Smaller adult fish size in warmer water is not explained by elevated metabolism

Abstract

Fish and other ectotherms living in warmer waters often grow faster as juveniles, mature earlier, but become smaller adults. Known as the temperature-size rule (TSR), this pattern is commonly attributed to higher metabolism in warmer waters, leaving fewer resources for growth. An alternative explanation focuses on growth and reproduction trade-offs across temperatures. We tested these hypotheses by measuring growth, maturation, metabolism and reproductive allocation from zebrafish populations kept at 26 and 30°C across six generations. Zebrafish growth and maturation followed TSR expectations but were not explained by baseline metabolic rate, which converged between temperature treatments after a few generations. Rather, we found that females at 30°C allocated more to reproduction, especially when maturing at the smallest sizes. We show that elevated temperatures do not necessarily increase baseline metabolism if sufficient acclimation is allowed and call for an urgent revision of modelling assumptions used to predict population and ecosystem responses to warming.

Larger but younger fish when growth outpaces mortality in heated ecosystem

“…This result was unexpected for two reasons: optimum growth temperatures generally decline with body size within species under food satiation in experimental studies (Lindmark et al . 2022), and fish tend to mature at smaller body size and allocate more energy into reproduction as it gets warmer (Wootton et al . 2022).…”

“…Size-at-age is generally predicted to increase with warming for small individuals, but decrease for large individuals according to the mentioned TSR (Atkinson 1994; Ohlberger 2013). Several factors likely contribute to this pattern, such as increased allocation to reproduction (Wootton et al . 2022) and larger individuals in fish populations having optimum growth rates at lower temperatures (Lindmark et al .…”

Changes in benthic and pelagic production interact with warming to drive responses to climate change in a temperate coastal ecosystem

“…A number of experimental and modelling studies have reported that warming waters will lead to smaller fish (Daufresne et al 2009, Cheung et al 2013, Pauly and Cheung 2018). At an intraspecific level this is believed to be driven by the thermal dependence of physiological processes (Angilletta Jr et al 2004, Brown et al 2004, Forster et al 2011), although the exact mechanisms remain debated (Pauly and Cheung 2018, Audzijonyte et al 2019a, Wootton et al 2022). In contrast our study reports that physiological responses to warming generally increased, rather than decreased, mean species body sizes.…”

“…Some degree of growth-reproduction trade-off does occur in size-based models, because growth and therefore maturation (set to occur over some size range) are not set, but are emergent model properties (Andersen et al 2007). Recent inter-generational experiments show that some populations may be capable of complete metabolic acclimation to higher temperatures, and that changes in growth and size may be largely driven by reproductive decisions (Wootton et al 2022). Future studies should explore more direct impacts of temperature on these trade-offs by allowing decreasing maturation sizes, consistent with TSR observations and different reproductive allocation curves.…”

“…All rates were assumed to increase exponentially with temperature based on Arrhenius temperature correction factor where A r is the activation energy [eV] for individual rate r here assumed to be 0.63, T is temperature [K], T ref is the reference temperature where temperature scaling equals 1 (here assumed to be 12°C or here 285.27 K), and κ is Boltzmann’s constant in eV K -1 ( 8.617 × 10 -5 eV K -1 ). This representation of temperature is a simplification (see Discussion), and likely does not reflect inter-generational population physiological responses (Denderen et al 2020, Wootton et al 2022). Yet, it allows consistent comparison with other models exploring climate change effects (Blanchard et al 2012, Bryndum-Buchholz et al 2019, Heneghan et al 2021a), results in a tractable number of simulations for ANOVA-type analyses, and, in a manageable way, addresses relative importance of internal, physiological versus external, community driven, responses to warming.…”