Seasonal time constraints can pose strong selection on life histories. Time-constrained animals should prioritise fast development over predation risk to avoid unfavourable growing conditions. However, changes in phenology could alter the balance between anti-predator and developmental needs. We studied variation of anti-predator strategies in common frog (Rana temporaria) tadpoles in four populations from the two extremes of a latitudinal gradient across Sweden. We examined, under common conditions in the laboratory, the anti-predator responses and life histories of tadpoles raised with predatory Aeshna dragonfly larvae in two consecutive years with a difference of 20 days in breeding time in the north, but no difference in breeding time in the nouth. In a year with late breeding, northern tadpoles did not modify their behaviour and morphology in the presence of predators, and metamorphosed faster and smaller than tadpoles born in a year with early breeding. In the year with early breeding, northern tadpoles showed a completely different anti-predator strategy by reducing activity and developing morphological defences in the presence of predators. We discuss the possible mechanisms that could activate these responses (likely a form of environmentally-mediated parental effect). To our knowledge, this is the first study to show that a vertebrate modifies the anti-predator strategy of its offspring in response to natural variation in reproductive phenology, which highlights the need to consider phenology in studies of life-history evolution.
Environmental conditions experienced early in the ontogeny can have a strong impact on individual fi tness and performance later in life. Organisms may counteract the negative eff ects of poor developmental conditions by developing compensatory responses in growth and development. However, previous studies on compensatory responses have largely ignored the eff ects that poor embryonic conditions could have during the later life stages. In this study, we examined the eff ects of artifi cially delayed development in early life over two later life history transitions by investigating the compensatory growth of larval moor frogs Rana arvalis in response to temperature variation during embryonic development, and the associated costs during the larval `and postmetamorphic stages. Low temperature during embryonic stage lead to delayed hatching at smaller size. Th e groups with delayed embryonic development showed strong compensatory growth during the larval stage, and reached similar metamorphic size than the controls in a shorter time. However, the most strongly delayed group was not able to fully catch up the total development time. Th ese compensatory responses were found in the absence of photoperiod cues indicating that the delay in embryonic development was suffi cient to initiate the compensatory response in larval growth and development. No apparent costs of compensatory growth were detected in terms of morphology or locomotor performance at the juvenile stage. We found that compensatory responses can be activated as early as at the embryonic stage and extend over several consecutive life history transitions, mitigating the eff ects of poor conditions experienced early in development. Potential short-term costs in natural environments and the occurrence of long-term costs, which prevent the generalisation of a faster larval life style, are discussed.
Organisms normally grow at a sub-maximal rate. After experiencing a period of arrested growth, individuals often show compensatory growth responses by modifying their life-history, behaviour and physiology. However, the strength of compensatory responses may vary across broad geographic scales as populations differ in their exposition to varying time constraints. We examined differences in compensatory growth strategies in common frog (Rana temporaria) populations from southern and northern Sweden. Tadpoles from four populations were reared in the laboratory and exposed to low temperature to evaluate the patterns and mechanisms of compensatory growth responses. We determined tadpoles' growth rate, food intake and growth efficiency during the compensation period. In the absence of arrested growth conditions, tadpoles from all the populations showed similar (size-corrected) growth rates, food intake and growth efficiency. After being exposed to low temperature for 1 week, only larvae from the northern populations increased growth rates by increasing both food intake and growth efficiency. These geographic differences in compensatory growth mechanisms suggest that the strategies for recovering after a period of growth deprivation may depend on the strength of time constraints faced by the populations. Due to the costs of fast growth, only populations exposed to the strong time constraints are prone to develop fast recovering strategies in order to metamorphose before conditions deteriorate. Understanding how organisms balance the cost and benefits of growth strategies may help in forecasting the impact of fluctuating environmental conditions on life-history strategies of populations likely to be exposed to increasing environmental variation in the future.
Summary 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.
In natural systems, organisms are frequently exposed to spatial and temporal variation in predation risk. Prey organisms are known to develop a wide array of plastic defences to avoid being eaten. If inducible plastic defences are costly, prey living under fluctuating predation risk should be strongly selected to develop reversible plastic traits and adjust their defences to the current predation risk. Here, we studied the induction and reversibility of antipredator defences in common frog Rana temporaria tadpoles when confronted with a temporal switch in predation risk by dragonfly larvae. We examined the behaviour and morphology of tadpoles in experimental treatments where predators were added or withdrawn at mid larval development, and compared these to treatments with constant absence or presence of predators. As previous studies have overlooked the effects that developing reversible anti‐predator responses could have later in life (e.g. at life history switch points), we also estimated the impact that changes in antipredator responses had on the timing of and size at metamorphosis. In the presence of predators, tadpoles reduced their activity and developed wider bodies, and shorter and wider tails. When predators were removed tadpoles switched their behaviour within one hour to match that found in the constant environments. The morphology matched that in the constant environments in one week after treatment reversal. All these responses were highly symmetrical. Short time lags and symmetrical responses for the induction/reversal of defences suggest that a strategy with fast switches between phenotypes could be favoured in order to maximise growth opportunities even at the potential cost of phenotypic mismatches. We found no costs of developing reversible responses to predators in terms of life‐history traits, but a general cost of the induction of the defences for all the individuals experiencing predation risk during some part of the larval development (delayed metamorphosis). More studies examining the reversibility of plastic defences, including other type of costs (e.g. physiological), are needed to better understand the adaptive value of these flexible strategies.
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