Locomotor performance of cane toads differs between native-range and invasive populations.
ABSTRACT: Invasive species provide a robust opportunity to evaluate how animals deal with novel environmental challenges. Shifts in locomotor performance-and thus the ability to disperse-(and especially, the degree to which it is constrained by thermal and hydric extremes) are of special importance, because they might affect the rate that an invader can spread. We studied cane toads (Rhinella marina) across a broad geographical range: two populations within the species' native range in Brazil, two invasive populations on the island of Hawai'i and eight invasive populations encompassing the eastern, western and southern limits of the toad invasion in Australia. A toad's locomotor performance on a circular raceway was strongly affected by both its temperature and its hydration state, but the nature and magnitude of those constraints differed across populations. In their native range, cane toads exhibited relatively low performance (even under optimal test conditions) and a rapid decrease in performance at lower temperatures and hydration levels. At the other extreme, performance was high in toads from southern Australia, and virtually unaffected by desiccation. Hawai'ian toads broadly resembled their Brazilian conspecifics, plausibly reflecting similar climatic conditions. The invasion of Australia has been accompanied by a dramatic enhancement in the toads' locomotor abilities, and (in some populations) by an ability to maintain locomotor performance even when the animal is cold and/or dehydrated. The geographical divergences in performance among cane toad populations graphically attest to the adaptability of invasive species in the face of novel abiotic challenges.
Project description:Temperature has pervasive effects on physiological processes and is critical in setting species distribution limits. Since invading Australia, cane toads have spread rapidly across low latitudes, but slowly into higher latitudes. Low temperature is the likely factor limiting high-latitude advancement. Several previous attempts have been made to predict future cane toad distributions in Australia, but understanding the potential contribution of phenotypic plasticity and adaptation to future range expansion remains challenging. Previous research demonstrates the considerable thermal metabolic plasticity of the cane toad, but suggests limited thermal plasticity of locomotor performance. Additionally, the oxygen-limited thermal tolerance hypothesis predicts that reduced aerobic scope sets thermal limits for ectotherm performance. Metabolic plasticity, locomotor performance and aerobic scope are therefore predicted targets of natural selection as cane toads invade colder regions. We measured these traits at temperatures of 10, 15, 22.5 and 30°C in low- and high-latitude toads acclimated to 15 and 30°C, to test the hypothesis that cane toads have adapted to cooler temperatures. High-latitude toads show increased metabolic plasticity and higher resting metabolic rates at lower temperatures. Burst locomotor performance was worse for high-latitude toads. Other traits showed no regional differences. We conclude that increased metabolic plasticity may facilitate invasion into higher latitudes by maintaining critical physiological functions at lower temperatures.
Project description:Biological invasions can stimulate rapid shifts in organismal performance, via both plasticity and adaptation. We can distinguish between these two proximate mechanisms by rearing offspring from populations under identical conditions and measuring their locomotor abilities in standardized trials. We collected adult cane toads (Rhinella marina) from invasive populations that inhabit regions of Australia with different climatic conditions. We bred those toads and raised their offspring under common-garden conditions before testing their locomotor performance. At high (but not low) temperatures, offspring of individuals from a hotter location (northwestern Australia) outperformed offspring of conspecifics from a cooler location (northeastern Australia). This disparity indicates that, within less than 100 years, thermal performance in cane toads has adapted to the novel abiotic challenges that cane toads have encountered during their invasion of tropical Australia.
Project description:Understanding negative effects of native species on introduced taxa may suggest novel ways to control the invasive species by enhancing such effects. Previous studies have reported that the larvae of invasive cane toads (Rhinella marina) are suppressed by competition with the larvae of native anurans in Australia, but not in North America. We conducted laboratory trials to measure the effect of exposure to the larvae of Japanese frogs (Microhyla ornata, Fejervarya sakishimensis, Rhacophorus owstoni) on rates of survival, growth and development of cane toad tadpoles in Ishigaki Island, in southern Japan. Survival rates were not affected by native species, but competition with Dicroglossids and Rhacophorids (but not Microhylids) strongly reduced rates of growth and development in the tadpoles of cane toads. Dicroglossid tadpoles also reduced the body condition to toad tadpoles in addition to effects on SVL and mass. Encouraging populations of native frogs in toad-invaded areas of Japan thus may help to reduce the numbers of invasive cane toads.
Project description:Cane toads are a notorious invasive species, inhabiting over 1.2 million km2 of Australia and threatening native biodiversity. The release of pathogenic cane toad viruses is one possible biocontrol strategy yet is currently hindered by the poorly described cane toad virome. Metatranscriptomic analysis of 16 cane toad livers revealed the presence of a novel and full-length picornavirus, Rhimavirus A (RhiV-A), a member of a reptile- and amphibian-specific cluster of the Picornaviridae basal to the Kobuvirus-like group. In the combined liver transcriptome, we also identified a complete genome sequence of a distinct epsilonretrovirus, Rhinella marina endogenous retrovirus (RMERV). The recently sequenced cane toad genome contains 8 complete RMERV proviruses as well as 21 additional truncated insertions. The oldest full-length RMERV provirus was estimated to have inserted 1.9 million years ago (MYA). To screen for these viral sequences in additional toads, we analyzed publicly available transcriptomes from six diverse Australian locations. RhiV-A transcripts were identified in toads sampled from three locations across 1,000 km of Australia, stretching to the current Western Australia (WA) invasion front, while RMERV transcripts were observed at all six sites. Finally, we scanned the cane toad genome for nonretroviral endogenous viral elements, finding three sequences related to small DNA viruses in the family Circoviridae This shows ancestral circoviral infection with subsequent genomic integration. The identification of these current and past viral infections enriches our knowledge of the cane toad virome, an understanding of which will facilitate future work on infection and disease in this important invasive species.IMPORTANCE Cane toads are poisonous amphibians that were introduced to Australia in 1935 for insect control. Since then, their population has increased dramatically, and they now threaten many native Australian species. One potential method to control the population is to release a cane toad virus with high mortality rates, yet few cane toad viruses have been characterized. This study samples cane toads from different Australian locations and uses an RNA sequencing and computational approach to find new viruses. We report novel complete picornavirus and retrovirus sequences that were genetically similar to viruses infecting frogs, reptiles, and fish. Using data generated in other studies, we show that these viral sequences are present in cane toads from distinct Australian locations. Three sequences related to circoviruses were also found in the toad genome. The identification of new viral sequences will aid future studies that investigate their prevalence and potential as agents for biocontrol.
Project description:Invasive species often exhibit rapid evolutionary changes, and can provide powerful insights into the selective forces shaping phenotypic traits that influence dispersal rates and/or sexual interactions. Invasions also may modify sexual dimorphism. We measured relative lengths of forelimbs and hindlimbs of more than 3000 field-caught adult cane toads (Rhinella marina) from 67 sites in Hawai'i and Australia (1-80 years post-colonization), along with 489 captive-bred individuals from multiple Australian sites raised in a 'common garden' (to examine heritability and reduce environmental influences on morphology). As cane toads spread from east to west across Australia, the ancestral condition (long limbs, especially in males) was modified. Limb length relative to body size was first reduced (perhaps owing to natural selection on locomotor ability), but then increased again (perhaps owing to spatial sorting) in the invasion vanguard. In contrast, the sex disparity in relative limb length has progressively decreased during the toads' Australian invasion. Offspring reared in a common environment exhibited similar geographical divergences in morphology as did wild-caught animals, suggesting a genetic basis to the changes. Limb dimensions showed significant heritability (2-17%), consistent with the possibility of an evolved response. Cane toad populations thus have undergone a major shift in sexual dimorphism in relative limb lengths during their brief (81 years) spread through tropical Australia.
Project description:Commonly, invaders have different impacts in different places. The spread of cane toads (Rhinella marina: Bufonidae) has been devastating for native fauna in tropical Australia, but the toads' impact remains unstudied in temperate-zone Australia. We surveyed habitat characteristics and fauna in campgrounds along the central eastern coast of Australia, in eight sites that have been colonized by cane toads and another eight that have not. The presence of cane toads was associated with lower faunal abundance and species richness, and a difference in species composition. Populations of three species of large lizards (land mullets Bellatorias major, eastern water dragons Intellagama lesueurii, and lace monitors Varanus varius) and a snake (red-bellied blacksnake Pseudechis porphyriacus) were lower (by 84 to 100%) in areas with toads. The scarcity of scavenging lace monitors in toad-invaded areas translated into a 52% decrease in rates of carrion removal (based on camera traps at bait stations) and an increase (by 61%) in numbers of brush turkeys (Alectura lathami). The invasion of cane toads through temperate-zone Australia appears to have reduced populations of at least four anurophagous predators, facilitated other taxa, and decreased rates of scavenging. Our data identify a paradox: The impacts of cane toads are at least as devastating in southern Australia as in the tropics, yet we know far more about toad invasion in the sparsely populated wilderness areas of tropical Australia than in the densely populated southeastern seaboard.
Project description:Invasive species must deal with novel challenges, both from the alien environment and from pressures arising from range expansion per se (e.g. spatial sorting). Those conditions can create geographical variation in behaviour across the invaded range, as has been documented across regions of Australia invaded by cane toads; range-edge toads are more exploratory and willing to take risks than are conspecifics from the range-core. That behavioural divergence might be a response to range expansion and invasion per se, or to the different environments encountered. Climate differs across the cane toads' invasion range from the wet tropics of Queensland to the seasonally dry climates of northwestern Western Australia. The different thermal and hydric regimes may affect behavioural traits via phenotypic plasticity or through natural selection. We cannot tease apart the effects of range expansion versus climate in an expanding population but can do so in a site where the colonizing species was simultaneously released in all suitable areas, thus removing any subsequent phase of range expansion. Cane toads were introduced to Hawai'i in 1932; and thence to Australia in 1935. Toads were released in all major sugarcane-growing areas in Hawai'i within a 12-month period. Hence, Hawai'ian cane toads provide an opportunity to examine geographical divergence in behavioural traits in a climatically diverse region (each island has both wet and dry sides) in the absence of range expansion subsequent to release. We conducted laboratory-based behavioural trials testing exploration, risk-taking and response to novelty using field-caught toads from the wet and dry sides of two Hawai'ian islands (Oahu and Hawai'i). Toads from the dry side of Oahu had a higher propensity to take risks than did toads from the dry side of Hawai'i. Toads from Oahu were also more exploratory than were conspecifics from the island of Hawai'i. However, toads from wet versus dry climates were similar in all behaviours that we scored, suggesting that founder effects, genetic drift, or developmentally plastic responses to ecological factors other than climate may have driven behavioural divergence between islands.
Project description:Most ecological research on cane toads (Rhinella marina) has focused on invasive populations in Australia, ignoring other areas where toads have been introduced. We radio-tracked and spool-tracked 40 toads, from four populations on the island of Hawai'i. Toads moved extensively at night (mean 116 m, from spool-tracking) but returned to the same or a nearby retreat-site each day (from radio-tracking, mean distance between successive retreat sites 11 m; 0 m for 70% of records). Males followed straighter paths during nocturnal movements than did females. Because moist sites are scarce on the highly porous lava substrate, Hawai'ian toads depend on anthropogenic disturbance for shelter (e.g. beneath buildings), foraging (e.g. suburban lawns, golf courses) and breeding (artificial ponds). Foraging sites are further concentrated by a scarcity of flying insects (negating artificial lights as prey-attractors). Habitat use of toads shifted with time (at night, toads selected areas with less bare ground, canopy, understory and leaf-litter), and differed between sexes (females foraged in areas of bare ground with dense understory vegetation). Cane toads in Hawai'i thrive in scattered moist patches within a severely arid matrix, despite a scarcity of flying insects, testifying to the species' ability to exploit anthropogenic disturbance.
Project description:Infectious diseases are contributing to the decline of endangered amphibians. We identified myxosporean parasites, Myxidium spp. (Myxosporea: Myxozoa), in the brain and liver of declining native frogs, the Green and Golden Bell frog (Litoria aurea) and the Southern Bell frog (Litoria raniformis). We unequivocally identified two Myxidium spp. (both generalist) affecting Australian native frogs and the invasive Cane toad (Bufo marinus, syn. Rhinella marina) and demonstrated their association with disease. Our study tested the identity of Myxidium spp. within native frogs and the invasive Cane toad (brought to Australia in 1935, via Hawaii) to resolve the question whether the Cane toad introduced them to Australia. We showed that the Australian brain and liver Myxidium spp. differed 9%, 7%, 34% and 37% at the small subunit rDNA, large subunit rDNA, internal transcribed spacers 1 and 2, but were distinct from Myxidium cf. immersum from Cane toads in Brazil. Plotting minimum within-group distance against maximum intra-group distance confirmed their independent evolutionary trajectory. Transmission electron microscopy revealed that the brain stages localize inside axons. Myxospores were morphologically indistinguishable, therefore genetic characterisation was necessary to recognise these cryptic species. It is unlikely that the Cane toad brought the myxosporean parasites to Australia, because the parasites were not found in 261 Hawaiian Cane toads. Instead, these data support the enemy-release hypothesis predicting that not all parasites are translocated with their hosts and suggest that the Cane toad may have played an important spill-back role in their emergence and facilitated their dissemination. This work emphasizes the importance of accurate species identification of pathogens relevant to wildlife management and disease control. In our case it is paving the road for the spill-back role of the Cane toad and the parasite emergence.
Project description:As is common in biological invasions, the rate at which cane toads (<i>Rhinella marina</i>) have spread across tropical Australia has accelerated through time. Individuals at the invasion front travel further than range-core conspecifics and exhibit distinctive morphologies that may facilitate rapid dispersal. However, the links between these morphological changes and locomotor performance have not been clearly documented. We used raceway trials and high-speed videography to document locomotor traits (e.g. hop distances, heights, velocities, and angles of take-off and landing) of toads from range-core and invasion-front populations. Locomotor performance varied geographically, and this variation in performance was linked to morphological features that have evolved during the toads' Australian invasion. Geographical variation in morphology and locomotor ability was evident not only in wild-caught animals, but also in individuals that had been raised under standardized conditions in captivity. Our data thus support the hypothesis that the cane toad's invasion across Australia has generated rapid evolutionary shifts in dispersal-relevant performance traits, and that these differences in performance are linked to concurrent shifts in morphological traits.