Understanding thermal performance at life stages that limit persistence is necessary to predict responses to climate change, especially for ectotherms whose fitness (survival and reproduction) depends on environmental temperature. Ectotherms often undergo stage-specific changes in size, complexity, and duration that are predicted to modify thermal performance. Yet performance is mostly explored for adults, while performance at earlier stages that typically limit persistence remains poorly understood. Here, we experimentally isolate thermal performance curves at fertilization, embryo development, and larval development in an aquatic ectotherm whose early planktonic stages (gametes, embryos, and larvae) govern adult abundances and dynamics. Unlike previous studies based on short-term exposures, responses with unclear links to fitness, or proxies in lieu of explicit curve descriptors (thermal optima, limits, and breadth), we measure performance as successful completion of each stage after exposure throughout, and at temperatures that explicitly capture curve descriptors at all stages. Formal comparisons of descriptors using a combination of generalized linear mixed modelling and parametric bootstrapping reveal important differences among life stages. Thermal performance differs significantly from fertilization to embryo development (with thermal optimum declining by ∼2 °C, thermal limits shifting inwards by ∼8–10 °C, and thermal breadth narrowing by ∼10 °C), while performance declines independently of temperature thereafter. Our comparisons show that thermal performance at one life stage can misrepresent performance at others, and point to gains in complexity during embryogenesis, rather than subsequent gains in size or duration of exposure, as a key driver of thermal sensitivity in early life.

Predictions of ectotherms' responses to global warming depend on the relationship between environmental temperature and organismal performance. To date, most predictions of thermal responses are generated from experimentally derived measures of thermal tolerances of adults or estimates of thermal niches derived from geographic distributions of adults. It is unknown how measures derived from these different approaches compare, or, as thermal performance of ectotherms varies through ontogeny, how they compare across life stages. To understand the efficacy of the temperature–performance relationship of early developmental stages as predictors of geographic range, we empirically documented the upper and lower thermal tolerance limits of embryos of eight species of ectotherms with complex life cycles. We compared the embryonic thermal tolerances of each species to that of the adults (documented in a previous study), as well as to an estimate of the thermal niche derived from adult distributions. Our results show that in all eight species the upper thermal limit estimated from embryos is significantly lower than the upper thermal limit estimated from adults. The lower thermal limit for embryos and for adult performance are similar, but the lower thermal limit for adult survival is significantly lower. Warming tolerances, calculated as the difference between upper tolerance limit and the average ambient temperature during the warmest month, for each species are also smaller for embryos (~1°C) than for adults (~5°C). These results show that thermal tolerances of early developmental stages, which are often easier to obtain for large sample sizes over an array of temperatures than are tolerances of adults, are a powerful, and potentially more accurate tool for predicting future responses to climate change. A free Plain Language Summary can be found within the Supporting Information of this article.

Understanding links between thermal performance and environmental variation is necessary to predict organismal responses to climate change, and remains an ongoing challenge for ectotherms with complex life cycles. Distinct life stages can differ in thermal sensitivity, experience different environmental conditions as development unfolds, and, because stages are by nature interdependent, environmental effects can carry over from one stage to affect performance at others. Thermal performance may therefore respond to carryover effects of prior thermal environments, yet detailed insights into the nature, strength, and direction of those responses are still lacking. Here, in an aquatic ectotherm whose early planktonic stages (gametes, embryos, and larvae) govern adult abundances and dynamics, we explore the effects of prior thermal environments at fertilization and embryogenesis on thermal performance curves at the end of planktonic development. We factorially manipulate temperatures at fertilization and embryogenesis, then, for each combination of prior temperatures, measure thermal performance curves for survival of planktonic development (end of the larval stage) throughout the performance range. By combining generalized linear mixed modeling with parametric bootstrapping, we formally estimate and compare curve descriptors (thermal optima, limits, and breadth) among prior environments, and reveal carryover effects of temperature at embryogenesis, but not fertilization, on thermal optima at completion of development. Specifically, thermal optima shifted to track temperature during embryogenesis, while thermal limits and breadth remained unchanged. Our results argue that key aspects of thermal performance are shaped by prior thermal environment in early life, warranting further investigation of the possible mechanisms underpinning that response, and closer consideration of thermal carryover effects when predicting organismal responses to climate change.

. Although larval stages are often considered particularly vulnerable to stressors, for many marine invertebrates studies of thermal tolerance have focused on adults. Here we determined the upper thermal limit (LT50) of the zoea I of four Caribbean crab species (Macrocoelomatrispinosum, Aratuspisonii, Armasesricordi, and Minucarapax) and compared their thermal tolerance over time and among species. The zoea from the subtidal species M.trispinosum and tree climbing mangrove species A.pisonii had a lower thermal tolerance, 35 and 38.5 °C respectively, than did the semiterrestrial A.ricordi and M.rapax. In all four species tested, the estimates of thermal tolerance depend on the duration of exposure to elevated temperatures. Longer exposures to thermal stress produce lower estimates of LT50, which decreased by ~1 °C from a two- to a six-hour exposure. Crab embryos develop on the abdomen of the mother until the larvae are ready to hatch. Therefore, the thermal tolerances of the embryos which need to coincide with the environmental conditions experienced by the adult stage, may carry over into the early zoea stage. Our results suggest that semiterrestrial species, in which embryos may need to withstand higher temperatures than embryos of subtidal species also produce larvae with higher thermal tolerances. Over the short term, the larvae of these tropical crab species can withstand significantly higher temperatures than those experienced in their marine habitat. Longer term rearing studies are necessary to determine the temperature at which chronic exposure has a negative impact on embryonic and larval survival.