Most ectothermic organisms mature at smaller body sizes when reared in warmer conditions. This phenotypically plastic response, known as the “temperature-size rule” (TSR), is one of the most taxonomically widespread patterns in biology. However, the TSR remains a longstanding life-history puzzle for which no dominant driver has been found. We propose that oxygen supply plays a central role in explaining the magnitude of ectothermic temperature-size responses. Given the much lower oxygen availability and greater effort required to increase uptake in water vs. air, we predict that the TSR in aquatic organisms, especially larger species with lower surface area–body mass ratios, will be stronger than in terrestrial organisms. We performed a meta-analysis of 1,890 body mass responses to temperature in controlled experiments on 169 terrestrial, freshwater, and marine species. This reveals that the strength of the temperature-size response is greater in aquatic than terrestrial species. In animal species of ∼100 mg dry mass, the temperature-size response of aquatic organisms is 10 times greater than in terrestrial organisms (−5.0% °C ⁻¹ vs. −0.5% °C ⁻¹ ). Moreover, although the size response of small (<0.1 mg dry mass) aquatic and terrestrial species is similar, increases in species size cause the response to become increasingly negative in aquatic species, as predicted, but on average less negative in terrestrial species. These results support oxygen as a major driver of temperature-size responses in aquatic organisms. Further, the environment-dependent differences parallel latitudinal body size clines, and will influence predicted impacts of climate warming on food production, community structure, and food-web dynamics.

An inverse relationship between organism size and rearing temperature is widely observed in ectotherms (‘the temperature–size rule’, TSR). This has rarely been quantified for related taxa, and its applicability to protists also required testing. Here, we quantify the relationship between temperature and mean cell volume within the protists by a meta–analysis of published data covering marine, brackish water and freshwater autotrophs and heterotrophs. In each of 44 datasets, a linear relationship between temperature and size could not be rejected, and a negative trend was found in 32 cases (20 gave significant negative regressions, p < 0.05). By combining 65 datasets, we revealed, for each 1 °C increase, a cell–size reduction of 2.5% (95% CI of 1.7–3.3%) of the volume observed at 15 °C. The value did not differ across taxa (amoebae, ciliates, diatoms, dinoflagellates, flagellates), habitats, modes of nutrition or combinations of these. The data are consistent with two hypotheses that are capable of explaining the TSR in ectotherms generally: (i) resource, especially respiratory gas, limitation; and (ii) fitness gains from dividing earlier as population growth increases. Using the above relationship we show how changes in cell numbers with temperature can be estimated from changes in biomass and vice versa; ignoring this relationship would produce a systematic error.

Body size is central to ecology at levels ranging from organismal fecundity to the functioning of communities and ecosystems. Understanding temperature‐induced variations in body size is therefore of fundamental and applied interest, yet thermal responses of body size remain poorly understood. Temperature–size (T–S) responses tend to be negative (e.g. smaller body size at maturity when reared under warmer conditions), which has been termed the temperature–size rule (TSR). Explanations emphasize either physiological mechanisms (e.g. limitation of oxygen or other resources and temperature‐dependent resource allocation) or the adaptive value of either a large body size (e.g. to increase fecundity) or a short development time (e.g. in response to increased mortality in warm conditions). Oxygen limitation could act as a proximate factor, but we suggest it more likely constitutes a selective pressure to reduce body size in the warm: risks of oxygen limitation will be reduced as a consequence of evolution eliminating genotypes more prone to oxygen limitation. Thus, T–S responses can be explained by the ‘Ghost of Oxygen‐limitation Past’, whereby the resulting (evolved) T–S responses safeguard sufficient oxygen provisioning under warmer conditions, reflecting the balance between oxygen supply and demands experienced by ancestors. T–S responses vary considerably across species, but some of this variation is predictable. Body‐size reductions with warming are stronger in aquatic taxa than in terrestrial taxa. We discuss whether larger aquatic taxa may especially face greater risks of oxygen limitation as they grow, which may be manifested at the cellular level, the level of the gills and the whole‐organism level. In contrast to aquatic species, terrestrial ectotherms may be less prone to oxygen limitation and prioritize early maturity over large size, likely because overwintering is more challenging, with concomitant stronger end‐of season time constraints. Mechanisms related to time constraints and oxygen limitation are not mutually exclusive explanations for the TSR. Rather, these and other mechanisms may operate in tandem. But their relative importance may vary depending on the ecology and physiology of the species in question, explaining not only the general tendency of negative T–S responses but also variation in T–S responses among animals differing in mode of respiration (e.g. water breathersversusair breathers), genome size, voltinism and thermally associated behaviour (e.g. heliotherms).