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).

Keywords: Bergmann's rule; cell size; climate warming; gigantism; growth trajectory; hypoxia; life-history trade-off; phenotypic plasticity; temperature-size rule; thermal reaction norms.

Fig 1

Thermal responses in body size (A) and growth rate (B). Responses are indicated for warm (red lines) and cold (blue lines) conditions. Arrows in B indicate that effects of warming are contingent on body size (and hence on time during ontogeny), stimulating growth during small, early life stages (upward arrow), but reducing growth in later, larger life stages (downward arrow). Note that this is a simplified schematic and in reality, the temperature–size rule (TSR) may progress irregularly over ontogeny (see Forster, Hirst, & Atkinson, 2011; Horne et al., 2019).

Fig 2

Temperature–size (T–S) responses (% change in body mass per °C) for terrestrial (black circles), freshwater (grey triangles) and marine (white triangles) arthropod species, plotted against their dry mass (standardized to 20°C) With increasing body mass, T–S responses became more negative in aquatic arthropods (dashed line; F _1,43 = 5.40, P = 0.02, r ² = 0.09), but in terrestrial arthropods they became more positive (solid line; F _1,69 = 9.28, P = 0.003, r ² = 0.11). Figure reprinted from Horne et al. (2015) with permission from John Wiley & Sons Ltd/CNRS.

Fig 3

Role of constraints in the von Bertalanffy/Pauly model (A) and the maintain aerobic scope and regulate oxygen supply (MASROS) model (B–D). In A, constraints on growing to a larger size are considered to be insurmountable, arising from geometric constraints on gill surface area scaling, and growth ceases when maintenance metabolism converges to supply capacity. Maintenance is here considered to fuel essential processes such as maintenance of electrochemical gradients, protein synthesis, and repair. In the MASROS model, animals still have aerobic scope left when reaching maximum size, which is considered to be a safety margin when animals face demanding but transient conditions (e.g. disease, episodes of hypoxia, predator attack, and possibly part of reproduction). Aerobic scope not reserved for the safety margin (in white) can be used to fuel growth and other routine activities (e.g. activity, digestion and possibly part of reproduction). Evolution is thus assumed to have modified growth trajectories to avoid oxygen limitation. Growth trajectories can be modulated by adaptive changes in the scaling of standard metabolic rate (SMR), maximum metabolic rate (MMR) or the width of the safety margin for aerobic scope. Warm conditions (shown in red), may lead to growth to a smaller size if the thermal sensitivity of maintenance (SMR) is higher than that of supply (MMR). This size decrease could be partly compensated for by allowing a reduction in the safety margin (panel D). Note that the slopes of the lines (i.e. the scaling exponents) can also vary with temperature, but are here kept constant for reasons of clarity.

Fig 4

Overview of influences on growth rate (G) and development rate (D) responses to temperature, and hence their ratio and the temperature–size response. TSR, temperature–size rule. Temperature stimulates both growth rate and development rate, but the relative increase may be modulated by effects of cell size, genome size, body size, life cycle, thermoregulatory behaviour and mode of respiration. Oxygen limitation is more likely in large aquatic ectotherms with large cells, and could constrain the stimulating effects of temperature on growth rate. Consequently, animal development outpaces growth under warmer conditions, resulting in a decrease in body size (purple pathway). A large genome size may be associated with a lower thermal sensitivity of development. Consequently, development does not outpace growth under warmer conditions and the faster growth results in larger body sizes (green pathway). Due to the strong linkage between genome size and cell size, both mechanisms will operate in tandem, but the relative importance of these mechanisms may differ among animals, depending on their characteristics.

Fig 5

Schematic overview of different temperature‐size (T–S) responses in relation to voltinism. T–S responses may depend on the interaction between the length of the growing season (green box) and the development time (brown arrow), especially in (terrestrial) organisms living in habitats with strong end‐of season constraints. For univoltine species, warming may allow animals to grow faster during their (fixed) development time, resulting in animals reaching a larger size (A), unless time for development is also reduced under warmer conditions (B). Warming may also allow animals to fit more generations into a certain amount of time, either by increasing the number of generations (C; multivoltine species) or by decreasing the number of years needed for completion (D; semivoltine species). A faster development can result in animals growing to a smaller size under warmer conditions when viewed across the whole thermal gradient (dashed black line). However, shifts in voltinism may result in a sawtooth pattern, with animals growing to a larger size with warming (solid black line), until there is an increase in voltinism at which point animals reach a smaller size (due to less time available for growth in a given generation, dotted grey line). Such shifts in voltinism and the resulting sawtooth patterns are most readily seen in latitudinal clines.