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

Dahl, Emma; Orizaola, Germán; Nicieza, Alfredo G.; Laurila, Anssi

doi:10.1111/j.1365-2656.2012.02009.x

Cited by 39 publications

(45 citation statements)

References 57 publications

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“…Poor initial growth conditions, such as low temperature or high salinity, induce compensatory responses in amphibians (Hector, Bishop, & Nakagawa, 2012;Murillo-Rincón et al, 2017;Orizaola, Dahl, & Laurila, 2010;Orizaola, Richter-Boix, & Laurila, 2016;Squires, Bailey, Reina, & Wong, 2010). Compensatory growth negatively affects fitness-related components of larvae by reducing, for instance their swimming speed and immune status, or the locomotor performance of metamorphs (Dahl, Orizaola, Nicieza, & Laurila, 2012;Hector et al, 2012;Murillo-Rincón et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Metabolic costs of altered growth trajectories across life transitions in amphibians

Burraco

Valdés

Orizaola

2019

Journal of Animal Ecology

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Climate change is causing increases in temperature and in the frequency of extreme weather events. Under this scenario, organisms should maintain or develop strategies to cope with environmental fluctuations, such as the capacity to modify growth trajectories. However, altering growth can have negative consequences for organisms’ fitness. Here, we investigated the metabolic alterations induced by compensatory growth during the larval development of the common frog (Rana temporaria), quantifying changes in oxidative stress, corticosterone levels and telomere length. We induced compensatory growth responses by exposing frog embryos to cold conditions (i.e. a ‘false spring’ scenario), which cause a delay in hatching. Once hatched, we reared larvae at two different photoperiods (24:0, representing the natural photoperiod of larvae, and 18:6) to test also for the interactive effects of light on growth responses. Larvae experiencing delayed hatching showed fast compensatory responses and reached larger size at metamorphosis. Larvae shortened their developmental period in response to delayed hatching. Non‐permanent light conditions resulted in relaxed growth compared with larvae reared under permanent light conditions, which grew at their natural photoperiod and closer to their maximal rates. Growth responses altered the redox status and corticosterone levels of larvae. These physiological changes were developmental stage‐dependent and mainly affected by photoperiod conditions. At catch‐up, larvae reared at 18:6 light:dark cycles showed higher antioxidant activities and glucocorticoid secretion. On the contrary, larvae reared at 24:0 developed at higher rates without altering their oxidative status, likely an adaptation to grow under very restricting seasonal conditions at early life. At metamorphosis, compensatory responses induced higher cellular antioxidant activities probably caused by enhanced metabolism. Telomere length remained unaltered by experimental treatments but apparently tended to elongate across larval ontogeny, which would be a first evidence of telomere lengthening across metamorphosis. Under the forecasted increase in extreme climatic events, adjusting growth and developmental rates to the dynamics of environmental fluctuations may be essential for survival, but it can carry metabolic costs and affect later performance. Understanding the implications of such costs will be essential to properly estimate the impact of climate change on wild animals.

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Section: Introductionmentioning

confidence: 99%

Metabolic costs of altered growth trajectories across life transitions in amphibians

Burraco

Valdés

Orizaola

2019

Journal of Animal Ecology

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“…Amphibians can compensate for adverse growing conditions during the larval stage by increasing growth rate and/or extending the larval period to achieve a larger size at metamorphosis (Capellán & Nicieza ; Dahl et al . ; Orizaola et al . ) and can compensate for a delay in breeding or hatching by shortening their larval period and increasing growth rate (Orizaola, Dahl & Laurila ; Orizaola et al .…”

Section: Introductionmentioning

confidence: 99%

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

Murillo-Rincón

Kolter

Laurila

et al. 2016

Journal of Animal Ecology

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Summary1. 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). 2. 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. 3. 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. Nondelayed individuals gained advantage from developing with delayed larvae by increasing their developmental and growth rates as compared to single phenology groups. 4. 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. 5. 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.

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“…Moreover, rapid somatic growth prior to the breeding season would allow more time for gonad growth and hence increased fecundity or sperm production. The tendency to show a catch-up growth response may vary between populations in relation to the likelihood that they would naturally experience a time constraint (Dahl et al 2012;Orizaola, Dahl & Laurila 2014), suggesting that time constraints influence whether the benefits of faster growth would outweigh the costs of growth compensation. Metcalfe & Alonso- Alvarez (2010) argued that the extent of growth acceleration should be flexible under time stress since reduced time available prior to a life-history event such as reproduction would affect the ability of the animal to repair any molecular or tissue damage that had occurred as a result of the accelerated growth.…”

Section: Introductionmentioning

confidence: 99%

Perturbations in growth trajectory due to early diet affect age‐related deterioration in performance

2015

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Summary Fluctuations in early developmental conditions can cause changes in growth trajectories that subsequently affect the adult phenotype. Here, we investigated whether compensatory growth has long‐term consequences for patterns of senescence.Using three‐spined sticklebacks (Gasterosteus aculeatus), we show that a brief period of dietary manipulation in early life affected skeletal growth rate not only during the manipulation itself, but also during a subsequent compensatory phase when fish caught up in size with controls.However, this growth acceleration influenced swimming endurance and its decline over the course of the breeding season, with a faster decline in fish that had undergone faster growth compensation.Similarly, accelerated growth led to a more pronounced reduction in the breeding period (as indicated by the duration of sexual ornamentation) over the following two breeding seasons, suggesting faster reproductive senescence. Parallel experiments showed a heightened effect of accelerated growth on these age‐related declines in performance if the fish were under greater time stress to complete their compensation prior to the breeding season.Compensatory growth led to a reduction in median life span of 12% compared to steadily growing controls. While life span was independent of the eventual adult size attained, it was negatively correlated with the age‐related decline in swimming endurance and sexual ornamentation.These results, complementary to those found when growth trajectories were altered by temperature rather than dietary manipulations, show that the costs of accelerated growth can last well beyond the time over which growth rates differ and are affected by the time available until an approaching life‐history event such as reproduction.

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

Cited by 39 publications

References 57 publications

Metabolic costs of altered growth trajectories across life transitions in amphibians

Metabolic costs of altered growth trajectories across life transitions in amphibians

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

Perturbations in growth trajectory due to early diet affect age‐related deterioration in performance

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