Experimental evidence of gradual size-dependent shifts in body size and growth of fish in response to warming.

Magnus Huss,Renee M Van Dorst,Anna Gårdmark,Philip Jacobson,Max Lindmark

doi:10.1111/gcb.14637

Abstract

A challenge facing ecologists trying to predict responses to climate change is the few recent analogous conditions to use for comparison. For example, negative relationships between ectotherm body size and temperature are common both across natural thermal gradients and in small‐scale experiments. However, it is unknown if short‐term body size responses are representative of long‐term responses. Moreover, to understand population responses to warming, we must recognize that individual responses to temperature may vary over ontogeny. To enable predictions of how climate warming may affect natural populations, we therefore ask how body size and growth may shift in response to increased temperature over life history, and whether short‐ and long‐term growth responses differ. We addressed these questions using a unique setup with multidecadal artificial heating of an enclosed coastal bay in the Baltic Sea and an adjacent reference area (both with unexploited populations), using before‐after control‐impact paired time‐series analyses. We assembled individual growth trajectories of ~13,000 unique individuals of Eurasian perch and found that body growth increased substantially after warming, but the extent depended on body size: Only among small‐bodied perch did growth increase with temperature. Moreover, the strength of this response gradually increased over the 24 year warming period. Our study offers a unique example of how warming can affect fish populations over multiple generations, resulting in gradual changes in body growth, varying as organisms develop. Although increased juvenile growth rates are in line with predictions of the temperature–size rule, the fact that a larger body size at age was maintained over life history contrasts to that same rule. Because the artificially heated area is a contemporary system mimicking a warmer sea, our findings can aid predictions of fish responses to further warming, taking into account that growth responses may vary both over an individual's life history and over time.

Highlights

There is a growing awareness that marine ecosystems and the services they provide are threatened by anthropogenic global climate change (Doney et al, 2012; IPCC, 2014, 2018)
Evidence is accumulating that one such common response to global warming is faster juvenile growth and/or developmental rates and smaller adult body sizes, referred to as the temperature–size rule (TSR) (Atkinson, 1994; Baudron, Needle, Rijnsdorp, & Marshall, 2014; Horne, Hirst, & Atkinson, 2017; Kingsolver & Huey, 2008; Ohlberger, 2013; Tseng et al, 2018)
Observations of declines in adult body size in warming environments are in agree‐ ment with long‐known temperature–size relationships in endotherms based on latitudinal gradients, both between species and between populations of the same species (James, 1970), with organisms generally being smaller in warmer regions (Torres‐Romero, Morales‐Castilla, & Olalla‐ Tárraga, 2016; but see Riemer, Guralnick, & White, 2018)

Summary

| INTRODUCTION

There is a growing awareness that marine ecosystems and the services they provide are threatened by anthropogenic global climate change (Doney et al, 2012; IPCC, 2014, 2018). Despite increasing evidence for size‐ and life stage‐specific re‐ sponses to rising temperatures (Daufresne et al, 2009; Gardner, Peters, Kearney, Joseph, & Heinsohn, 2011; Messmer et al, 2017), most current ecological theory (e.g., Binzer, Guill, Brose, & Rall, 2012; Vasseur & McCann, 2005) aiming to explain population responses to temperature variation is based on the assumption of size‐indepen‐ dent effects of warming (e.g., assuming no temperature dependence of allometric exponents of vital rates, such as metabolic rates; but see Lindmark, Huss, Ohlberger, & Gårdmark, 2018; Lindmark, Ohlberger, Huss, & Gårdmark, 2019; Ohlberger, Edeline, Vollestad, Stenseth, & Claessen, 2011) This may be a serious limitation given that life stage and body size have major influences on the physiology (e.g., Brown, Gillooly, Allen, Savage, & West, 2004) and ecological role of individu‐ als (e.g., Brose, 2010). This study offers a unique example of how warming can affect individual body growth and size‐at‐age over multiple generations in an artificially heated enclosed coastal eco‐ system relative to an adjacent reference area

| MATERIALS AND METHODS

Findings

| DISCUSSION