John Llewelyn

Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area

Cane toads (Bufo marinus) are now moving about 5 times faster through tropical Australia than they did a half-century ago, during the early phases of toad invasion. Radio-tracking has revealed higher daily rates of displacement by toads at the invasion front compared to those from long-colonised areas: toads from frontal populations follow straighter paths, move more often, and move further per displacement than do toads from older (long-established) populations. Are these higher movement rates of invasion-front toads associated with modified locomotor performance (e.g. speed, endurance)? In an outdoor raceway, toads collected from the invasion front had similar speeds, but threefold greater endurance, compared to conspecifics collected from a long-established population. Thus, increased daily displacement in invasion-front toads does not appear to be driven by changes in locomotor speed. Instead, increased dispersal is associated with higher endurance, suggesting that invasion-front toads tend to spend more time moving than do their less dispersive conspecifics. Whether this increased endurance is a cause or consequence of behavioural shifts associated with rapid dispersal is unclear. Nonetheless, shifts in endurance between frontal and core populations of this invasive species point to the complex panoply of traits affected by selection for increased dispersal ability on expanding population fronts.

Adaptation or preadaptation: why are keelback snakes (Tropidonophis mairii) less vulnerable to invasive cane toads (Bufo marinus) 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.

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.

Heat hardening in a tropical lizard: geographic variation explained by the predictability and variance in environmental temperatures

Over the coming decades, our planet will experience a dramatic increase in average temperatures and an increase in the variance around those temperatures leading to more frequent and harsher heat waves. These changes will impact most species and impose strong selection on physiological traits. Rapid acclimation is the most direct way for organisms to respond to such extreme events, but we currently have little understanding of how the capacity to mount such plastic responses evolves. Accordingly, there is some urgency to determine how the physiological response to high temperatures varies within species, and how this variation is driven by the environment. Here, we investigate heat-hardening capacity - a rapid physiological response that confers a survival advantage under extreme thermal stress - across 13 populations of a rain forest lizard, Lampropholis coggeri, from the tropics of north-eastern Australia. Our results reveal that heat hardening is constrained in these lizards by a hard upper thermal limit for locomotor function (approximately 43 degrees C). Further, hardening response shows strong geographic variation associated with thermal environment: lizards from more predictable and more seasonal thermal environments exhibited greater hardening compared with those from more stochastic and less seasonal habitats. This finding - that predictability in thermal variation influences hardening capacity - aligns closely with theoretical expectations. Our results suggest that tropical species may harbour adaptive variation in physiological plasticity that they can draw from in response to climate change, and this variation is spatially structured in locally adapted populations. Our results also suggest that, by using climatic data, we can predict which populations contain particular adaptive variants; information critical to assisted gene flow strategies.

Thermal regimes and diel activity patterns of four species of small elapid snakes from south-eastern Australia

Two of the most basic biological attributes for any ectothermic animal are the times of day that it is active and the body temperatures that it exhibits. Published studies on reptile biology display a heavy bias towards diurnal lizards from Northern Hemisphere habitats. To help redress this imbalance, we quantified thermal regimes and activity times in four species of small Australian elapid snakes. Mean selected body temperature in a thermal gradient was affected by the time of testing (i.e. night v. day), with snakes choosing higher body temperatures at night than by day. In outdoor enclosures, whip snakes (Demansia psammophis) were shuttling heliotherms active only during daylight hours at relatively high body temperatures; in a laboratory thermal gradient these animals selected high body temperatures (mean 31.3°C during the day and 33.2°C at night). The other three taxa – golden-crowned snakes (Cacophis squamulosus), small-eyed snakes (Cryptophis nigrescens) and marsh snakes (Hemiaspis signata) – were active mostly at night at relatively low body temperatures, and selected low body temperatures in a thermal gradient (18.1–23.4°C). Thus, mean selected body temperatures differ substantially among sympatric elapid species in south-eastern Australia and are correlated with times of activity.

Do evolutionary constraints on thermal performance manifest at different organizational scales

The two foremost hypotheses on the evolutionary constraints on an organisms thermal sensitivity – the hotter‐is‐better expectation, and the specialist–generalist trade‐off – have received mixed support from empirical studies testing for their existence. Could these conflicting results reflect confusion regarding the organizational level (i.e. species > population > individual) at which these constraints should manifest? We propose that these evolutionary constraints should manifest at different organizational levels because of differences in their underlying causes and requirements. The hotter‐is‐better expectation should only manifest across separate evolutionary units (e.g. species, populations), and not within populations. The specialist–generalist trade‐off, by contrast, should manifest within as well as between separate evolutionary units. We measured the thermal sensitivity of sprint performance for 440 rainforest sun skinks (Lampropholis coggeri) representing 10 populations, and used the resulting performance curves to test for evidence for the hypothesized constraints at two organizational levels: (i) across populations and (ii) within populations. As predicted, the hotter‐is‐better expectation was evident only at the across‐population level, whereas the specialist–generalist trade‐off was evident within, as well as across, populations. Our results suggest that, depending on the processes that drive them, evolutionary constraints can manifest at different organizational levels. Consideration of these underlying processes, and the organizational level at which a constraint should manifest, may help resolve conflicting empirical results.

Ontogenetic shifts in a prey's chemical defences influence feeding responses of a snake predator

Foraging theory suggests that predator responses to potential prey should be influenced by prey chemical defences, but the effects of ontogenetic variation in such defences on prey vulnerability to predators remain unclear. Cane toads (Rhinella marina) are toxic to anurophagous snakes, including the keelback (Tropidonophis mairii, a natricine colubrid that occurs within the toads’ invasive range in Australia). Toxin levels and diversity change through toad ontogeny, decreasing from the egg stage to metamorphosis, then increasing in postmetamorphic toads. If the toxin content of a prey item influences predator responses, we predict that keelbacks should exhibit selective predation on toads close to metamorphosis. The results of our laboratory trials on adult (field-collected, and thus toad-experienced) and hatchling (laboratory-incubated, and thus toad-naive) keelbacks supported this prediction. The snakes selectively consumed later-stage rather than earlier-stage tadpoles, and earlier-stage rather than later-stage metamorphs. Our data are thus consistent with the hypothesis that ontogenetic changes in toxin content can affect individuals’ vulnerability to predation.

Peripheral isolates as sources of adaptive diversity under climate change

As climate change progresses, there is increasing focus on the possibility of using targeted gene flow (the movement of pre-adapted individuals into declining populations) as a management tool. Targeted gene flow is a relatively cheap, low-risk management option and will almost certainly come into increased use over the coming decades. Before such action can be taken, however, we need to know where to find pre-adapted individuals. We argue that, for many species, the obvious place to look for this diversity is in peripheral isolates: isolated populations at the current edges of a species’ range. Both evolutionary and ecological considerations suggest that the bulk of a species’ adaptive variation may be contained in the total set of these peripheral isolates. Moreover, by exploring both evolutionary and ecological perspectives it becomes clear that we should be able to assess the potential value of each isolate using remotely sensed data and three measurable axes of variation in patch traits: population size, connectivity, and climatic environment. Locating the “sweet spot” in this trait space, however, remains a challenge. Throughout, we illustrate these ideas using Australia’s Wet Tropics rainforests as a model system.

Chemoreception and mating behaviour of a tropical Australian skink

In many reptile groups, molecular systematics is currently revealing high levels of cryptic diversity (i.e. genetically distinct lineages that are difficult to distinguish morphologically). One obvious mode for mate discrimination in these cryptic species is chemoreception. We hypothesise that diversity in these groups is not cryptic for pheromones, and mate recognition via chemoreception may be the primary reproductive isolating mechanism. Here, we present a preliminary study of chemoreception in Lampropholis coggeri, a rainforest skink of north-eastern Australia. We first describe the mating behaviour of captive pairs, showing that tongue-flicking is an important component for both males and females, and find that L. coggeri mate more readily when paired with a conspecific from their own population vs. from a nearby population. Based on the assumption that tongue-flicking represents the lizard’s interest, we then experimentally tested scent discrimination using lizard-swabbed cotton buds presented to captive individuals. We found both sexes tongue-flicked more to conspecific scent than to unscented controls. Males tongue-flicked more to female scent than to male scent but did not discriminate between mated and unmated females. While females showed greater interest in conspecific scent, they showed no greater interest in scent from males than females. This lack of discrimination was true for both mated and unmated females. Unexpectedly, however, mated females tongue-flicked substantially more than unmated females. Finally, males tended to tongue flick more often to female scents from their own population than to a nearby population that is moderately genetically divergent. Our results suggest that chemoreception plays a role in mate recognition in this species. Further work should extend to establishing mate recognition between the highly divergent cryptic lineages within this species and the pheromones underlying mate recognition.

Using connectivity to identify climatic drivers of local adaptation

Understanding the climatic drivers of local adaptation is vital. Such knowledge is not only of theoretical interest but is critical to inform management actions under climate change, such as assisted translocation and targeted gene flow. Unfortunately, there are a vast number of potential trait-environment combinations, and simple relationships between trait and environment are ambiguous: representing either plastic or evolved variation. Here, we show that by incorporating connectivity as an index of gene flow, we can differentiate trait-environment relationships reflecting genetic variation vs. phenotypic plasticity. In this way, we rapidly shorten the list of trait-environment combinations that are of significance. Our analysis of an existing data set on geographic variation in a tropical lizard shows that we can effectively rank climatic variables by the strength of their role in local adaptation. The promise of our method is a rapid and general approach to identifying the environmental drivers of local adaptation.