Christa Beckmann

Small within-day increases in temperature affects boldness and alters personality in coral reef fish

Consistent individual differences in behaviour, termed personality, are common in animal populations and can constrain their responses to ecological and environmental variation, such as temperature. Here, we show for the first time that normal within-daytime fluctuations in temperature of less than 3°C have large effects on personality for two species of juvenile coral reef fish in both observational and manipulative experiments. On average, individual scores on three personality traits (PTs), activity, boldness and aggressiveness, increased from 2.5- to sixfold as a function of temperature. However, whereas most individuals became more active, aggressive and bold across temperature contexts (were plastic), others did not; this changed the individual rank order across temperatures and thus altered personality. In addition, correlations between PTs were consistent across temperature contexts, e.g. fish that were active at a given temperature also tended to be both bold and aggressive. These results (i) highlight the importance of very carefully controlling for temperature when studying behavioural variation among and within individuals and (ii) suggest that individual differences in energy metabolism may contribute to animal personality, given that temperature has large direct effects on metabolic rates in ectotherms.

Widespread convergence in toxin resistance by predictable molecular evolution

Significance Convergence has strong bearing on the fundamental debate about whether evolution is stochastic and unpredictable or subject to constraints. Here we show that, in certain circumstances, evolution can be highly predictable. We demonstrate that several lineages of insects, amphibians, reptiles, and mammals have utilized the same molecular solution, via the process of convergence, to evolve resistance to toxic cardiac glycosides produced defensively by plants and bufonid toads. The repeatability of this process across the animal kingdom demonstrates that evolution can be constrained to proceed along highly predictable pathways at molecular and functional levels. Our study has important implications for conservation biology by providing a predictive framework for assessing the vulnerability of native fauna to the introduction of invasive toxic toads. The question about whether evolution is unpredictable and stochastic or intermittently constrained along predictable pathways is the subject of a fundamental debate in biology, in which understanding convergent evolution plays a central role. At the molecular level, documented examples of convergence are rare and limited to occurring within specific taxonomic groups. Here we provide evidence of constrained convergent molecular evolution across the metazoan tree of life. We show that resistance to toxic cardiac glycosides produced by plants and bufonid toads is mediated by similar molecular changes to the sodium-potassium-pump (Na+/K+-ATPase) in insects, amphibians, reptiles, and mammals. In toad-feeding reptiles, resistance is conferred by two point mutations that have evolved convergently on four occasions, whereas evidence of a molecular reversal back to the susceptible state in varanid lizards migrating to toad-free areas suggests that toxin resistance is maladaptive in the absence of selection. Importantly, resistance in all taxa is mediated by replacements of 2 of the 12 amino acids comprising the Na+/K+-ATPase H1–H2 extracellular domain that constitutes a core part of the cardiac glycoside binding site. We provide mechanistic insight into the basis of resistance by showing that these alterations perturb the interaction between the cardiac glycoside bufalin and the Na+/K+-ATPase. Thus, similar selection pressures have resulted in convergent evolution of the same molecular solution across the breadth of the animal kingdom, demonstrating how a scarcity of possible solutions to a selective challenge can lead to highly predictable evolutionary responses.

Toad’s tongue for breakfast: exploitation of a novel prey type, the invasive cane toad, by scavenging raptors in tropical Australia

Although interest in the ecological impacts of invasive species has largely focused on negative effects, some native taxa may benefit from invader arrival. In tropical Australia, invasive cane toads (Bufo marinus) have fatally poisoned many native predators (e.g., marsupials, crocodiles, lizards) that attempt to ingest the toxic anurans, but birds appear to be more resistant to toad toxins. We quantified offtake of dead (road-killed) cane toads by raptors (black kites (Milvusmigrans) and whistling kites (Haliastursphenurus)) at a site near Darwin, in the Australian wet-dry tropics. Raptors readily took dead toads, especially small ones, although native frogs were preferred to toads if available. More carcasses were removed in the dry season than the wet season, perhaps reflecting seasonal availability of alternative prey. Raptors appeared to recognize and avoid bufotoxins, and typically removed and consumed only the toads’ tongues (thereby minimizing toxin uptake). The invasion of cane toads thus constitutes a novel prey type for scavenging raptors, rather than (as is the case for many other native predators) a threat to population viability.

Impact of invasive cane toads on Australian birds.

The cane toad (Bufo marinus), a large, toxic, American anuran, was introduced to Australia in 1935. Populations of many of Australias reptiles (snakes, varanid lizards, crocodiles) and carnivorous mammals (dasyurid marsupials) have declined because these predators are killed by the toads powerful toxins. In contrast to these well-studied species, little is known about the cane toads impacts on Australian birds. We reviewed published and unpublished data on behavioral interactions between Australian avian predators and cane toads and collated distributional and dietary information to identify avian taxa potentially at risk from cane toad invasion. Cane toads are sympatric with 172 frog-eating bird species in Australia, and an additional 8 bird species overlap with the predicted future range of the toad. Although many bird species thus are potentially at risk, behavioral observations suggest the risk level is generally low. Despite occasional reports of Australian birds being killed when they ingest cane toads, most birds either ignore toads or survive the predation event. The apparently higher tolerance of Australian birds to toad toxins, compared with Australian reptiles and marsupials, may reflect genetic exchange between Australian birds and Asian populations that encounter other bufonid species regularly and hence have evolved the capacity to recognize or tolerate this toxic prey.

High atmospheric temperatures and ‘ambient incubation’ drive embryonic development and lead to earlier hatching in a passerine bird

Tropical and subtropical species typically experience relatively high atmospheric temperatures during reproduction, and are subject to climate-related challenges that are largely unexplored, relative to more extensive work conducted in temperate regions. We studied the effects of high atmospheric and nest temperatures during reproduction in the zebra finch. We characterized the temperature within nests in a subtropical population of this species in relation to atmospheric temperature. Temperatures within nests frequently exceeded the level at which embryo’s develop optimally, even in the absence of parental incubation. We experimentally manipulated internal nest temperature to demonstrate that an average difference of 6°C in the nest temperature during the laying period reduced hatching time by an average of 3% of the total incubation time, owing to ‘ambient incubation’. Given the avian constraint of laying a single egg per day, the first eggs of a clutch are subject to prolonged effects of nest temperature relative to later laid eggs, potentially increasing hatching asynchrony. While birds may ameliorate the negative effects of ambient incubation on embryonic development by varying the location and design of their nests, high atmospheric temperatures are likely to constitute an important selective force on avian reproductive behaviour and physiology in subtropical and tropical regions, particularly in the light of predicted climate change that in many areas is leading to a higher frequency of hot days during the periods when birds breed.

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.

Cancer and life-history traits: lessons from host-parasite interactions

Despite important differences between infectious diseases and cancers, tumour development (neoplasia) can nonetheless be closely compared to infectious disease because of the similarity of their effects on the body. On this basis, we predict that many of the life-history (LH) responses observed in the context of host-parasite interactions should also be relevant in the context of cancer. Parasites are thought to affect LH traits of their hosts because of strong selective pressures like direct and indirect mortality effects favouring, for example, early maturation and reproduction. Cancer can similarly also affect LH traits by imposing direct costs and/or indirectly by triggering plastic adjustments and evolutionary responses. Here, we discuss how and why a LH focus is a potentially productive but under-exploited research direction for cancer research, by focusing our attention on similarities between infectious disease and cancer with respect to their effects on LH traits and their evolution. We raise the possibility that LH adjustments can occur in response to cancer via maternal/paternal effects and that these changes can be heritable to (adaptively) modify the LH traits of their offspring. We conclude that LH adjustments can potentially influence the transgenerational persistence of inherited oncogenic mutations in populations.

Noisy neighbours at the frog pond: effects of invasive cane toads on the calling behaviour of native Australian frogs.

Invasive species can disrupt the communication systems that native biota use for reproductive interactions. In tropical Australia, invasive cane toads (Rhinella marina) breed in many of the same waterbodies that are used by native frogs, and males of both the invader and the native taxa rely on vocal signals to attract mates. We conducted playback experiments to test the hypothesis that calls of toads may influence the calling behaviour of frogs (Limnodynastes convexiusculus and Litoria rothii). Male L. convexiusculus adjusted their calling rate and the variance in inter-call interval in response to a variety of sounds, including the calls of cane toads as well as those of other native frog species, and other anthropogenic noise, whereas L. rothii did not. Within the stimulus periods of playbacks, male L. convexiusculus called more intensely during long silent gaps than during calling blocks. Thus, males of one frog species reduced their calling rate, possibly to minimise energy expenditure during periods of acoustic interference generated by cane toads. In spite of such modifications, the number of overlapping calls (within stimulus periods) did not differ significantly from that expected by chance. In natural conditions, the calls of cane toads are continuous rather than episodic, leaving fewer gaps of silence that male frogs could exploit. Future work could usefully quantify the magnitude of temporal (e.g. diel and seasonal) and spatial overlap between calling by toads and by frogs and the impact of call-structure shifts on the ability of male frogs to attract receptive females.

Hierarchical analysis of avian re-nesting behavior: mean, across-individual, and intra-individual responses

Anti-predator behavior is a key aspect of life history evolution, usually studied at the population (mean), or across-individual levels. However individuals can also differ in their intra-individual (residual) variation, but to our knowledge, this has only been studied once before in free-living animals. Here we studied the distances moved and changes in nest height and concealment between successive nesting attempts of marked pairs of grey fantails (Rhipidura albiscapa) in relation to nest fate, across the breeding season. We predicted that females (gender that decides where the nest is placed) should on average show adaptive behavioral responses to the experience of prior predation risk such that after an unsuccessful nesting attempt, replacement nests should be further away, higher from the ground, and more concealed compared with replacement nests after successful nesting attempts. We found that, on average, females moved greater distances to re-nest after unsuccessful nesting attempts (abandoned or depredated) in contrast to after a successful attempt, suggesting that re-nesting decisions are sensitive to risk. We found no consistent across-individual differences in distances moved, heights, or concealment. However, females differed by 53-fold (or more) in their intra-individual variability (i.e., predictability) with respect to distances moved and changes in nest height between nesting attempts, indicating that either some systematic variation went unexplained and/or females have inherently different predictability. Ignoring these individual differences in residual variance in our models obscured the effect of nest fate on re-nesting decisions that were evident at the mean level.

Curvilinear telomere length dynamics in a squamate reptile

The lack of consensus concerning the impact of telomere length (TL) dynamics on survival emphasizes the need for additional studies to evaluate the effect of TL on key life-history processes. Using both cross-sectional and longitudinal data, we therefore explored age-specific TL dynamics in a squamate reptile: the frillneck lizard (Chlamydosaurus kingii). Our cross-sectional analyses revealed that young lizards had short TL, TL increased in medium-aged lizards, but TL decreased in older age cohorts, revealing a curvilinear relationship between TL and frillneck lizard age. Neither our cross-sectional nor our longitudinal analyses revealed any association between TL dynamics and lizard survival. We observed a significant positive relationship between TL and telomerase expression (TE), suggesting that TE is a significant determinant of frillneck lizard TL dynamics. Importantly, our longitudinal analyses revealed a positive relationship between initial TL and telomere attrition rate within individual lizards, that is lizards with short initial telomeres were subjected to reduced telomere attrition rates compared to lizards with long initial TL. Our results strongly suggest that TL and TE dynamics in frillneck lizards is not associated with lizard survival but rather reflect an adaptation to maintain TL above a critical minimum length in order to sustain cellular homeostasis. A lay summary is available for this article.