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Impact of the invasive cane toad (Bufo marinus) on an Australian frog (Opisthodon ornatus) depends on reproductive timing

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Abstract

Invasive species are widely viewed as unmitigated ecological catastrophes, but the reality is more complex. Theoretically, invasive species could have negligible or even positive effects if they sufficiently reduce the intensity of processes regulating native populations. Understanding such mechanisms is crucial to predicting ultimate ecological impacts. We used a mesocosm experiment to quantify the impact of eggs and larvae of the introduced cane toad (Bufo marinus) on fitness-related traits (number, size and time of emergence of metamorphs) of a native Australian frog species (Opisthodon ornatus). The results depended upon the timing of oviposition of the two taxa, and hence the life-history stages that came into contact. Growth and survival of O. ornatus tadpoles were enhanced when they preceded B. marinus tadpoles into ponds, and reduced when they followed B. marinus tadpoles into ponds, relative to when tadpoles of both species were added to ponds simultaneously. The dominant tadpole-tadpole interaction is competition, and the results are consistent with competitive priority effects. However, these priority effects were reduced or reversed when O. ornatus tadpoles encountered B. marinus eggs. Predation on toxic toad eggs reduced the survival of O. ornatus and B. marinus. The consequent reduction in tadpole densities allowed the remaining O. ornatus tadpoles to grow more rapidly and to metamorphose at larger body sizes (>60% disparity in mean mass). Thus, exposure to B. marinus eggs reduced the number of O. ornatus metamorphs, but increased their body sizes. If the increased size at metamorphosis more than compensates for the reduced survival, the effective reproductive output of native anurans may be increased rather than decreased by the invasive toad. Minor interspecific differences in the seasonal timing of oviposition thus have the potential to massively alter the impact of invasive cane toads on native anurans.
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... One interesting example of competitive suppression involves the invasive cane toad (Rhinella marina). Experimental studies in two parts of the toads' invasive range (Australia and Ishigaki Island, Japan) have shown that the survival and growth of larval cane toads is strongly reduced by the presence of frog tadpoles [16][17][18][19] , via exploitative competition for food 20 . In these studies, the viability of a cane toad tadpole was reduced more by competition with a frog tadpole than with a conspecific toad tadpole-but why? ...
... 7,[27][28][29] ). However, we did not find a stronger competitive effect of frog tadpoles than of toad tadpoles, unlike the results of studies on invasive cane toads in Australia and Okinawa [16][17][18][19] . Why, then, are tadpoles of the cane toad more sensitive to the presence of frog tadpoles than conspecific toad tadpoles? ...
... Instead, the results for cane toads may reflect two aspects of this system. First, most of the Australian frog tadpoles tested were much larger than the toad tadpoles-in some cases, by a 20-fold margin [16][17][18] . Larger tadpoles may (in general) be better competitors (e.g. 30 ), and this effect may be stronger if the size disparity is greater. ...
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Competition within and among species can play a key role in structuring the assemblages of anuran tadpoles. Previous studies have reported that tadpoles of the invasive cane toad ( Rhinella marina ) are more strongly disadvantaged by the presence of native frog tadpoles than by the same number of conspecific toad tadpoles. That effect might arise from a lack of coevolution of the invasive toad with its competitors; and/or from a generalized superiority of frog tadpoles over toad tadpoles. To clarify those possibilities, we conducted experimental trials using the larvae of a native rather than invasive toad ( Bufo japonicus formosus in Japan) exposed to larvae of native anurans (the sympatric frogs Rana japonica and Rana ornativentris and the parapatric toad Bufo japonicus japonicus ). In intraspecific competition trials, higher densities of B. j. formosus prolonged the larval period and reduced size at metamorphosis, but did not affect survival. In interspecific competition trials, the effects of the other anuran species on B. j. formosus were similar to the effects of the same number of conspecific larvae. This similarity in impact of interspecific versus intraspecific competition argues against any overall competitive superiority of frog larvae over toad larvae. Instead, the vulnerability of larval cane toads to frog tadpoles may result from a lack of coevolutionary history.
... The cane toad (Rhinella marina), native to Central and tropical South America but introduced widely throughout the world as a biocontrol agent for insect pests of sugarcane crops [9], has been a popular study species for research on competition among tadpoles (Australia: [3,[10][11][12][13][14][15][16][17]; Philippines: [18]; Japan: [19]; USA: [20]; Puerto Rico: [21]). Most of these studies have looked at overall impacts and thus have not attempted to separate the impacts of exploitation from those of interference, but two studies have explicitly assessed interference competition. ...
... Our study was conducted with invasive cane toads in Australia. Indeed, all previous studies assessing competition involving cane toad tadpoles have been conducted in invasive populations (Australia: [3,[10][11][12][13][14][15][16][17]; Philippines: [18]; Japan: [19]; USA: [20]; Puerto Rico: [21]). We are unaware of any published studies on competition involving cane toad tadpoles in their native range. ...
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Competition among larval anurans can occur via interference as well as via a reduction in per-capita food supply. Previous research on intraspecific interference competition in cane toad (Rhinella marina) tadpoles found conflicting results, with one study detecting strong effects on tadpoles and another detecting no effects on metamorphs. A capacity to recover from competitive suppression by the time of metamorphosis might explain those contrasting impacts. In a laboratory experiment, we found that nine days of exposure to intraspecific interference competition strongly reduced tadpole growth and development, especially when the competing tadpoles were young (early-stage) individuals. Those competitive effects disappeared by the time of metamorphosis, with no significant effect of competition on metamorph body condition, size, larval period or survival. Temporal changes in the impact of competition were not related to tadpole density or to variation in water quality. The ability of larval cane toads to recover from intraspecific interference competition may enhance the invasive success of this species, because size at metamorphosis is a significant predictor of future fitness. Our study also demonstrates a cautionary tale: conclusions about the existence and strength of competitive interactions among anuran larvae may depend on which developmental stages are measured.
... As in many anuran species, cane toad tadpoles exhibit extreme developmental plasticity. For example, rates of development and growth are sensitive to abiotic factors (such as water temperature) and biotic factors (such as crowding, and intraspecific and interspecific competition: Crossland et al. 2009Crossland et al. , 2011Ducatez et al. 2016). In this study, we focus on a developmentally plastic response to chemical cues ("alarm cues") that alert a tadpole to heightened risk of predation. ...
... We investigated relationships between chronic exposure to alarm cues during early life, CpG methylation, and CORT levels in the cane toad. Australian cane toads are an iconic invasive species that are ideal for these investigations because they exhibit strong divergences in life-history traits, and differ in developmental plasticity and acute CORT responses across their range (Crossland et al. 2009(Crossland et al. , 2011Brown et al. 2015;Ducatez et al. 2016;Rollins et al. 2015;Shine 2018). Predation and zebularine exposure affected DNA methylation and whole body CORT levels, but these effects were locusspecific and life-stage dependent (Table 2). ...
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The developmental environment can exert powerful effects on animal phenotype. Recently epigenetic modifications have emerged as one mechanism that can modulate developmentally plastic responses to environmental variability. For example, the DNA methylation profile at promoters of hormone receptor genes can affect their expression and patterns of hormone release. Across taxonomic groups, epigenetic alterations have been linked to changes in glucocorticoid (GC) physiology. GCs are metabolic hormones that influence growth, development, transitions between life-history stages, and thus fitness. To date, relatively few studies have examined epigenetic effects on phenotypic traits in wild animals, especially in amphibians. Here, we examined the effects of exposure to predation threat and experimentally manipulated DNA methylation on corticosterone (CORT) levels in tadpoles and metamorphs of the invasive cane toad (Rhinella marina). We included offspring of toads sampled from populations across the species' Australian range. In these animals, exposure to chemical cues from injured conspecifics induces shifts in developmental trajectories, putatively as an adaptive response that lessens vulnerability to predation. We exposed tadpoles to these alarm cues, and measured changes in DNA methylation and CORT levels, both of which are mechanisms that have been implicated in the control of phenotypically plastic responses in tadpoles. To test the idea that DNA methylation drives shifts in GC physiology, we also experimentally manipulated methylation levels with the drug zebularine. We found differentially methylated regions between control tadpoles and their full-siblings exposed to alarm cues, zebularine or both treatments. However, the effects of these manipulations on methylation patterns were weaker than clutch (e.g. genetic, maternal, etc.) effects. CORT levels were higher in larval cane toads exposed to alarm cues and zebularine. We found little evidence of changes in DNA methylation across the glucocorticoid receptor gene (NR3C1) promoter region in response to alarm cue or zebularine exposure. In both alarm cue and zebularine-exposed individuals, we found differentially methylated DNA in the suppressor of cytokine signaling 3 gene (SOCS3), which may be involved in predator avoidance behavior. In total, our data reveal that alarm cues have significant impacts on tadpole physiology, but show only weak links between DNA methylation and CORT levels. We also identify genes containing differentially methylated regions in tadpoles exposed to alarm cues and zebularine, particularly in range-edge populations, that warrant further investigation.
... It was expected that disadvantaged tadpole species, in this case the Fowler's toad, would have lower survivorship and a lower weight at metamorphosis (Bardsley & Beebee, 1998;Cabrera-Guzmán et al., 2013;Griffiths, 1991 (Crossland et al., 2009). Fowler's toad tadpoles also had a lower weight at metamorphosis when raised with Gray Treefrog (Dryophytes versicolor) tadpoles than when raised alone (Parris & Cornelius, 2004). ...
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The outcomes of species interactions can vary by life stage, year, and surrounding environmental conditions. Amphibian species are expected to compete most strongly during their tadpole stage when they exist in the highest densities. Changes in arrival timing, surrounding aquatic communities, and yearly conditions could all affect the outcome of larval competition. In Long Point, Ontario, the Fowler's toad (Anaxyrus fowleri) is at the northern edge of its range and overlaps with the more common American toad (Anaxyrus americanus). Both species breed in ponds that encounter high inter-annual variation. To determine whether these species compete strongly, and if this effect was replicated across multiple years, we raised both species as tadpoles together and, apart, in mesocosms in 2018 and 2021. We measured survivorship to, weight at, and time to metamorphosis for both species in both years. We determined that the presence of American toad tadpoles consistently had a detrimental effect on Fowler's toad tadpoles, even though this effect presented itself differently across years. Our study suggests that competitive exclusion by American toads could be occurring at the edge of the Fowler's toad's range. This study further demonstrates the importance of studying communities across multiple years to understand the full scope of species interactions.
... Cane toads were introduced to Australia in 1935 as biocontrol for two major pests, the greyback beetle (Dermolepida albohirtum) and the Frenchi beetle (Lepidiota frenchi) (Mungomery and Buzacott 1936). Following establishment, cane toads increased geographic range, causing significant environmental impacts (Boland 2004;Greenlees et al. 2006;Letnic et al. 2008;Crossland et al. 2009;Price-Rees et al. 2010;Bleach et al. 2015). Recent genetic and morphological evaluation of cane toads has identified two species (R. marina and R. horribilis) occurring within the range historically attributed to cane toads (Acevedo et al. 2016). ...
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Context Invasive vertebrates have significant negative impacts on biodiversity and agricultural production worldwide. Increased connectivity among countries, through trade and tourism, is escalating the rate of introductions of vertebrate species, particularly herpetofauna, across international borders. In Australia, Asian black-spined toads (ABSTs; Duttaphrynus melanostictus) are one of the species most intercepted at borders. They are considered a biosecurity risk because of the potential for negative environmental impacts, similar to those caused by cane toads (Rhinella marina). Aims We aimed to compare ABSTs with cane toads to investigate potential impacts and distribution of ABSTs in the Australian context. We also aimed to identify knowledge gaps regarding ABST biology and the potential role of cane toads in an ABST invasion in Australia. Methods We undertook a literature review to obtain published data to compare the life history characteristics of ABSTs and cane toads. We also modelled climatic niche overlap and compared suitable habitat for both species in Australia. Key results Our results show ABSTs and cane toads have broadly similar reproductive life histories and feeding niches. In particular, similarities include large clutch sizes, preferred oviposition sites, and diet at tadpole and adult life stages. In Australia, the species share suitable potential habitat, particularly in North Queensland, where the majority of ABST incursions have occurred. The species differ in size, call characteristics, clutch size relative to body size, and egg development rate, although the environment also influences these traits. We identify gaps in our knowledge of ABST spatial ecology, thermal tolerances, water reliance, and habitat. Conclusions ABSTs pose a significant biosecurity threat to Australia. Similarities in life history to cane toads means they may have similar impacts, but may have a more limited distribution in Australia. Invasion of Australia by ABSTs would likely result in interactions with cane toads, but it is not possible to accurately determine the outcomes of those interactions without further investigation. Implications Addressing knowledge gaps and quantitatively determining the potential for competition between ABSTs and cane toads will assist surveillance and response planning for ABST incursions in Australia.
... (Huffaker and Kennet 1959). Conversely, notable failures include the cane toad Rhinella marina introductions into Florida (Smith 2005) and Australia (Sutherst et al. 1996;Crossland et al. 2009) as well as introductions of bigheaded carps Hypophthalmichthys spp. (Chick and Pegg 2001;Sass et al. 2014) and kudzu Pueraria spp. ...
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Proliferative Gill Disease (PGD), caused by the myxozoan Henneguya ictaluri, is an important parasitic disease in US catfish aquaculture. Continuous exposure of Channel Catfish Ictalurus punctatus to the actinospore stage of H. ictaluri results in a severe inflammatory response at the gills, leading to morbidity and death. Previous work indicates chemical cues in fish mucus recognized by myxozoan actinospores are not host‐specific. Building on these findings, the potential decoy effects of non‐ictalurid fish to actinospores of H. ictaluri were evaluated. Actinospores exposed to gill mucus from multiple non‐ictalurid fishes resulted in actinospore activation for all fish species tested. Based on these findings, experimental transmission trials with potential interceptor fish were conducted. Individual Channel Catfish were co‐stocked with Western Mosquitofish Gambusia affinis at 0, 10, 25, or 50% mean Channel Catfish biomass and exposed to 3,000 actinospores of H. ictaluri. Gill tissues were sampled 24 hours post‐challenge and parasite burden was estimated by H. ictaluri‐specific qPCR. Results revealed Mosquitofish stocked at 25 and 50% catfish biomass reduced H. ictaluri DNA in catfish gills >3‐fold. In a second study, catfish were exposed to pond water collected from an active PGD outbreak in the presence of Mosquitofish stocked at 25% catfish biomass. Channel Catfish were sampled 24 hours and seven days after the last pond water exposure. Twenty‐four hours after the last exposure, catfish co‐stocked with Mosquitofish showed significantly lower H. ictaluri DNA than catfish stocked alone. This treatment effect was absent seven days later, as parasite quantities within tissues had increased >1000X, with marked variability. Still, results indicate chemical cues that activate H. ictaluri actinospores are not specific to channel catfish. This work evinces a potential benefit of non‐ictalurid fish in combating H. ictaluri, suggesting the presence of non‐ictalurid interceptor fish in catfish ponds may minimize PGD severity.
... Secondly, anuran tadpole growth and development are often highly density-dependent (Alford, 1999). A reduction in tadpole density therefore results in fewer, but larger, metamorphs emerging from ponds (e.g., Crossland et al., 2009). This larger size can confer significant fitness advantages in terms of increased survival (Berven & Gill, 1983;Cabrera-Guzm an et al., 2013;Smith, 1987) and reproductive output (Berven, 1981;Clarke, 1974;Howard, 1978;Wilbur et al., 1978). ...
Article
Biological invasions adversely affect the survival of many native species, but long‐term consequences of the novel pressures imposed by invaders on natives are less clear. If natives can adapt to the presence of the invader, the severity of impact will decline with time. On Hokkaido, Japan, alien toads (Bufo japonicus formosus) are highly toxic to native frog tadpoles (Rana pirica) that attempt to eat their hatchlings. Therefore, the arrival of toads potentially imposes selection pressure on native frogs in the context of behavioral response (feeding aversion) and physiological resistance to toad toxins. Here, we compared the consumption tendency and toxin resistance of R. pirica from several sites with different histories of toad invasion (0 to >100 years exposure). We found no evidence of adaptive response to invasive toads. The vast majority of R. pirica tadpoles from all sites readily consumed toad hatchlings and died, regardless of time since invasion or whether hatchlings were from sympatric versus allopatric toad populations. In contrast, tadpoles of a closely related species (Rana ornativentris), which co‐occurs naturally with B. j. formosus on Honshu, readily consumed toad hatchlings without ill effect. Our results indicate that the lethal toxic effect of the alien toads on native frogs on Hokkaido is maintained over long time periods without mitigation through adaptation. Biological invasions adversely affect the survival of many native species, but long‐term consequences of the novel pressures imposed by invaders on natives are less clear. Here, we compared the consumption tendency and toxin resistance of native frog tadpoles for alien toxic toads from several sites with different histories of toad invasion in Hokkaido. We found that the lethal toxic effect of the alien toads on native frogs is maintained over long time periods without mitigation through adaptation.
... Expansion and Stability refer to the ratio of the non-native niche that does or does not overlap, respectively, to the native niche. Unfilling represents the proportion of the native niche that is present in non-native ranges yet remains unoccupied with native faunas would likely lead to an overall reduction in richness and diversity, mirroring impacts already reported, for example, in Australia (Crossland et al. 2009;Mayer et al. 2015). Failed eradication protocols and the continued spread of cane toads in the Australian continent (Tingley et al. 2017) are, thus, suggestive of the fate of native biodiversity elsewhere under the introduction of this species. ...
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Niche conservatism explains biological invasions worldwide. However, a plethora of ecological processes may lead invasive species to occupy environments that are different from those found within native ranges. Here, we assess the potential invadable areas of the world’s most pervasive invasive amphibians: the cane toad, Rhinella marina + R. horribilis, and the North American bullfrog, Lithobates catesbeianus. The uncontrolled spread of such voracious, large-bodied, and disease-tolerant anurans has been documented to impact native faunas worldwide. To disentangle their invasion-related niche dynamics, we compared the predictive ability and distributional forecasts of ecological niche models calibrated with information from native, invaded and pooled (native + invaded) ranges. We found that including occurrences from invaded ranges improved model accuracy for both studied species. Non-native occurrences also accounted for 54% and 61% increase in the total area of potential distribution of the cane toad and bullfrog, respectively. Besides, the latter species occupied locations with climatic conditions that are more extreme than those found within its native range. Our results indicate that the occupancy of environments different from those found in native ranges increases the overall potential distribution of the studied invasive anuran species. Therefore, climate information on native ranges alone is insufficient to explain and anticipate the distributional patterns of invasion of cane toads and bullfrogs, underestimating predictions of potential invadable distribution. Moreover, such an observed expansion of realized niches towards occupancy of climates not found within native ranges also has clear implications for invasion risk assessments based on climate modelling worldwide.
... Studies on interactions between Australian anurans and cane toads largely have focused on early life history stages (eggs, larvae and metamorphs). Native frog tadpoles die from eating the toxic eggs of cane toads (Crossland et al. 2008), but the consequent decrease in tadpole density may benefit the survivors, leading to a larger body size among metamorphs (Crossland, Alford & Shine 2009). Toxic cane toad tadpoles also may reduce fish predation on native frog tadpoles, because fish and frogs learn to avoid preying on tadpoles (Nelson, Crossland & Shine 2010;Nelson, Crossland & Shine 2011). ...
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Competition within and among species can play a key role in structuring the assemblages of anuran tadpoles. Previous studies have reported that tadpoles of the invasive cane toad ( Rhinella marina ) are more strongly disadvantaged by the presence of native frog tadpoles than by the same number of conspecific toad tadpoles. That effect might arise from a lack of coevolution of the invasive toad with its competitors; and/or from a generalized superiority of frog tadpoles over toad tadpoles. To clarify those possibilities, we conducted experimental trials using the larvae of a native rather than invasive toad ( Bufo japonicus formosus in Japan) exposed to larvae of native anurans (the sympatric frogs Rana japonica and Rana ornativentris and the parapatric toad Bufo japonicus japonicus ). In intraspecific competition trials, higher densities of B. j. formosus prolonged the larval period and reduced size at metamorphosis, but did not affect survival. In interspecific competition trials, the effects of the other anuran species on B. j. formosus were similar to the effects of the same number of conspecific larvae. This similarity in impact of interspecific versus intraspecific competition argues against any overall competitive superiority of frog larvae over toad larvae. Instead, the vulnerability of larval cane toads to frog tadpoles may result from a lack of coevolutionary history.
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Eggs, hatchlings, and tadpoles of bufonids are unpalatable or toxic to some aquatic predators but are readily consumed by other species without ill effect. We investigated the effects of toxic Bufo marinus on potential predators (tadpoles) which are phylogenetically related but which differ in their history of evolutionary exposure to B. marinus. Our aim was to determine whether the behavioral and/or physiological responses of tadpoles to toxic B. marinus varied depending on their history of evolutionary exposure to these toxins. Dead tadpoles of B. marinus and other species were offered as food to anuran larvae in controlled laboratory experiments in native (Brazil) and exotic (Australia) habitats of B. marinus. Tadpoles in Brazil consumed dead tadpoles of B. marinus without any apparent ill effect but avoided them when alternate food was available. In contrast, the majority of Australian tadpoles died after consuming dead tadpoles of B. marinus. The tendency of Australian tadpoles to avoid consuming larval B. marinus when alternate food was available varied widely. Some species largely avoided larval B. marinus and experienced high survival rates. Other species, however, did not avoid consuming tadpoles of B. marinus and experienced low survival rates. Differences in the responses of tadpoles in Brazil and Australia to toxic B. marinus may result from differences in their evolutionary histories of exposure to these toxins.
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