Species’ vulnerability to climate change depends on the most temperature-sensitive life stages, but for major animal groups such as fish, life cycle bottlenecks are often not clearly defined. We used observational, experimental, and phylogenetic data to assess stage-specific thermal tolerance metrics for 694 marine and freshwater fish species from all climate zones. Our analysis shows that spawning adults and embryos consistently have narrower tolerance ranges than larvae and nonreproductive adults and are most vulnerable to climate warming. The sequence of stage-specific thermal tolerance corresponds with the oxygen-limitation hypothesis, suggesting a mechanistic link between ontogenetic changes in cardiorespiratory (aerobic) capacity and tolerance to temperature extremes. A logarithmic inverse correlation between the temperature dependence of physiological rates (development and oxygen consumption) and thermal tolerance range is proposed to reflect a fundamental, energetic trade-off in thermal adaptation. Scenario-based climate projections considering the most critical life stages (spawners and embryos) clearly identify the temperature requirements for reproduction as a critical bottleneck in the life cycle of fish. By 2100, depending on the Shared Socioeconomic Pathway (SSP) scenario followed, the percentages of species potentially affected by water temperatures exceeding their tolerance limit for reproduction range from ~10% (SSP 1–1.9) to ~60% (SSP 5–8.5). Efforts to meet ambitious climate targets (SSP 1–1.9) could therefore benefit many fish species and people who depend on healthy fish stocks.

Acidification narrows thermal ranges of Arctic fish embryos and thereby constraints reproductive opportunities in a warming ocean.

Thermal tolerance windows serve as a powerful tool for estimating the vulnerability of marine species and their life stages to increasing temperature means and extremes. However, it remains uncertain to which extent additional drivers, such as ocean acidification, modify organismal responses to temperature. This study investigated the effects of CO -driven ocean acidification on embryonic thermal sensitivity and performance in Atlantic cod, Gadus morhua, from the Kattegat. Fertilized eggs were exposed to factorial combinations of two PCO conditions (400 μatm vs. 1100 μatm) and five temperature treatments (0, 3, 6, 9 and 12 °C), which allow identifying both lower and upper thermal tolerance thresholds. We quantified hatching success, oxygen consumption (MO ) and mitochondrial functioning of embryos as well as larval morphometrics at hatch and the abundance of acid-base-relevant ionocytes on the yolk sac epithelium of newly hatched larvae. Hatching success was high under ambient spawning conditions (3-6 °C), but decreased towards both cold and warm temperature extremes. Elevated PCO caused a significant decrease in hatching success, particularly at cold (3 and 0 °C) and warm (12 °C) temperatures. Warming imposed limitations to MO and mitochondrial capacities. Elevated PCO stimulated MO at cold and intermediate temperatures, but exacerbated warming-induced constraints on MO , indicating a synergistic interaction with temperature. Mitochondrial functioning was not affected by PCO . Increased MO in response to elevated PCO was paralleled by reduced larval size at hatch. Finally, ionocyte abundance decreased with increasing temperature, but did not differ between PCO treatments. Our results demonstrate increased thermal sensitivity of cod embryos under future PCO conditions and suggest that acclimation to elevated PCO requires reallocation of limited resources at the expense of embryonic growth. We conclude that ocean acidification constrains the thermal performance window of embryos, which has important implication for the susceptibility of cod to projected climate change.