Optimum growth temperature declines with body size within fish species

Abstract

According to the temperature-size rule, warming of aquatic ecosystems is generally predicted to increase individual growth rates but reduce asymptotic body sizes of ectotherms. However, we lack a comprehensive understanding of how growth and key processes affecting it, such as consumption and metabolism, depend on both temperature and body mass within species. This limits our ability to inform growth models, link experimental data to observed growth patterns, and advance mechanistic food web models. To examine the combined effects of body size and temperature on individual growth, as well as the link between maximum consumption, metabolism and body growth, we conducted a systematic review and compiled experimental data on fishes from 59 studies that combined body mass and temperature treatments. By fitting hierarchical models accounting for variation between species, we estimated how these three processes scale jointly with temperature and body mass within species. We found that whole-organism maximum consumption increases more slowly with body mass than metabolism, and is unimodal over the full temperature range, which leads to the prediction that optimum growth temperatures decline with body size. Using an independent dataset, we confirmed this negative relationship between optimum growth temperature and size within fish species. Small individuals may therefore exhibit increased growth with initial warming, whereas larger conspecifics could be the first to experience negative impacts of warming on growth. These findings help advance mechanistic models of individual growth and food web dynamics and improve our understanding of how climate warming affects the growth and size structure of aquatic ectotherms.Significance statementPredicting organism responses to a warming climate requires understanding how physiological processes such as feeding, metabolism, and growth depend on body size and temperature. Common growth models predict declining optimum growth temperatures with body size if energetic costs (metabolism) increase faster than gains (feeding) with body size. However, the generality of these features has not been evaluated at the within-species level. By collating data on fish through a systematic literature review, we find support for both declining net energy gain and declining optimum growth temperatures with body size. This implies large individuals within populations may be the first to suffer poor growth due to warming, with consequences for fisheries yield and food web structure in warmer climates.

Effects of Warming on Intraguild Predator Communities with Ontogenetic Diet Shifts

“…The temperature effect described above does not depend on body size, and therefore increases the rates uniformly across life stages and species. However, temperature can affect intraspecific energetic efficiency by reducing the increase in intake rate with size more than for maintenance (Fonds et al 1992, Lindmark et al 2021. This results in warming induced relative declines in the energetic efficiency of large individuals within a population and is in line with the observation that optimum growth temperature declines with size (Björnsson et al 2007, Morita et al 2010, Lindmark et al 2021.…”

“…However, temperature can affect intraspecific energetic efficiency by reducing the increase in intake rate with size more than for maintenance (Fonds et al 1992, Lindmark et al 2021. This results in warming induced relative declines in the energetic efficiency of large individuals within a population and is in line with the observation that optimum growth temperature declines with size (Björnsson et al 2007, Morita et al 2010, Lindmark et al 2021. We implement a simplistic size-dependent temperature effect by adding a linear scalar of temperature on the maximum intake rate of adult predators that decreases their intake in relation to that of juveniles and consumers (Supplement S1).…”

“…the ratio between consumption and metabolic rates, Vucic-Pestic et al 2011) matters for predictions on community responses to warming (Vasseur and McCann 2005, Fussmann et al 2014, Uszko et al 2017). Most such predictions, however, stem from models without intraspecific variation in life stage or body size and therefore ignore that optimum growth temperatures within species often decline with size (Björnsson et al 2007, Morita et al 2010, Lindmark et al 2021. Size-dependent declines in energetic efficiency and growth in warmer environments could modify the relative efficiency of different life stages to produce biomass, which affects the strength of species interactions.…”

Temperature impacts on fish physiology and resource abundance lead to faster growth but smaller fish sizes and yields under warming

“…As activation energies vary substantially between processes, species and taxonomic groups and are estimated with uncertainty, we parameterized 200 projections of the food web model using randomly sampled activation energies from normal distributions with rate-specific means and standard deviations. For metabolism and maximum consumption, we acquired means and standard deviations from the posterior distributions in (Lindmark et al 2021) (note we assume search volume scales identically as maximum consumption and mortality as metabolism). The normal distributions describing activation energies for background resource parameters were defined by a mean equal to the point estimate from a linear regression of natural log of growth rate as a function of Arrhenius temperature (1/ [eV "# ]) from experimental data in Savage et al (2004) (pooling protists, algae and zooplankton, extracted using the software WebPlotDigitizer v. 4.1 (Rohatgi 2012)).…”

“…This could reduce generality of predictions and increased challenges in parameterizing models of data poor systems. We approached this by applying random parameterization, rather than fixed values of temperature dependence, by sampling parameters from distributions based on estimates of activation energies of physiological rates in the literature (Lindmark et al 2021), to capture the uncertainty in these parameters. This approach revealed that in terms of body growth and mean body size in populations, the combination of activation energies can determine whether the mean size increases or decreases with warming, and at what age body sizes decline relative to the current temperatures (degree of decline in size-at-age).…”