Michael R. Crossland

An assessment of the introduced mosquitofish (Gambusia affinis holbrooki) as a predator of eggs, hatchlings and tadpoles of native and non-native anurans

The introduced mosquitofish (Gambusia affinis holbrooki) is a pest species in Australia and has been implicated in the decline of populations of native fishes and anurans. However, few quantitative data exist regarding interactions between Gambusia and native aquatic fauna. We used replicated laboratory experiments to investigate predation by G. a. holbrooki on eggs, hatchlings and tadpoles of native (Limnodynastes ornatus) and non-native (Bufo marinus) anurans. Our aims were to determine (1) whether the susceptibility of anurans to predation by G. a. holbrooki changes during larval development, and (2) the potential for G. a. holbrooki as a predator of the introduced toad B. marinus. Gambusia were significant predators of all aquatic life-history stages of L. ornatus, but were significant predators of B. marinus only at the hatchling stage. When offered both species simultaneously, Gambusia consumed tadpoles of L. ornatus but avoided those of B. marinus. The differences between the responses of Gambusia to L. ornatus and B. marinus are probably due to differences in palatability and toxicity of eggs, hatchlings and tadpoles of these species. The results indicate that G. a. holbrooki is unlikely to significantly affect larval populations of B. marinus via predation. However, Gambusia has the potential to significantly affect larval populations of L. ornatus in natural water bodies where these species co-occur.

Larger Body Size at Metamorphosis Enhances Survival, Growth and Performance of Young Cane Toads (Rhinella marina)

Body size at metamorphosis is a key trait in species (such as many anurans) with biphasic life-histories. Experimental studies have shown that metamorph size is highly plastic, depending upon larval density and environmental conditions (e.g. temperature, food supply, water quality, chemical cues from conspecifics, predators and competitors). To test the hypothesis that this developmental plasticity is adaptive, or to determine if inducing plasticity can be used to control an invasive species, we need to know whether or not a metamorphosing anuran’s body size influences its subsequent viability. For logistical reasons, there are few data on this topic under field conditions. We studied cane toads (Rhinella marina) within their invasive Australian range. Metamorph body size is highly plastic in this species, and our laboratory studies showed that larger metamorphs had better locomotor performance (both on land and in the water), and were more adept at catching and consuming prey. In mark-recapture trials in outdoor enclosures, larger body size enhanced metamorph survival and growth rate under some seasonal conditions. Larger metamorphs maintained their size advantage over smaller siblings for at least a month. Our data support the critical but rarely-tested assumption that all else being equal, larger body size at metamorphosis is likely to enhance an individual’s long term viability. Thus, manipulations to reduce body size at metamorphosis in cane toads may help to reduce the ecological impact of this invasive species.

Indirect ecological impacts of an invasive toad on predator-prey interactions among native species

One of the many ways that invasive species can affect native ecosystems is by modifying the behavioural and ecological interactions among native species. For example, the arrival of the highly toxic cane toad (Bufo marinus) in tropical Australia has induced toad-aversion in some native predators. Has that shift also affected the predators’ responses to native prey—for example, by reducing vulnerability of native tadpoles via a mimicry effect, or increasing vulnerability of other prey types (such as insects) via a shift in predator feeding tactics? We exposed a native predator (northern trout gudgeon, Mogurnda mogurnda) to toad tadpoles in the laboratory, and measured effects of that exposure on the fish’s subsequent intake of native tadpoles and crickets. As predicted, toad-exposed fishes reduced their rate of predation on (palatable) tadpoles of native frogs (Litoria caerulea and L. nasuta). If alternative prey (crickets) were available also, the toad-exposed fishes shifted even more strongly away from predation on native tadpoles. Thus, invasion of a toxic species can provide a mimicry benefit to native taxa that resemble the invader, and can shift predation pressure onto other taxa.

The myth of the toad‐eating frog

Abstract In 2005, news media widely reported the discovery that a native Australian frog species, Litoria dahlii, could consume the normally toxic tadpoles of invasive cane toads (Bufo marinus) without ill effects, and might therefore be helpful in controlling these troublesome pests. Our experimental studies show that, contrary to the story, L dahlii is just as vulnerable to toad toxins as are other native frog species. So, why did the story spread so widely, and what does this tell us about the power of myth in public debates about conservation issues?

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

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.

Sublethal effects of fluctuating hypoxia on juvenile tropical Australian freshwater fish

Hypoxia in freshwater ecosystems of the Australian wet tropics occurs naturally, but is increasing as a result of anthropogenic influences. Diel cycling of dissolved oxygen (DO) concentration (fluctuating hypoxia) is common in the region. Laboratory experiments sought to identify relationships between severity of fluctuating hypoxia and sublethal effects on ventilation, feeding and growth for juvenile barramundi (Lates calcarifer), eastern rainbowfish (Melanotaenia splendida splendida) and sooty grunter (Hephaestus fuliginosus). Fish continued to feed and grow under daily exposure to severe fluctuating hypoxia treatments for several weeks. Ventilation rates increased in a significant direct quadratic relationship with the severity of hypoxia treatments and increasing hypoxia caused ventilatory behaviour changes in all species. Barramundi and rainbowfish attempted aquatic surface respiration and were more tolerant of severe hypoxia than was sooty grunter; barramundi and rainbowfish are also more likely to experience hypoxia in the wild. There was a significant quadratic relationship between growth and minimum DO saturation for barramundi. Although all three species were tolerant of hypoxia, anthropogenic stressors on tropical Australian aquatic ecosystems may increase the frequency and severity of hypoxic conditions causing a concomitant increase in fish kill events.

Predation on invasive cane toads (Rhinella marina) by native Australian rodents

The success of an invasive species can be reduced by biotic resistance from the native fauna. For example, an invader that is eaten by native predators is less likely to thrive than one that is invulnerable. The ability of invasive cane toads (Rhinella marina) to spread through Australia has been attributed to the toad’s potent defensive chemicals that can be fatal if ingested by native snakes, lizards, marsupials and crocodiles. However, several taxa of native insects and birds are resistant to cane toad toxins. If native rodents are also capable of eating toads (as suggested by anecdotal reports), these large, abundant and voracious predators might reduce toad numbers. Our field observations and laboratory trials confirm that native rodents (Melomys burtoni, Rattus colletti and Rattus tunneyi) readily kill and consume cane toads (especially small toads), and are not overtly affected by toad toxins. Captive rodents did not decrease their consumption of toads over successive trials, and ate toads even when alternative food types were available. In combination with anecdotal reports, our data suggest that rodents (both native and invasive) are predators of cane toads in Australia. Despite concerns about the decline of rodents following the invasion of toads, our data suggest that the species we studied are not threatened by toads as toxic prey, and no specific conservation actions are required to ensure their persistence.

Responses of Australian wading birds to a novel toxic prey type, the invasive cane toad Rhinella marina

The impact of invasive predators on native prey has attracted considerable scientific attention, whereas the reverse situation (invasive species being eaten by native predators) has been less frequently studied. Such interactions might affect invasion success; an invader that is readily consumed by native species may be less likely to flourish in its new range than one that is ignored by those taxa. Invasive cane toads (Rhinella marina) in Australia have fatally poisoned many native predators (e.g., marsupials, crocodiles, lizards) that attempt to ingest the toxic anurans, but birds are more resistant to toad toxins. We quantified prey preferences of four species of wading birds (Nankeen night heron, purple swamphen, pied heron, little egret) in the wild, by offering cane toads and alternative native prey items (total of 279 trays offered, 14 different combinations of prey types). All bird species tested preferred the native prey, avoiding both tadpole and metamorph cane toads. Avoidance of toads was strong enough to reduce foraging on native prey presented in combination with the toads, suggesting that the presence of cane toads could affect predator foraging tactics, and reduce the intensity of predation on native prey species found in association with toads.

Differences in developmental strategies between long-settled and invasion-front populations of the cane toad in Australia.

Phenotypic plasticity can enhance a species’ ability to persist in a new and stressful environment, so that reaction norms are expected to evolve as organisms encounter novel environments. Biological invasions provide a robust system to investigate such changes. We measured the rates of early growth and development in tadpoles of invasive cane toads (Rhinella marina) in Australia, from a range of locations and at different larval densities. Populations in long‐colonized areas have had the opportunity to adapt to local conditions, whereas at the expanding range edge, the invader is likely to encounter challenges that are both novel and unpredictable. We thus expected invasion‐vanguard populations to exhibit less phenotypic plasticity than range‐core populations. Compared to clutches from long‐colonized areas, clutches from the invasion front were indeed less plastic (i.e. rates of larval growth and development were less sensitive to density). In contrast, those rates were highly variable in clutches from the invasion front, even among siblings from the same clutch under standard conditions. Clutches with highly variable rates of growth and development under constant conditions had lower phenotypic plasticity, suggesting a trade‐off between these two strategies. Although these results reveal a strong pattern, further investigation is needed to determine whether these different developmental strategies are adaptive (i.e. adaptive phenotypic plasticity vs. bet‐hedging) or instead are driven by geographic variation in genetic quality or parental effects.

The enduring toxicity of road-killed cane toads (Rhinella marina)

The primary ecological impact of invasive cane toads (Rhinella marina) in Australia is mediated by their powerful toxins, which are fatal to many native species. Toads use roads as invasion corridors and feeding sites, resulting in frequent road-kills. The flattened, desiccated toad carcasses remain highly toxic despite being heated daily to >40°C for many months during the tropical dry-season. In controlled laboratory experiments, native tadpoles (Cyclorana australis, Litoria rothii), fishes (Mogurnda mogurnda) and leeches (Family Erpobdellidae) died rapidly when we added fragments of sun-dried toad to their water, even if the native animals had no physical access to the carcass. Given the opportunity, native tadpoles and fishes strongly avoided the vicinity of dried toad fragments. Hence, long-dead toads may contaminate roadside ponds formed by early wet-season rains and induce avoidance and/or mortality of native anuran larvae, fishes and invertebrates. Our studies show that the toxicity of this invasive species does not end with the toad’s death, and that methods for disposing of toad carcasses (e.g., after culling operations) need to recognize the persistent danger posed by those carcasses.