntos
Bufo marinus/fisiologia , Bufonidae/fisiologia , Espécies Introduzidas , Distribuição Animal/fisiologia , Migração Animal/fisiologia , Animais , Austrália , Ecossistema , Guiana Francesa , Havaí , Modelos Biológicos , Tecnologia de Sensoriamento RemotoRESUMO
Biotic conflict can create evolutionary arms races, in which innovation in one group increases selective pressure on another, such that organisms must constantly adapt to maintain the same level of fitness. In some cases, this process is driven by conflict among members of the same species. Intraspecific conflict can be an especially important selective force in high-density invasive populations, which may favor the evolution of strategies for outcompeting or eliminating conspecifics. Cannibalism is one such strategy; by killing and consuming their intraspecific competitors, cannibals enhance their own performance. Cannibalistic behaviors may therefore be favored in invasive populations. Here, we show that cane toad tadpoles (Rhinella marina) from invasive Australian populations have evolved an increased propensity to cannibalize younger conspecifics as well as a unique adaptation to cannibalism-a strong attraction to vulnerable hatchlings-that is absent in the native range. In response, vulnerable conspecifics from invasive populations have evolved both stronger constitutive defenses and greater cannibal-induced plastic responses than their native range counterparts (i.e., rapid prefeeding development and inducible developmental acceleration). These inducible defenses are costly, incurring performance reductions during the subsequent life stage, explaining why plasticity is limited in native populations where hatchlings are not targeted by cannibalistic tadpoles. These results demonstrate the importance of intraspecific conflict in driving rapid evolution, highlight how plasticity can facilitate adaptation following shifts in selective pressure, and show that evolutionary processes can produce mechanisms that regulate invasive populations.
Assuntos
Evolução Biológica , Bufo marinus/fisiologia , Canibalismo , Espécies Introduzidas , Adaptação Fisiológica , Animais , Feminino , MasculinoRESUMO
Biological invasions can massively disrupt ecosystems, but evolutionary and ecological adjustments may modify the magnitude of that impact through time. Such post-colonisation shifts can change priorities for management. We quantified the abundance of two species of giant monitor lizards, and of the availability of their mammalian prey, across 45 sites distributed across the entire invasion trajectory of the cane toad (Rhinella marina) in Australia. One varanid species (Varanus panoptes from tropical Australia) showed dramatic population collapse with toad invasion, with no sign of recovery at most (but not all) sites that toads had occupied for up to 80 years. In contrast, abundance of the other species (Varanus varius from eastern-coastal Australia) was largely unaffected by toad invasion. That difference might reflect availability of alternative food sources in eastern-coastal areas, perhaps exacerbated by the widespread prior collapse of populations of small mammals across tropical (but not eastern) Australia. According to this hypothesis, the impact of cane toads on apex predators has been exacerbated and prolonged by a scarcity of alternative prey. More generally, multiple anthropogenically-induced changes to natural ecosystems may have synergistic effects, intensifying the impacts beyond that expected from either threat in isolation.
Assuntos
Bufo marinus/fisiologia , Ecossistema , Espécies Introduzidas , Lagartos/fisiologia , Modelos Biológicos , Comportamento Predatório/fisiologia , Animais , AustráliaRESUMO
Chemical cues produced by late-stage embryos of the cane toad (Rhinella marina) attract older conspecific larvae, which are highly cannibalistic and can consume an entire clutch. To clarify the molecular basis of this attraction response, we presented captive tadpoles with components present in toad eggs. As previously reported, attractivity arises from the distinctive toxins (bufadienolides) produced by cane toads, with some toxins (e.g., bufagenins) much stronger attractants than others (e.g., bufotoxins). Extracts of frozen toad parotoid glands (rich in bufagenins) were more attractive than were fresh MeOH extracts of the parotoid secretion (rich in bufotoxins), and purified marinobufagin was more effective than marinobufotoxin. Cardenolide aglycones (e.g., digitoxigenin) were active attractors, whereas C-3 glycosides (e.g., digoxin, oubain) were far less effective. A structure-activity relationship study revealed that tadpole attractant potency strongly correlated with Na+/K+ ATPase inhibitory activity, suggesting that tadpoles monitor and rapidly react to perturbations to Na+/K+ ATPase activity.
Assuntos
Bufanolídeos/química , Bufo marinus/fisiologia , Canibalismo , Toxinas Biológicas/química , Animais , Larva/efeitos dos fármacos , Larva/fisiologiaRESUMO
In response to novel environments, invasive populations often evolve rapidly. Standing genetic variation is an important predictor of evolutionary response but epigenetic variation may also play a role. Here, we use an iconic invader, the cane toad (Rhinella marina), to investigate how manipulating epigenetic status affects phenotypic traits. We collected wild toads from across Australia, bred them, and experimentally manipulated DNA methylation of the subsequent two generations (G1, G2) through exposure to the DNA methylation inhibitor zebularine and/or conspecific tadpole alarm cues. Direct exposure to alarm cues (an indicator of predation risk) increased the potency of G2 tadpole chemical cues, but this was accompanied by reductions in survival. Exposure to alarm cues during G1 also increased the potency of G2 tadpole cues, indicating intergenerational plasticity in this inducible defence. In addition, the negative effects of alarm cues on tadpole viability (i.e. the costs of producing the inducible defence) were minimized in the second generation. Exposure to zebularine during G1 induced similar intergenerational effects, suggesting a role for alteration in DNA methylation. Accordingly, we identified intergenerational shifts in DNA methylation at some loci in response to alarm cue exposure. Substantial demethylation occurred within the sodium channel epithelial 1 subunit gamma gene (SCNN1G) in alarm cue exposed individuals and their offspring. This gene is a key to the regulation of sodium in epithelial cells and may help to maintain the protective epidermal barrier. These data suggest that early life experiences of tadpoles induce intergenerational effects through epigenetic mechanisms, which enhance larval fitness. This article is part of the theme issue 'How does epigenetics influence the course of evolution?'
Assuntos
Bufo marinus/fisiologia , Metilação de DNA , Epigênese Genética , Características de História de Vida , Animais , Austrália , Bufo marinus/genética , Bufo marinus/crescimento & desenvolvimento , Sinais (Psicologia) , Citidina/administração & dosagem , Citidina/análogos & derivados , Espécies Introduzidas , Larva/efeitos dos fármacos , Larva/crescimento & desenvolvimento , Larva/fisiologiaRESUMO
If optimal investment in anti-predator defences depends on predation risk, invading new regions (and thus, encountering different predators) may favour shifts in that investment. Cane toads offer an ideal system to test this prediction: expensive anti-predator toxins are stored mainly in parotoid glands whose dimensions are easy to measure, and toad invasions have changed the suites of predators they encounter. Although plasticity may influence parotoid morphology, comparisons between parents and progeny revealed that gland dimensions were highly heritable. That heritability supports the plausibility of an evolved basis to variation in gland dimensions. Measurements of 3779 adult toads show that females have larger glands than males, invasive populations have larger glands than in the native-range, and that parotoid sexual size dimorphism varies strongly among invaded areas. Geographic variation in parotoid morphology may be driven by predation risk to both adult toads and offspring (provisioned with toxins by their mother), with toxins allocated to eggs exacerbating the risk of cannibalism but reducing the risk of interspecific predation. Investment into chemical defences has evolved rapidly during the cane toad's international diaspora, consistent with the hypothesis that organisms flexibly adjust resource allocation to anti-predator tactics in response to novel challenges.
Assuntos
Bufanolídeos/toxicidade , Bufo marinus/metabolismo , Glândula Parótida/fisiologia , Animais , Anuros/metabolismo , Anuros/fisiologia , Bufo marinus/fisiologia , Feminino , Espécies Introduzidas , Masculino , Glândula Parótida/metabolismo , Comportamento Predatório/fisiologia , Toxinas Biológicas/metabolismo , Toxinas Biológicas/fisiologiaRESUMO
Vulnerable native species may survive the impact of a lethally toxic invader by changes in behaviour, physiology and/or morphology. The roles of such mechanisms can be clarified by standardised testing. We recorded behavioural responses of monitor lizards (Varanus panoptes and V. varius) to legs of poisonous cane toads (Rhinella marina) and non-toxic control meals (chicken necks or chicken eggs and sardines) along 1300 and 2500 km transects, encompassing the toad's 85-year invasion trajectory across Australia as well as yet-to-be-invaded sites to the west and south of the currently colonised area. Patterns were identical in the two varanid species. Of monitors that consumed at least one prey type, 96% took control baits whereas toad legs were eaten by 60% of lizards in toad-free sites but 0% from toad-invaded sites. Our survey confirms that the ability to recognise and reject toads as prey enables monitor lizards to coexist with cane toads. As toxic invaders continue to impact ecosystems globally, it is vital to understand the mechanisms that allow some taxa to persist over long time-scales.
Assuntos
Comportamento Animal , Bufo marinus/fisiologia , Cadeia Alimentar , Espécies Introduzidas , Lagartos/fisiologia , Animais , AustráliaRESUMO
Amphibians in hot climates may be able to avoid high temperatures by controlling their rates of heating. In northern Australia, invasive cane toads (Rhinella marina) experience hot dry conditions in newly-colonized (western) sites but milder conditions in longer-occupied (eastern) sites. Under standardized conditions, toads from western sites heated less rapidly than did conspecifics from an eastern site. The availability of free water slowed heating rates of eastern but not western toads. Thus, the colonization of climatically extreme sites has been accompanied by a rapid shift in the toads' ability to remain cool under hot conditions, even when free water is not available.
Assuntos
Bufo marinus/crescimento & desenvolvimento , Espécies Introduzidas , Animais , Austrália , Temperatura Corporal , Bufo marinus/fisiologia , Clima , Ecossistema , História do Século XX , História do Século XXI , Temperatura Alta , Espécies Introduzidas/história , Masculino , Dinâmica Populacional/história , Água/químicaRESUMO
Cane toads (Rhinella marina) were introduced worldwide and have become invasive in multiple locations, representing a major driver of biodiversity loss through competition (food, shelter, territory), predation, and the poisoning of native species. These toads have been used in Australia as a model for studies concerning invasion biology and ecoimmunology, as longer-established (core) and invasion front (edge) populations show altered stress and immune response profiles. Although cane toads were also introduced into the United States in the 1950s, these patterns have yet to be evaluated for the populations spanning Florida. Toads introduced into Florida have dispersed primarily northward along a latitudinal gradient, where they encounter cooler temperatures that may further impact stress and immune differences between core and edge populations. In this study, we sampled cane toads from nine different locations spanning their invasion in Florida. Cane toads from southern populations showed higher plasma bacterial killing ability and natural antibody titers than the toads from the northern populations, indicating they have a better immune surveillance system. Also, southern toads were more responsive to a novel stressor (1 hr restraint), showing a higher increase in corticosterone levels. These results indicate that possible trade-offs have occurred between immune and stress responses as these toads have become established in northern cooler areas in Florida.
Assuntos
Bufo marinus/imunologia , Estresse Fisiológico/imunologia , Animais , Atividade Bactericida do Sangue , Bufo marinus/sangue , Bufo marinus/fisiologia , Corticosterona/sangue , Feminino , Florida , Testes de Hemaglutinação , Espécies Introduzidas , Linfócitos/fisiologia , Masculino , Neutrófilos/fisiologia , Estresse Fisiológico/fisiologia , TemperaturaRESUMO
Attempts to control invasive species using species-specific pheromones need to incorporate an understanding of interactive effects among those pathways. The larvae of invasive cane toads (Rhinella marina) utilise chemical cues to repulse, attract or suppress conspecific larvae. We can exploit these effects to reduce toad abundance, but the effects of each cue may not be additive. That is, exposure to one type of cue may lessen the impact of exposure to another cue. To assess this possibility, we exposed toad larvae to combinations of cues. Tadpoles that had been exposed to the suppression cue during larval development exhibited no response to the attraction cue, resulting in lower capture rates in attractant-baited traps. Suppression, however, did not affect a tadpole's response to the alarm cue, and exposure to the alarm cue during tadpole development did not affect response to the attraction cue. Tadpoles exposed to the suppression cue were smaller than control tadpoles at 10 days post-exposure, and consequently were more vulnerable to gape-limited invertebrate predators. Our results demonstrate that the responses by toad tadpoles to chemical cues interact in important ways, and are not simply additive when combined. Control efforts need to incorporate an understanding of such interactions if we are to most effectively use chemical-communication pathways to control invasive amphibians.
Assuntos
Bufo marinus/fisiologia , Espécies Introduzidas , Animais , Bufo marinus/crescimento & desenvolvimento , Feminino , Larva/crescimento & desenvolvimento , Larva/fisiologia , Feromônios/metabolismo , Comportamento PredatórioRESUMO
Although adult cane toads (Rhinella marina) are generally active only at night, a recent study reported that individuals of this species switched to diurnal activity in response to encountering a novel habitat type (deeply shaded gorges) in the course of their Australian invasion. Our sampling over a broader geographic scale challenges the idea that this behaviour is novel; we documented diurnal behaviour both in the species' native range and in several sites within the invaded range, in multiple habitat types. Diurnal activity was most common in the tropics and in areas where toads attain high population densities and are in poor body condition, suggesting that the expansion of activity times may be induced by intraspecific competition for food.
Assuntos
Bufo marinus/fisiologia , Ritmo Circadiano/fisiologia , Animais , Austrália , Comportamento Animal/fisiologia , Ecossistema , Guiana Francesa , Espécies IntroduzidasRESUMO
Controlled landing requires preparation. Mammals and bipedal birds vary how they prepare for landing by predicting the timing and magnitude of impact from the integration of visual and non-visual information. Here, we explore how the cane toad Rhinella marina - an animal that moves primarily through hopping - integrates sensory information to modulate landing preparation. Earlier work suggests that toads may modulate landing preparation using predictions of impact timing and/or magnitude based on non-visual sensory feedback during takeoff rather than visual cues about the landing itself. We disentangled takeoff and landing conditions by hopping toads off platforms of different heights while measuring electromyographic (EMG) activity of an elbow extensor (m. anconeus) and capturing high-speed images to quantify whole body and forelimb kinematics. This enabled us to test how toads integrate visual and non-visual information in landing preparation. We asked two questions: (1) when they conflict, do toads correlate landing preparation with takeoff or landing conditions? And (2) for hops with the same takeoff conditions, does visual information alter the timing of landing preparation? We found that takeoff conditions are a better predictor of the onset of landing preparation than landing conditions, but that visual information is not ignored. When hopping off higher platforms, toads start to prepare for landing later when takeoff conditions are invariant. This suggests that, unlike mammals, toads prioritize non-visual sensory feedback about takeoff conditions to coordinate landing, but that they do integrate visual information to fine-tune landing preparation.
Assuntos
Bufo marinus/fisiologia , Retroalimentação Sensorial , Locomoção/fisiologia , Animais , Fenômenos Biomecânicos , Feminino , Membro Anterior/fisiologiaRESUMO
Individuals at the leading edge of a biological invasion experience novel evolutionary pressures on mating systems, due to low population densities coupled with tradeoffs between reproduction and dispersal. Our dissections of >1,200 field-collected cane toads (Rhinella marina) at a site in tropical Australia reveal rapid changes in morphological and reproductive traits over a three-year period after the invaders first arrived. As predicted, individuals with dispersal-enhancing traits (longer legs, narrower heads) had reduced reproductive investment (lower gonad mass). Post-invasion, the population was increasingly dominated by individuals with less dispersive phenotypes and a higher investment into reproduction (including, increased expression of sexually dimorphic traits in males). These rapid shifts in morphology and reproductive biology emphasise the impacts of the invasion process on multiple, interlinked aspects of organismal biology.