Germán Orizaola

Rapid evolution of constitutive and inducible defenses against an invasive predator

Invasive alien predators can impose strong selection on native prey populations and induce rapid evolutionary change in the invaded communities. However, studies on evolutionary responses to invasive predators are often complicated by the lack of replicate populations differing in coexistence time with the predator, which would allow the determination of how prey traits change during the invasion. The red swamp crayfish Procambarus clarkii has invaded many freshwater areas worldwide, with negative impacts for native fauna. Here, we examined how coexistence time shapes antipredator responses of the Iberian waterfrog (Pelophylax perezi) to the invasive crayfish by raising tadpoles from five populations differing in historical exposure to P. clarkii (30 years, 20 years, or no coexistence). Tadpoles from non-invaded populations responded to the presence of P. clarkii with behavioral plasticity (reduced activity), whereas long-term invaded populations showed canalized antipredator behavior (constant low activity level). Tadpoles from one of the long-term invaded populations responded to the crayfish with inducible morphological defenses (deeper tails), reflecting the use of both constitutive and inducible antipredator defenses against the exotic predator by this population. Our results suggest that, while naive P. perezi populations responded behaviorally to P. clarkii, the strong predation pressure imposed by the crayfish has induced the evolution of qualitatively different antipredator defenses in populations with longer coexistence time. These responses suggest that strong selection by invasive predators may drive rapid evolutionary change in invaded communities. Examining responses of prey species to biological invasions using multiple populations will help us better forecast the impact of invasive predators in natural communities.

Microgeographic variation in temperature-induced plasticity in an isolated amphibian metapopulation

Variation in local environments may lead to variation in the selection pressures and differentiation among local populations even at microgeographic scale. We investigated variation in temperature-induced plasticity in larval life-history traits among populations of an isolated pool frog (Rana lessonae) metapopulation in Central Sweden. Successful breeding of this northern fringe metapopulation is highly dependent on early summer temperature, however, the metapopulation shows very little variation in molecular genetic markers suggesting limited potential for local differentiation. We exposed larvae from three closely-located populations to two temperatures (20 and 25°C) in laboratory to investigate their growth and development responses to temperature variation. In general, larvae exposed to warmer temperature experienced higher survival and metamorphosed faster, but at a smaller size than those at low temperature. We found differences among the populations in both trait mean values and in the plastic responses. Among-family variation within populations was found in growth rate and time to metamorphosis, as well as in plasticity suggesting that these traits have a capacity to evolve. Our results indicate ample phenotypic variation within and among these closely-located populations despite the low molecular genetic variation. The differences in pond temperature characteristics detected in the study in the three localities may suggest that differential selection is acting in the populations. The strong differentiation found in the larval traits implies that understanding the factors that influence the potential of the populations to adapt to environmental changes may be essential for successful conservation strategies.

Time constraints and flexibility of growth strategies: geographic variation in catch-up growth responses in amphibian larvae

1. As size is tightly associated with fitness, compensatory strategies for growth loss can be vital for restoring individual fitness. However, immediate and delayed costs of compensatory responses may prevent their generalization, and the optimal strategy may depend on environmental conditions. Compensatory responses may be particularly important in high-latitude habitats with short growing seasons, and thus, high-latitude organisms might be more efficient at compensating after periods of unfavourable growth conditions than low-latitude organisms. 2. We investigated geographical differences in catch-up growth strategies of populations of the common frog (Rana temporaria) from southern and northern Sweden in two factorial common garden experiments involving predation risk and two different causes of growth arrest (nutritional stress and low temperatures) to evaluate how the compensatory strategies can be affected by context-dependent costs of compensation. Larval and metamorphic traits, and post-metamorphic performance were used as response variables. 3. Only northern tadpoles exposed to low food completely caught up in terms of metamorphic size, mainly by extending the larval period. Low food decreased survival and post-metamorphic jumping performance in southern, but not in northern tadpoles, suggesting that northern tadpoles have a better ability to compensate after periods of restricted food. 4. Both northern and southern tadpoles were able to metamorphose at the same size as control tadpoles after being exposed to low temperatures, indicating that consequences of variation in temperature and food availability differed for tadpoles. However, the combination of low temperatures and predation risk reduced survival in both southern and northern tadpoles. Also, predation risk decreased energy storage in both experiments. 5. Our results highlight the influence of climatic variation and the type of stressor as selective factors shaping compensatory strategies.

Geographic variation in corticosterone response to chronic predator stress in tadpoles

Chronic stress often affects growth and development negatively, and these effects are often mediated via glucocorticoid hormones, which elevate during stress. We investigated latitudinal variation in corticosterone (CORT) response to chronic predator stress in Rana temporaria tadpoles along a 1500‐km latitudinal cline in Sweden tadpoles, in a laboratory experiment. We hypothesized that more time‐constrained high‐latitude populations have evolved a lower CORT response to chronic stress to maintain higher growth under stressful conditions. Southern tadpoles had higher CORT content in response to predators after 1 day of exposure, whereas there was no increase in CORT in the northern populations. Two weeks later, there were no predator‐induced CORT elevations. Artificially elevated CORT levels strongly decreased growth, development and survival in both northern and southern tadpoles. We suggest that the lower CORT response in high‐latitude populations can be connected with avoidance of CORT‐mediated reduction in growth and development, but also discuss other possible explanations.

Transgenerational phenotypic plasticity links breeding phenology with offspring life‐history

The timing of seasonal life-history events is assumed to evolve to synchronize life cycles with the availability of resources. Temporal variation in breeding time can have severe fitness consequences for the offspring, but the interplay between adult reproductive decisions and offspring phenotypes remains poorly understood. Transgenerational plasticity (TGP) is a potential mechanism allowing rapid responses to environmental change. Here, we investigated if experimentally delayed breeding induces TGP in larval life-history traits in the moor frog (Rana arvalis). We found clear evidence of TGP in response to changes in breeding phenology: delayed breeding increased offspring development and growth rates in the absence of external cues. This constitutes the first unequivocal evidence for TGP in response to changes in breeding phenology in vertebrates. TGP can play an important role in adjusting offspring life-history strategies to the environment they are most likely to encounter, and may constitute an important mechanism for coping with climate change.

Assessing the role of multiple environmental factors on Eurasian Spoonbill departure decisions from stopover sites

Understanding the factors driving departure decisions from stopover sites is critical when predicting the dynamics of bird migration. We Investigated the Interactive effects of wind, tidal characteristics, and precipitation on the departure decisions of the Eurasian Spoonbill Platalea l. leucorodia from a major coastal stopover locality in northern Iberia. Most departing Spoonbills (>80%) crossed an adjacent mountain range to follow a direct route over Inland Iberia, while the remainder made a detour following an Indirect coastal route along the coast of the Iberian Peninsula. During four consecutive autumns, we daily monitored departing Spoonbills leaving along these two routes. The birds taking the Inland route, crossing unsuitable habitats and needing therefore higher fuel-loads, departed preferentially under favourable tailwind conditions (TWC). This represented a significant increase in distance covered and/or a decrease in energy spent per unit time. Moreover, Spoonbills taking the inland route often departed during spring tides. For the indirect coastal route, TWC did not affect the onset of migration but bird departures increased with neap tides. Precipitation and date were negatively correlated with departures towards both routes, whereas Spoonbill density at the stopover had a positive effect. Our findings provide empirical support for the role that wind assistance may play for Spoonbills to resume migration.

Warm vegetarians? Heat waves and diet shifts in tadpoles

Temperature can play an important role in determining the feeding preferences of ectotherms. In light of the warmer temperatures arising with the current climatic changes, omnivorous ectotherms may perform diet shifts toward higher herbivory to optimize energetic intake. Such diet shifts may also occur during heat waves, which are projected to become more frequent, intense, and longer lasting in the future. Here, we investigated how heat waves of different duration affect feeding preferences in omnivorous anuran tadpoles and how these choices affect larval life history. In laboratory experiments, we fed tadpoles of three species on animal, plant, or mixed diet and exposed them to short heat waves (similar to the heat waves these species experience currently) or long heat waves (predicted to increase under climate change). We estimated the dietary choices of tadpoles fed on the mixed diet using stable isotopes and recorded tadpole survival and growth, larval period, and mass at metamorphosis. Tadpole feeding preferences were associated with their thermal background, with herbivory increasing with breeding temperature in nature. Patterns in survival, growth, and development generally support decreased efficiency of carnivorous diets and increased efficiency or higher relative quality of herbivorous diets at higher temperatures. All three species increased herbivory in at least one of the heat wave treatments, but the responses varied among species. Diet shifts toward higher herbivory were maladaptive in one species, but beneficial in the other two. Higher herbivory in omnivorous ectotherms under warmer temperatures may impact species differently and further contribute to changes in the structure and function of freshwater environments.

Is one defence enough? Disentangling the relative importance of morphological and behavioural predator-induced defences

Many organisms show predator-induced behavioural and morphological phenotypic plasticity. These defence mechanisms are often expressed simultaneously. To estimate the relative importance of these two defences, we conducted a laboratory experiment using tadpoles of the common frog (Rana temporaria) as prey and Aeshna dragonfly larvae as predators. We first raised tadpoles in the presence and absence of caged predators to induce differences in defensive morphology, and then conducted free ranging predator trials in environments that were either with or without the presence of predation cues to induce differences in defensive behaviour. This 2 × 2 design allowed us to separate the effects of inducible morphology from inducible behaviour. Caged predators induced deeper bodies and tailfins and reduced activity levels in tadpoles. The time to first capture was shortest in tadpoles without morphological or behavioural defences. Tadpoles with a behavioural defence had a significantly longer time to first capture. Tadpoles with only antipredator morphology tended to have a longer time to first capture as compared to those without any induced defences. This treatment also had a higher number of injured tadpoles as compared to other treatments, suggesting that inducible morphology facilitates predator escape due to the ‘lure effect’. However, tadpoles with both behavioural and morphological defences did not have a longer time to first capture as compared to tadpoles with only morphological or behavioural induced defences. Our results suggest that both behavioural and morphological antipredator responses contribute to reduced capture efficiency by predators, but their simultaneous expression did not have any additive effect to the time of first capture and survival, and that the morphology response is most effective when tadpoles are active.

Developmental plasticity increases at the northern range margin in a warm‐dependent amphibian

Accurate predictions regarding how climate change affects species and populations are crucial for the development of effective conservation measures. However, models forecasting the impact of climate change on natural environments do not often consider the geographic variation of an organisms life history. We examined variation in developmental plasticity to changing temperature in the pool frog (Pelophylax lessonae) across its distribution by studying populations from central areas (Poland), edge populations (Latvia) and northern marginal populations (Sweden). Relative to central and edge populations, northern populations experience lower and less variable temperature and fewer episodes of warm weather during larval development. Plasticity in larval life‐history traits was highest at the northern range margin: larvae from marginal populations shortened larval period and increased growth rate more than larvae from central and edge populations when reared at high temperature. Maintaining high growth and development under the scarce spells of warm weather is likely adaptive for high‐latitude populations. The detection of high levels of developmental plasticity in isolated, marginal populations suggests that they may be better able to respond to the temperature regimes expected under climate change than often predicted, reflecting the need to incorporate geographic variation in life‐history traits into models forecasting responses to environmental change.

Intraspecific priority effects modify compensatory responses to changes in hatching phenology in an amphibian

In seasonal environments, modifications in the phenology of life-history events can alter the strength of time constraints experienced by organisms. Offspring can compensate for a change in timing of hatching by modifying their growth and development trajectories. However, intra- and interspecific interactions may affect these compensatory responses, in particular if differences in phenology between cohorts lead to significant priority effects (i.e. the competitive advantage that early-hatching individuals have over late-hatching ones). Here, we conducted a factorial experiment to determine whether intraspecific priority effects can alter compensatory phenotypic responses to hatching delay in a synchronic breeder by rearing moor frog (Rana arvalis) tadpoles in different combinations of phenological delay and food abundance. Tadpoles compensated for the hatching delay by speeding up their development, but only when reared in groups of individuals with identical hatching phenology. In mixed phenology groups, strong competitive effects by non-delayed tadpoles prevented the compensatory responses and delayed larvae metamorphosed later than in single phenology treatments. Non-delayed individuals gained advantage from developing with delayed larvae by increasing their developmental and growth rates as compared to single phenology groups. Food shortage prolonged larval period and reduced mass at metamorphosis in all treatments, but it did not prevent compensatory developmental responses in larvae reared in single phenology groups. This study demonstrates that strong intraspecific priority effects can constrain the compensatory growth and developmental responses to phenological change, and that priority effects can be an important factor explaining the maintenance of synchronic life histories (i.e. explosive breeding) in seasonal environments.