Shrinking body sizes in response to warming: explanations for the temperature–size rule with special emphasis on the role of oxygen

Abstract

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 breathers versus air breathers), genome size, voltinism and thermally associated behaviour (e.g. heliotherms).

Oxygen limitation may affect the temperature and size dependence of metabolism in aquatic ectotherms

“…Second, large individuals are likely more susceptible to oxygen limitation and therefore they could experience a greater reduction in aerobic scope with warming. This prediction supports the idea that oxygen limitation is at least partly responsible for driving the reduction of body size in response to global warming ( 32 , 45 , 49 ). Finally, risks of oxygen limitation will be greater in aquatic ecosystems.…”

“…A secondorder extrapolation of our model is that, in aquatic ectotherms, larger individuals likely experience greater oxygen limitation whenever temperatures are warmer, or activity levels are higher. Therefore, large animals may have some aerobic scope left to fuel activity, growth, and reproduction in cold waters but not in warmer waters--a prediction that is consistent with the temperature-size rule, i.e., the tendency of many ectotherms to grow to smaller final sizes when reared in warmer temperatures (45). Thus, Forster et al (46) found that the temperature-size rule is more pronounced in aquatic than terrestrial species.…”

Elevated temperatures drive the evolution of armour loss in the threespine sticklebackGasterosteus aculeatus

“…Because we control for spatial autocorrelation in the data, we can tentatively conclude that these associations do not simply reflect other ecological responses to elevated temperatures with consequences for lateral plate number that also correlate with body size, such as predation. However, we believe the most parsimonious interpretation of the results are that (a) A decline in body size is associated with elevated average temperatures, which shows a temporal association (this study) and a spatial association (Smith et al, 2020b), and reflects a well-established ecological relationship between body size and temperature (Verberk et al, 2021). (b) Lateral plate number is strongly associated with body size in sticklebacks, which is associated with swimming efficiency (Bergstrom, 2002;Smith et al, 2020b).…”

“…Conversely, a switch from 91% dominance by lowplated sticklebacks to dominance by completely plated fish in Lake Washington was associated with a 30% increase in mean fish length (Kitano et al, 2008). (Verberk et al, 2021). The causal explanation for this relationship is unclear, but applies across a range of endotherms and ectotherms, including fishes (Morris et al, 2017;Verberk et al, 2021).…”

Reproduction probabilities and size distributions of the smooth snake Coronella austriaca in the Netherlands and Norway

“…Annual mean temperature can also affect reproductive output, for instance mild winter conditions can induce an increase in body condition, and consequently higher reproduction rates (Brischoux et al, 2016). These temperature effects on ectotherms also lead to the expectation that individual reproduction probabilities change over latitudinal or altitudinal gradients due to changes in temperature throughout the reproductive season: when summer seasons become shorter (e.g., pole-wards or at higher altitudes), reproduction could be expected to become less frequent, while energy maybe spent more on an increase of body mass (Buckley et al, 2012;Rutschmann et al, 2020;Verberk et al, 2020).…”