A macroecological approach to evolutionary rescue and adaptation to climate change

Despite the widespread use of ecological niche models (ENMs) for predicting the responses of species to climate change, these models do not explicitly incorporate any population‐level mechanism. On the other hand, mechanistic models adding population processes (e.g. biotic interactions, dispersal and adaptive potential to abiotic conditions) are much more complex and difficult to parameterize, especially if the goal is to predict range shifts for many species simultaneously. In particular, the adaptive potential (based on genetic adaptations, phenotypic plasticity and behavioral adjustments for physiological responses) of local populations has been a less studied mechanism affecting species’ responses to climatic change so far. Here, we discuss and apply an alternative macroecological framework to evaluate the potential role of evolutionary rescue under climate change based on ENMs. We begin by reviewing eco‐evolutionary models that evaluate the maximum sustainable evolutionary rate under a scenario of environmental change, showing how they can be used to understand the impact of temperature change on a Neotropical anuran species, the Schneider's toad Rhinella diptycha. Then we show how to evaluate spatial patterns of species’ geographic range shift using such models, by estimating evolutionary rates at the trailing edge of species distribution estimated by ENMs and by recalculating the relative amount of total range loss under climate change. We show how different models can reduce the expected range loss predicted for the studied species by potential ecophysiological adaptations in some regions of the trailing edge predicted by ENMs. For general applications, we believe that parameters for large numbers of species and populations can be obtained from macroecological generalizations (e.g. allometric equations and ecogeographical rules), so our framework coupling ENMs with eco‐evolutionary models can be applied to achieve a more accurate picture of potential impacts from climate change and other threats to biodiversity.     

Factors affecting the vulnerability of cane toads (Bufo marinus) to predation by ants

Experimental evidence on the determinants of prey vulnerability is scarce, especially for vertebrates in the field. Invasive species offer robust opportunities to explore prey vulnerability, because the intensity of predation on or by such animals has not been eroded by coevolution. Around waterbodies in tropical Australia, native meat ants (Iridomyrmex reburrus) consume many metamorph cane toads (Bufo marinus, an invasive anuran). We document the determinants of toad vulnerability, especially the roles of toad body size and ant density. Larger metamorphs were attacked sooner (because they attracted more ants), but escaped more often. Overall, smaller toads were more likely to be killed. Ant densities influenced toad responses, as well as attack rate and success. Data on the immediate outcomes of attacks underestimate mortality: more than 73% of apparent ‘escapees’ died within 24 h. Because mortality during this period was independent of toad size, predation was less size selective than suggested by immediate outcomes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 738–751.     

Predator behaviour and morphology mediates the impact of an invasive species: cane toads and death adders in Australia

The arrival of an invasive species can have severe impacts on native species. The extent of the impact, as well as the speed at which native species may mount an adaptive response, depend upon the correlation between impact and the individual phenotypes of the native species. Strong correlation between phenotype and impact within the native species raises the possibility of rapid adaptive response to the invader. Here, we examine the impact of a dangerous newly arrived prey species (the highly toxic cane toad Bufo marinus ) on naïve predators (death adders Acanthophis praelongus ) in northern Australia. During laboratory trials and field radiotracking, toads killed 48% of the adders we studied. Long-term monitoring of the population also suggests a massive decline (>89%) in recent years concurrent with the arrival of toads. Variation in snake physiology (resistance to toad toxin) had little bearing on snake survival in the field. Snake behaviour (tendency to attack toads) and morphology (body size and head size), however, were strong predictors of snake survival. Smaller snakes with relatively small heads, and snakes that were unwilling to attack toads in the laboratory, had much higher survival rates in the field. These results show that toads have a massive impact on death adder populations, but that snake phenotypes strongly mediate this impact. Thus natural selection is operating on these adder populations and an adaptive response is a possibility. If these adders can rapidly shift toad-relevant morphological and behavioural traits (either through plastic or evolved means), they will ultimately face a lowered impact from this toxic invader.     

Vulnerability of an Australian anuran tadpole assemblage to the toxic eggs of the invasive cane toad (Bufo marinus)

The invasion of cane toads (Bufo marinus) across tropical Australia has fatally poisoned many native predators; the most frequent victims may be tadpoles of native frogs, which die when they consume the toxic eggs of the toads. Field studies have documented high and species‐specific mortality of tadpoles following toad spawning. To clarify the determinants of tadpole vulnerability, we conducted 1593 laboratory trials in which single tadpoles were exposed to 10 toad eggs, either with or without an alternative food source (lettuce). At least some tadpoles within all 15 species tested consumed toad eggs. Interspecific variance in survival rates (from 0 to >70%) was driven by feeding responses not by physiological tolerance to toxins: almost all native tadpoles that consumed eggs died rapidly. Tadpole mortality was decreased by the presence of an alternative food source in four species, increased in two species, and not affected in seven species. In three of four taxa where we tested both small (early‐stage) and large (late‐stage) tadpoles, both mean survival rates and the effects of alternative food on survival shifted with tadpole body size. Trials with one species (Limnodynastes convexiusculus) showed no significant inter‐clutch variation in feeding responses or tolerance to toxins. Overall, our data show that cane toad eggs are highly toxic to native anuran tadpoles, but that whether or not a tadpole is killed by encountering toad eggs depends upon a complex interaction between the native anuran's species, its body size, and whether or not alternative food was present. In nature, larval vulnerability also depends upon the seasonal timing and location of spawning events, and habitat selection and foraging patterns of the tadpoles. Our results highlight the complexity of vulnerability determinants, and identify ecological factors (rather than physiology or feeding behaviour) as the primary determinants of cane toad impact on native tadpoles.     

Behavioural flexibility allows an invasive vertebrate to survive in a semi-arid environment

Plasticity or evolution in behavioural responses are key attributes of successful animal invasions. In northern Australia, the invasive cane toad (Rhinella marina) recently invaded semi-arid regions. Here, cane toads endure repeated daily bouts of severe desiccation and thermal stress during the long dry season (April–October). We investigated whether cane toads have shifted their ancestral nocturnal rehydration behaviour to one that exploits water resources during the day. Such a shift in hydration behaviour could increase the fitness of individual toads by reducing exposure to desiccation and thermal stress suffered during the day even within terrestrial shelters. We used a novel method (acoustic tags) to monitor the daily hydration behaviour of 20 toads at two artificial reservoirs on Camfield station, Northern Territory. Remarkably, cane toads visited reservoirs to rehydrate during daylight hours, with peaks in activity between 9.00 and 17.00. This diurnal pattern of rehydration activity contrasts with nocturnal rehydration behaviour exhibited by adult toads in their native geographical range and more mesic parts of Australia. Our results demonstrate that cane toads phase shift a key behaviour to survive in a harsh semi-arid landscape. Behavioural phase shifts have rarely been reported in invasive species but could facilitate ongoing invasion success.     

Amphibian larvae and zinc sulphate: a suitable model to study the role of brain-derived neurotrophic factor (BDNF) in the neuronal turnover of the olfactory epithelium

The vertebrate olfactory system has fascinated neurobiologists over the last six decades because of its ability to replace its neurons and synaptic connections continuously throughout adult life, under both physiological and pathological conditions. Among the factors that are proposed to be involved in this regenerative potential, brain-derived neurotrophic factor (BDNF) is a candidate for having an important role in the neuronal turnover in the olfactory epithelium (OE) because of its well-documented neurogenic and trophic effects throughout the nervous system. The aim of the present study was to generate a suitable model to study the participation of BDNF in the recovery of the OE after injury in vivo. We developed an experimental design in which the OE of Rhinella arenarum tadpoles could be easily and selectively damaged by immersing the animals in ZnSO₄ solutions of various concentrations for differing time periods. Image analysis of histological sections showed that different combinations of each of these conditions produced statistically different degrees of injury to the olfactory tissue. We also observed that the morphology of the OE was restored within a few days of recovery after ZnSO₄ treatment. Immunohistochemical analysis of BDNF was performed with an antiserum whose specificity was confirmed by Western blotting, and which showed drastic changes in the abundance and distribution pattern of this neurotrophin in the damaged olfactory system. Our results thus suggest that BDNF is involved in the regeneration of the OE of amphibian larvae, and that our approach is suitable for further investigations of this topic. This work was supported by grants from CONICET (PIP 5842), Universidad de Buenos Aires (UBACYT X131) and ANPCYT (PICT 32219).     

Teasing apart crypsis and aposematism – evidence that disruptive coloration reduces predation on a noxious toad

Both cryptic and aposematic colour patterns can reduce predation risk to prey. These distinct strategies may not be mutually exclusive, because the impact of prey coloration depends on a predator's sensory system and cognition and on the environmental background. Determining whether prey signals are cryptic or aposematic is a prerequisite for understanding the ecological and evolutionary implications of predator–prey interactions. This study investigates whether coloration and pattern in an exceptionally polymorphic toad, Rhinella alata, from Barro Colorado Island, Panama reduces predation via background matching, disruptive coloration, and/or aposematic signaling. When clay model replicas of R. alata were placed on leaf litter, the model's dorsal pattern – but not its colour – affected attack rates by birds. When models were placed on white paper, patterned and un‐patterned replicas had similar attack rates by birds. These results indicate that dorsal patterns in R. alata are functionally cryptic and emphasize the potential effectiveness of disruptive coloration in a vertebrate taxon.     

Pelvic function in anuran jumping: Interspecific differences in the kinematics and motor control of the iliosacral articulation during take‐off and landing

Although the anuran pelvis is thought to be adapted for jumping, the function of the iliosacral joint has seen little direct study. Previous work has contrasted the basal “ lateral‐bender ” pelvis from the “ rod‐like ” pelvis of crown taxa hypothesized to function as a sagittal hinge to align the trunk with take‐off forces. We compared iliosacral movements and pelvic motor patterns during jumping in the two pelvic types. Pelvic muscle activity patterns, iliosacral anteroposterior (AP) movements and sagittal bending of the pelvis during the take‐off and landing phases were quantified in lateral bender taxa Ascaphus (Leiopelmatidae) and Rhinella (Bufonidae) and the rod‐like Lithobates (Ranidae). All three species exhibit sagittal extension during take‐off, therefore, both pelvic types employ a sagittal hinge. However, trunk elevation occurs significantly earlier in the anuran rod‐like pelvis. Motor patterns confirm that the piriformis muscles depress the urostyle while the longissimus dorsi muscles elevate the trunk during take‐off. However, the coccygeoiliacus muscles also produce anterior translation of the sacrum on the ilia. A new model illustrates how AP translation facilitates trunk extension in the lateral‐bender anurans that have long been thought to have limited sagittal bending. During landing, AP translation patterns are similar because impact forces slide the sacrum from its posterior to anterior limits. Sagittal flexion during landing differs among the three taxa depending on the way the species land. AP translation during landing may dampen impact forces especially in Rhinella in which pelvic function is tuned to forelimb‐landing dynamics. The flexibility of the lateral‐bender pelvis to function in sagittal bending and AP translation helps to explain the retention of this basal configuration in many anurans. The novel function of the rod‐like pelvis may be to increase the rate of trunk elevation relative to faster rates of energy release from the hindlimbs enabling them to jump farther. J. Morphol. 277:1539–1558, 2016. © 2016 Wiley Periodicals, Inc.