Fatal attraction: adaptations to prey on native frogs imperil snakes after invasion of toxic toads

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.     

Something different for dinner? Responses of a native Australian predator (the keelback snake) to an invasive prey species (the cane toad)

Predictions from foraging theory suggest that the probability a native predator will incorporate a novel type of prey (such as an invasive species) into its diet depends upon the potential benefits (e.g., nutrient input) vs. costs (e.g., handling time) of ingesting it. Cane toads (Bufo marinus) were introduced to Australia in 1935 and are highly toxic to many frog-eating snakes, thus there was strong selection to delete toads from the diet of these species. What has happened, however, to the feeding responses of an Australian snake species that is able to consume toads without dying? Our field surveys in northeastern Queensland show that, despite their high tolerance to toad toxins (compared to other native snakes), keelbacks (Tropidonophis mairii) feed primarily on native frogs rather than cane toads. This pattern occurs because the snakes show active prey preferences; even under standardized conditions in the laboratory, snakes are more likely to consume frogs than toads. When they are force-fed, snakes frequently regurgitate toads but not frogs. Thus, despite the high availability of the abundant toads, these invasive anurans are largely avoided as prey. This probably occurs because consumption of toads, although not lethal to keelbacks, causes significant sublethal effects and confers little nutritional benefit. Hence, keelback populations are not threatened by toad invasion, but neither do the snakes benefit substantially from the availability of a new type of potential prey.     

Better the devil you know: avian predators find variation in prey toxicity aversive

Toxic prey that signal their defences to predators using conspicuous warning signals are called ‘aposematic’. Predators learn about the toxic content of aposematic prey and reduce their attacks on them. However, through regulating their toxin intake, predators will include aposematic prey in their diets when the benefits of gaining the nutrients they contain outweigh the costs of ingesting the prey''s toxins. Predators face a problem when managing their toxin intake: prey sharing the same warning signal often vary in their toxicities. Given that predators should avoid uncertainty when managing their toxin intake, we tested whether European starlings (Sturnus vulgaris) preferred to eat fixed-defence prey (where all prey contained a 2% quinine solution) to mixed-defence prey (where half the prey contained a 4% quinine solution and the other half contained only water). Our results support the idea that predators should be more ‘risk-averse’ when foraging on variably defended prey and suggest that variation in toxicity levels could be a form of defence.     

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.     

Does intraspecific niche partitioning in a native predator influence its response to an invasion by a toxic prey species?

Abstract The introduced and highly toxic cane toad (Bufo marinus) is rapidly spreading across northern Australia where it may affect populations of large terrestrial vertebrate predators. The ecological impact of cane toads will depend upon the diets, foraging modes and habitat use of native predators, and their feeding responses to cane toads. However, intraspecific niche partitioning may influence the degree of vulnerability of predators to toxic prey, as well as the time course of the impact of alien invaders on native species. We studied the diet of the northern death adder Acanthophis praelongus and their feeding responses to cane toads. In the laboratory, death adders from all size classes and sexes readily consumed frogs and cane toads. Diets of free ranging A. praelongus from the Adelaide River floodplain were more heterogeneous. Juvenile snakes ate mainly frogs (39% of prey items) and small scincid lizards (43%). Both sexes displayed an ontogenetic dietary shift from lizards to mammals, but adult males fed on frogs (49%) and mammals (39%) whereas adult females (which grew larger than males) fed mainly on mammals (91%) and occasionally, frogs (9%). Feeding rates and body condition of adult snakes varied temporally and tracked fluctuations in prey availability. These results suggest that cane toads may negatively affect populations of northern death adders in the Darwin region. However, we predict that different size and sex classes of A. praelongus will experience differential mortality rates over different timescales. The initial invasion of large toads may affect adult males, but juveniles may be unaffected until juvenile toads appear the following year, and major affects on adult female death adders may be delayed until annual rainfall fluctuations reduce the availability of alternative (rodent) prey.     

Exploiting intraspecific competitive mechanisms to control invasive cane toads (Rhinella marina)

If invasive species use chemical weapons to suppress the viability of conspecifics, we may be able to exploit those species-specific chemical cues for selective control of the invader. Cane toads (Rhinella marina) are spreading through tropical Australia, with negative effects on native species. The tadpoles of cane toads eliminate intraspecific competitors by locating and consuming newly laid eggs. Our laboratory trials show that tadpoles find those eggs by searching for the powerful bufadienolide toxins (especially, bufogenins) that toads use to deter predators. Using those toxins as bait, funnel-traps placed in natural waterbodies achieved near-complete eradication of cane toad tadpoles with minimal collateral damage (because most native (non-target) species are repelled by the toads' toxins). More generally, communication systems that have evolved for intraspecific conflict provide novel opportunities for invasive-species control.     

Reproductive state affects reliance on public information in sticklebacks

The degree to which animals use public and private sources of information has important implications for research in both evolutionary ecology and cultural evolution. While researchers are increasingly interested in the factors that lead individuals to vary in the manner in which they use different sources of information, to date little is known about how an animal''s reproductive state might affect its reliance on social learning. Here, we provide experimental evidence that in foraging ninespine sticklebacks (Pungitius pungitius), gravid females increase their reliance on public information generated by feeding demonstrators in choosing the richer of two prey patches than non-reproductive fish, while, in contrast, reproductive males stop using public information. Subsequent experiments revealed reproductive males to be more efficient asocial foragers, less risk-averse and generally less social than both reproductive females and non-reproductives. These findings are suggestive of adaptive switches in reliance on social and asocial sources of information with reproductive condition, and we discuss the differing costs of reproduction and the proximate mechanisms that may underlie these differences in information use. Our findings have important implications for our understanding of adaptive foraging strategies in animals and for understanding the way information diffuses through populations.     

Alternative mating tactics in the yellow dung fly: resolving mechanisms of small-male advantage off pasture

Recent work suggests that the yellow dung fly mating system may include alternative patroller–competitor mating tactics in which large males compete for gravid females on dung, whereas small, non-competitive males search for females at foraging sites. Small males obtain most matings off pasture, yet the behavioural mechanism(s) giving rise to this pattern are unknown. We investigated the male and female behaviours that determine mating success in this environment by conducting field mating experiments and found small males to benefit from several attributes specific to the off-pasture mating environment. First, small males from foraging sites exhibited higher mating propensity, indicating that large males away from dung may be depleted of energy and/or sperm. Second, small males were more discriminating, being significantly less likely to attempt with non-gravid females, which are absent on dung but common off pasture. Third, non-gravid females were generally more likely to actively struggle and reject mating attempts; however, such behaviours occurred disproportionately more often with large males. Female Scathophaga stercoraria thus appear to preferentially mate with small males when off pasture. These findings challenge assumptions about male–female interactions in systems with alternative mating tactics and reveal hidden processes that may influence selection patterns in the field.     

Behavioural responses of an Australian colubrid snake (<Emphasis Type="Italic">Dendrelaphis punctulatus</Emphasis>) to a novel toxic prey item (the Cane Toad <Emphasis Type="Italic">Rhinella marina</Emphasis>)

The invasion of a toxic prey type can differentially affect closely related predator species. In Australia, the invasive Cane Toad (Rhinella marina) kills native anurophagous predators that cannot tolerate the toad’s toxins; but predators that are physiologically resistant (i.e., belong to lineages that entered Australia recently from Asia, where toads of other species are common) have been more resilient. In the current study, we examine the case of an Asian-derived predator lineage that relies on behavioural not physiological adaptations to deal with toads. Despite their Asian origins, Common Tree Snakes (Dendrelaphis punctulatus) are highly sensitive to toad toxins; yet this snake has not declined in abundance due to toads. We exposed captive (field-collected) snakes to toads of different sizes and ontogenetic stages, to quantify feeding responses and outcomes. Tree Snakes were less likely to attack toads than to attack native frogs, and rarely retained their hold on large toads. Tree Snakes ingested frogs of a wide range of body sizes but only ingested very small toads (<?1 g vs. up to 30 g for frogs). Behavioural responses were virtually identical between Tree Snakes from invaded versus yet-to-be-invaded areas, suggesting that preadaptation (from Asia) rather than adaptation (within Australia) is the key to successful utilisation of this novel but potentially toxic prey resource. Nonetheless, a previously-documented shift in relative head sizes of Tree Snakes coincident with toad invasion suggests that the ancestral behavioural tactic may have been reinforced by a recent morphological shift that further reduces maximal prey size, and hence the risk of fatal poisoning.     

Increased predation of nutrient-enriched aposematic prey

Avian predators readily learn to associate the warning coloration of aposematic prey with the toxic effects of ingesting them, but they do not necessarily exclude aposematic prey from their diets. By eating aposematic prey ‘educated’ predators are thought to be trading-off the benefits of gaining nutrients with the costs of eating toxins. However, while we know that the toxin content of aposematic prey affects the foraging decisions made by avian predators, the extent to which the nutritional content of toxic prey affects predators'' decisions to eat them remains to be tested. Here, we show that European starlings (Sturnus vulgaris) increase their intake of a toxic prey type when the nutritional content is artificially increased, and decrease their intake when nutritional enrichment is ceased. This clearly demonstrates that birds can detect the nutritional content of toxic prey by post-ingestive feedback, and use this information in their foraging decisions, raising new perspectives on the evolution of prey defences. Nutritional differences between individuals could result in equally toxic prey being unequally predated, and might explain why some species undergo ontogenetic shifts in defence strategies. Furthermore, the nutritional value of prey will likely have a significant impact on the evolutionary dynamics of mimicry systems.     

Horseshoe bats make adaptive prey-selection decisions, informed by echo cues

Foragers base their prey-selection decisions on the information acquired by the sensory systems. In bats that use echolocation to find prey in darkness, it is not clear whether the specialized diet, as sometimes found by faecal analysis, is a result of active decision-making or rather of biased sensory information. Here, we tested whether greater horseshoe bats decide economically when to attack a particular prey item and when not. This species is known to recognize different insects based on their wing-beat pattern imprinted in the echoes. We built a simulation of the natural foraging process in the laboratory, where the bats scanned for prey from a perch and, upon reaching the decision to attack, intercepted the prey in flight. To fully control echo information available to the bats and assure its unambiguity, we implemented computer-controlled propellers that produced echoes resembling those from natural insects of differing profitability. The bats monitored prey arrivals to sample the supply of prey categories in the environment and to inform foraging decisions. The bats adjusted selectivity for the more profitable prey to its inter-arrival intervals as predicted by foraging theory (an economic strategy known to benefit fitness). Moreover, unlike in previously studied vertebrates, foraging performance of horseshoe bats was not limited by costly rejections of the profitable prey. This calls for further research into the evolutionary selection pressures that sharpened the species's decision-making capacity.     

The bright incubate at night: sexual dichromatism and adaptive incubation division in an open-nesting shorebird

Ornamentation of parents poses a high risk for offspring because it reduces cryptic nest defence. Over a century ago, Wallace proposed that sexual dichromatism enhances crypsis of open-nesting females although subsequent studies found that dichromatism per se is not necessarily adaptive. We tested whether reduced female ornamentation in a sexually dichromatic species reduces the risk of clutch depredation and leads to adaptive parental roles in the red-capped plover Charadrius ruficapillus, a species with biparental incubation. Males had significantly brighter and redder head coloration than females. During daytime, when visually foraging predators are active, colour-matched model males incurred a higher risk of clutch depredation than females, whereas at night there was no difference in depredation risk between sexes. In turn, red-capped plovers maintained a strongly diurnal/nocturnal division of parental care during incubation, with males attending the nest largely at night when visual predators were inactive and females incubating during the day. We found support for Wallace''s conclusion that reduced female ornamentation provides a selective advantage when reproductive success is threatened by visually foraging predators. We conclude that predators may alter their prey''s parental care patterns and therefore may affect parental cooperation during care.     

An ambusher's arsenal: chemical crypsis in the puff adder (Bitis arietans)

Ambush foragers use a hunting strategy that places them at risk of predation by both visual and olfaction-oriented predators. Resulting selective pressures have driven the evolution of impressive visual crypsis in many ambushing species, and may have led to the development of chemical crypsis. However, unlike for visual crypsis, few studies have attempted to demonstrate chemical crypsis. Field observations of puff adders (Bitis arietans) going undetected by several scent-orientated predator and prey species led us to investigate chemical crypsis in this ambushing species. We trained dogs (Canis familiaris) and meerkats (Suricata suricatta) to test whether a canid and a herpestid predator could detect B. arietans using olfaction. We also tested for chemical crypsis in five species of active foraging snakes, predicted to be easily detectable. Dogs and meerkats unambiguously indicated active foraging species, but failed to correctly indicate puff adder, confirming that B. arietans employs chemical crypsis. This is the first demonstration of chemical crypsis anti-predatory behaviour, though the phenomenon may be widespread among ambushers, especially those that experience high mortality rates owing to predation. Our study provides additional evidence for the existence of an ongoing chemically mediated arms race between predator and prey species.     

Drosophila male sex peptide inhibits siesta sleep and promotes locomotor activity in the post-mated female

Quiescence, or a sleep-like state, is a common and important feature of the daily lives of animals from both invertebrate and vertebrate taxa, suggesting that sleep appeared early in animal evolution. Recently, Drosophila melanogaster has been shown to be a relevant and powerful model for the genetic analysis of sleep behaviour. The sleep architecture of D. melanogaster is sexually dimorphic, with females sleeping much less than males during day-time, presumably because reproductive success requires greater foraging activity by the female as well as the search for egg-laying sites. However, this loss of sleep and increase in locomotor activity will heighten the risk for the female from environmental and predator hazards. In this study, we show that virgin females can minimize this risk by behaving like males, with an extended afternoon ‘siesta’. Copulation results in the female losing 70 per cent of day-time sleep and becoming more active. This behaviour lasts for at least 8 days after copulation and is abolished if the mating males lack sex peptide (SP), normally present in the seminal fluid. Our results suggest that SP is the molecular switch that promotes wakefulness in the post-mated female, a change of behaviour compatible with increased foraging and egg-laying activity. The stress resulting from SP-dependent sleep deprivation might be an important contribution to the toxic side-effects of male accessory gland products that are known to reduce lifespan in post-mated females.     

An island-wide predator manipulation reveals immediate and long-lasting matching of risk by prey

Anti-predator behaviour affects prey population dynamics, mediates cascading effects in food webs and influences the likelihood of rapid extinctions. Predator manipulations in natural settings provide a rare opportunity to understand how prey anti-predator behaviour is affected by large-scale changes in predators. Here, we couple a long-term, island-wide manipulation of an important rodent predator, the island fox (Urocyon littoralis), with nearly 6 years of measurements on foraging by deer mice (Peromyscus maniculatus) to provide unequivocal evidence that prey closely match their foraging behaviour to the number of fox predators present on the island. Peromyscus maniculatus foraging among exposed and sheltered microhabitats (a measure of aversion to predation risk) closely tracked fox density, but the nature of this effect depended upon nightly environmental conditions known to affect rodent susceptibility to predators. These effects could not be explained by changes in density of deer mice over time. Our work reveals that prey in natural settings are cognizant of the dynamic nature of their predators over timescales that span many years, and that predator removals spanning many generations of prey do not result in a loss of anti-predator behaviour.     

Toxin constraint explains diet choice,survival and population dynamics in a molluscivore shorebird

Recent insights suggest that predators should include (mildly) toxic prey when non-toxic food is scarce. However, the assumption that toxic prey is energetically as profitable as non-toxic prey misses the possibility that non-toxic prey have other ways to avoid being eaten, such as the formation of an indigestible armature. In that case, predators face a trade-off between avoiding toxins and minimizing indigestible ballast intake. Here, we report on the trophic interactions between a shorebird (red knot, Calidris canutus canutus) and its two main bivalve prey, one being mildly toxic but easily digestible, and the other being non-toxic but harder to digest. A novel toxin-based optimal diet model is developed and tested against an existing one that ignores toxin constraints on the basis of data on prey abundance, diet choice, local survival and numbers of red knots at Banc d''Arguin (Mauritania) over 8 years. Observed diet and annual survival rates closely fit the predictions of the toxin-based model, with survival and population size being highest in years when the non-toxic prey is abundant. In the 6 of 8 years when the non-toxic prey is not abundant enough to satisfy the energy requirements, red knots must rely on the toxic alternative.     

Activity and shelter use of an intertidal snail: effects of sex, reproductive condition and tidal cycle

Although activity patterns are an important component of the ecology of animals as they search for food, mates and appropriate habitats, substantial variation can be observed even within a single population. The source of this variation is the combination of intrinsic and extrinsic factors acting at an individual level. We documented the activity patterns of the ovoviviparous intertidal gastropod Littorina saxatilis (Olivi) over a series of tidal cycles to assess how differences in movements of individuals with different reproductive attributes (non-gravid females, gravid females and males) might explain intra-population variability in activity. Four behaviors were measured for four consecutive tidal cycles for each of 3 months: the magnitude, frequency, and orientation of movements, and the use of shelters (i.e., crevices). In addition, we correlated movements with variations in several environmental factors (temperature, wind, humidity) during low tide to investigate the possible risk sensitivity of the different reproductive groups. All groups were more active and moved greater distances during high tide. Females, especially gravid females, appeared to be more risk-sensitive as they moved shorter distances and used shelters more often. Gravid females were also the only group with a negative relationship between air temperature and movement during low tide. We interpret these behaviors as a means to increase the probability of survival of the brooded offspring carried by the female. Males were the only group to consistently have directionality in their movements and showed evidence of an “up-down” behavior for remaining in a restricted zone. Reproductive attributes appear to be able to explain part of the intra-population variability in foraging activity in natural populations and should be taken into account in the design and interpretation of behavioral and ecological studies.     

Sublethal costs associated with the consumption of toxic prey by snakes

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.     

Adaptation or preadaptation: why are keelback snakes (<Emphasis Type="Italic">Tropidonophis mairii</Emphasis>) less vulnerable to invasive cane toads (<Emphasis Type="Italic">Bufo marinus</Emphasis>) than are other Australian snakes?

Biological invasions can expose native predators to novel prey which may be less nutritious or detrimental to predators. The introduction and subsequent spread of cane toads (Bufo marinus) through Australia has killed many anuran-eating snakes unable to survive the toad’s toxins. However, one native species, the keelback snake (Tropidonophis mairii), is relatively resistant to toad toxins and remains common in toad-infested areas. Is the keelback’s ability to coexist with toads a function of its ancestral Asian origins, or a consequence of rapid adaptation since cane toads arrived in Australia? And does the snake’s feeding preference for frogs rather than toads reflect an innate or learned behaviour? We compared keelback populations long sympatric with toads with a population that has encountered toads only recently. Unlike toad-vulnerable snake species, sympatry with toads has not affected keelback toxin tolerances or feeding responses: T. mairii from toad-sympatric and toad-naïve populations show a similar sensitivity to toad toxin, and a similar innate preference for frogs rather than toads. Feeding responses of neonatal keelbacks demonstrate that learning plays little or no role in the snake’s aversion to toads. Thus, behavioural aversion to B. marinus as prey, and physiological tolerance to toad toxins are pre-existing innate characteristics of Australian keelbacks rather than adaptations to the cane toad’s invasion of Australia. Such traits were most likely inherited from ancestral keelbacks that adapted to the presence of bufonids in Asia. Our results suggest that the impact of invasive species on native taxa may be strongly influenced by the biogeographic histories of the species involved.     

The straight and narrow path: the evolution of straight-line dispersal at a cane toad invasion front

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.