Climate change-induced shifts in survival and size of the worlds' northernmost oviparous snake: A 68-year study.

Because of their dependence on ambient temperature ectothermic animals can serve as sentinels of conservation problems related to global warming. Reptiles in temperate areas are especially well suited to study such effects, as their annual and daily activity patterns directly depend on ambient temperature. This study is based on annual data spanning 68 years from a fringe population of Grass Snakes (Natrix natrix), which is the world's northernmost oviparous (egg-laying) reptile, and known to be constrained by temperature for reproduction, morphology, and behavior. Mark-recapture analyses showed that survival probability was generally higher in males than in females, and that it increased with body length. Body condition (scaled mass index) and body length increased over time, indicative of a longer annual activity period. Monthly survival was generally higher during winter (i.e., hibernation) than over the summer season. Summer survival increased over time, whilst winter survival decreased, especially during recent decades. Winter survival was lower when annual maximum snow depth was less than 15 cm, implying a negative effect of milder winters with less insulating snow cover. Our study demonstrates long-term shifts in body length, body condition and seasonal survival associated with a warming climate. Although the seasonal changes in survival ran in opposite directions and though changes were small in absolute terms, the trends did not cancel out, but total annual survival decreased. We conclude that effects of a warming climate can be diverse and pose a threat for thermophilic species in temperate regions, and that future studies should consider survival change by season, preferably in a long-term approach.

Manipulation of habitat isolation and area implicates deterministic factors and limited neutrality in community assembly.

Theory predicts deterministic and stochastic factors will contribute to community assembly in different ways: Environmental filters should regulate those species that establish in a particular area resulting in the ecological requirements of species being the primary driver of species distributions, while chance and dispersal limitation should dictate the likelihood of species reaching certain areas with the ecology of species being largely neutral. These factors are specifically relevant for understanding how the area and isolation of different habitats or islands interact to affect community composition. Our review of the literature found few experimental studies have examined the interactive effect of habitat area and isolation on community assembly, and the results of those experiments have been mixed. We manipulated the area and isolation of rock "islands" created de novo in a grassland matrix to experimentally test how deterministic and stochastic factors shape colonizing animal communities. Over 64 weeks, the experiment revealed the primacy of deterministic factors in community assembly, with habitat islands of the same size exhibiting remarkable consistency in community composition and diversity, irrespective of isolation. Nevertheless, tangible differences still existed in abundance inequality among taxa: Large, near islands had consistently higher numbers of common taxa compared to all other island types. Dispersal limitation is often assumed to be negligible at small spatial scales, but our data shows this not to be the case. Furthermore, the dispersal limitation of a subset of species has potentially complex flow-on effects for dictating the type of deterministic factors affecting other colonizing species.

Many Paths to a Common Destination: Morphological Differentiation of a Functionally Convergent Visual Signal.

Understanding the interacting outcomes of selection and historical contingency in shaping adaptive evolution remains a challenge in evolutionary biology. While selection can produce convergent outcomes when species occupy similar environments, the unique history of each species can also influence evolutionary trajectories and result in different phenotypic end points. The question is to what extent historical contingency places species on different adaptive pathways and, in turn, the extent to which we can predict evolutionary outcomes. Among lizards there are several distantly related genera that have independently evolved an elaborate extendible dewlap for territorial communication. We conducted a detailed morphological study and employed new phylogenetic comparative methods to investigate the evolution of the underlying hyoid that powers the extension of the dewlap. This analysis showed that there appear to have been multiple phenotypic pathways for evolving a functionally convergent dewlap. The biomechanical complexity that underlies this morphological structure implies that adaptation should have been constrained to a narrow phenotypic pathway. However, multiple adaptive solutions have been possible in apparent response to a common selection pressure. Thus, the phenotypic outcome that subsequently evolved in different genera seems to have been contingent on the history of the group in question. This blurs the distinction between convergent and historically contingent adaptation and suggests that adaptive phenotypic diversity can evolve without the need for divergent natural selection.

Patterns of Batrachochytrium dendrobatidis transmission between tadpoles in a high-elevation rainforest stream in tropical Australia.

The highly virulent fungal pathogen Batrachochytrium dendrobatidis (Bd) poses a global threat to amphibian biodiversity. Streams and other water bodies are central habitats in the ecology of the disease, particularly in rainforests where they may transport and transmit the pathogen and harbor infected tadpoles that serve as reservoir hosts. We conducted an experiment using larval green-eyed tree frogs Litoria serrata in semi-natural streamside channels to test the hypotheses that (1) the fungus can be transmitted downstream in stream habitats and (2) infection affects tadpole growth and mouthpart loss. Our results showed that transmission can occur downstream in flowing water with no contact between individuals, that newly infected tadpoles suffered increased mouthpart loss in comparison with controls that were never infected and that infected tadpoles grew at reduced rates. Although recently infected tadpoles showed substantial loss of mouthparts, individuals with longstanding infections did not, suggesting that mouthparts may re-grow following initial loss. Our study suggests that any management efforts that can reduce the prevalence of infections in tadpoles may be particularly effective if applied in headwater areas, as their effects are likely to be felt downstream.

Determinants of anti-predator tactics in hatchling grass snakes (Natrix natrix).

Many organisms exhibit diverse anti-predator tactics, influenced by genetics and prior experience. In ectothermic taxa, offspring phenotypes are often sensitive to developmental temperatures. If the effectiveness of alternative anti-predator responses depends on thermally sensitive traits, then the temperatures experienced during embryonic life should also affect how offspring respond to an approaching predator. We incubated 16 clutches of Swedish grass snakes (Natrix natrix) at a range of developmental temperatures, and scored body size, colour pattern, locomotor performance and anti-predator responses of 213 hatchlings from those clutches. A hatchling snake's size and locomotor abilities were affected by its clutch of origin, its developmental temperature, and by an interaction between these two factors. Anti-predator tactics were strongly linked to locomotor ability, such that slower snakes tended to rely upon aggressive displays rather than flight. Incubation temperatures that generated slow (and thus aggressive) snakes also modified the colour of the snake's nuchal spot. Temperatures in the low to medium range generated mostly cream, white and orange spots, whereas medium to high temperatures generated more yellow spots. Incubation effects, and gene X environment interactions, thus may generate complex correlations between morphology, locomotor ability, and anti-predator tactics.

Pheromone-induced life-history shifts A novel approach to controlling invasive toads.

In a recent paper,1 we showed that recurrent exposure to alarm pheromones reduced development time and size at metamorphosis in larval cane toads (Bufo marinus). Subsequent measurements of post-metamorphic toads revealed larger parotoid glands relative to body size and increased amounts of bufalin (a toxic bufodienalide) in animals from the experimental treatment, suggesting increased investment in chemical defenses. These findings are of interest for evolutionary theory. But the study was also part of a larger conservation-based research program of which this pheromone work was an important component in the development of a management strategy for reducing the ecological impact of invasive cane toads in Australia. For example, our study1 aimed to quantify biochemical and life-history effects as well as assess the likely longterm impact of pheromone exposure on toads. In this addendum, I discuss the conservation potential of our research, with emphasis on exploiting alarm pheromones to induce viability reducing life-history shifts.

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.

Association of coloration mode with population declines and endangerment in Australian frogs.

Successful protection of biodiversity requires increased understanding of the ecological characteristics that predispose some species to endangerment. Theory posits that species with polymorphic or variable coloration should have larger distributions, use more diverse resources, and be less vulnerable to population declines and extinctions, compared with taxa that do not vary in color. We used information from literature on 194 species of Australian frogs to search for associations of coloration mode with ecological variables. In general, species with variable or polymorphic color patterns had larger ranges, used more habitats, were less prone to have a negative population trend, and were estimated as less vulnerable to extinction compared with nonvariable species. An association of variable coloration with lower endangerment was also evident when we controlled statistically for the effects of range size. Nonvariable coloration was not a strong predictor of endangerment, and information on several characteristics is needed to reliably identify and protect species that are prone to decline and may become threatened by extinction in the near future. Analyses based on phylogenetic-independent contrasts did not support the hypothesis that evolutionary transitions between nonvariable and variable or polymorphic coloration have been accompanied by changes in the ecological variables we examined. Irrefutable demonstration of a role of color pattern variation in amphibian decline and in the dynamics and persistence of populations in general will require a manipulative experimental approach.

Ontogenetic variation in the chemical defenses of cane toads (Bufo marinus): toxin profiles and effects on predators.

We conducted a quantitative and qualitative chemical analysis of cane toad bufadienolides--the cardioactive steroids that are believed to be the principal cane toad toxins. We found complex shifts in toxin composition through toad ontogeny: (1) eggs contain at least 28 dominant bufadienolides, 17 of which are not detected in any other ontogenetic stage; (2) tadpoles present a simpler chemical profile with two to eight dominant bufadienolides; and (3) toxin diversity decreases during tadpole life but increases again after metamorphosis (larger metamorph/juvenile toads display five major bufadienolides). Total bufadienolide concentrations are highest in eggs (2.64 +/- 0.56 micromol/mg), decreasing during tadpole life stages (0.084 +/- 0.060 micromol/mg) before rising again after metamorphosis (2.35 +/- 0.45 micromol/mg). These variations in total bufadienolide levels correlate with toxicity to Australian frog species. For example, consumption of cane toad eggs killed tadpoles of two Australian frog species (Limnodynastes convexiusculus and Litoria rothii), whereas no tadpoles died after consuming late-stage cane toad tadpoles or small metamorphs. The high toxicity of toad eggs reflects components in the egg itself, not the surrounding jelly coat. Our results suggest a dramatic ontogenetic shift in the danger that toads pose to native predators, reflecting rapid changes in the types and amounts of toxins during toad development.

Factors influencing responses to alarm pheromone by larvae of invasive cane toads, Bufo marinus.

If pheromonal communication systems of invasive species differ from those of native biota, it may be possible to control the invader by exploiting that difference. When injured, the larvae of cane toads, Bufo marinus, an invasive species of major concern in tropical Australia, produce species-specific chemical cues that alert conspecific tadpoles to danger. Repeated exposure to the alarm chemical reduces tadpole survival rates and body sizes at metamorphosis and, thus, could help control toad populations. To evaluate the feasibility of this approach, we need to know how the intensity of toad tadpole response to the alarm chemical is affected by factors such as water temperature, time of day, larval stage and feeding history, geographic origin of the tadpoles, and habituation. Information on these topics may enable us to optimize deployment, so that tadpoles encounter pheromone at the times and places that confer maximum effect. In our studies, tadpole density, nutritional state, larval stage, and geographic origin had little effect on the intensity of the alarm response, but tadpoles reacted most strongly in higher water temperatures and during daylight hours. Repeated, once-daily exposure to pheromone did not induce habituation, but repeated exposure at 15-min intervals did not elicit further responses after 2 h total exposure. The insensitivity of response to most factors tested means that the effectiveness of the pheromone as a control agent should be relatively robust.

Calling is an honest indicator of paternal genetic quality in poison frogs.

Several competing hypotheses have been put forward to explain why females of many species mate preferentially with males possessing the most conspicuous signals (e.g., ornaments, displays, or songs). We performed a laboratory experiment using two species of poison frogs, Dendrobates leucomelas and Epipedobates tricolor, to test the hypothesis that male calling performance is an honest indicator of parental quality. Our analyses are based on data from behavioral observations of mating activities of captive-reared individuals (and their offspring) that were housed in terraria for four consecutive breeding seasons. Male mating success increased with male calling rate and chirp duration in both species, suggesting that females preferred males with more elaborate calls. Because calling performance improved with age in D. leucomelas, female poison frogs that prefer males with more elaborate calls in the wild may end up mating with older males that have already proven their ability to survive. Females that mated with good callers obtained higher quality offspring. Eggs fertilized by males with high calling rates and long chirp durations had higher hatching success and produced tadpoles that were more likely to metamorphose into surviving frogs. As a consequence, females that mated with males with high calling performance obtained more surviving offspring per egg, compared to females that mated with poor callers. Collectively, our findings comply with the notion that female poison frogs prefer to mate with good callers because calling performance is a reliable predictor of offspring quality. The possible influence of maternal allocation and reasons for the strong effect size compared to previous studies are discussed.

Correlated evolution of conspicuous coloration and body size in poison frogs (Dendrobatidae).

Conspicuous coloration is often used in combination with chemical defenses to deter predators from attacking. Experimental studies have shown that the avoidance inducing effect of conspicuous prey coloration increases with increasing size of pattern elements and with increasing body size. Here we use a comparative approach to test the prediction from these findings, namely that conspicuous coloration will evolve in tandem with body size. In our analysis, we use a previously published mitochondrial DNA-based phylogeny and comparative analysis of independent contrasts to examine if evolutionary shifts in color pattern have been associated with evolutionary changes in body size in aposematic poison frogs (Anura: Dendrobatidae). Information on body size (snout to vent length) and coloration were obtained from the literature. Two different measures of conspicuousness were used, one based on rankings by human observers and the other based on computer analysis of digitized photographs. The results from comparative analyses using either measure of coloration indicated that avoidance inducing coloration and body size have evolved in concert in poison frogs. Results from reconstruction of character change further indicate that the correlated evolution of size and coloration has involved changes in both directions within each of the different clades of the phylogenetic tree. This finding is consistent with the hypothesis that selection imposed by visually guided predators has promoted the evolution of larger body size in species with conspicuous coloration, or enhanced evolution of conspicuous coloration in larger species.