Evaluating the influences of temperature, primary production, and evolutionary history on bivalve growth rates

James Saulsbury,David Goodwin,David K Moss,Michał Kowalewski,Linda C Ivany,Peter D Roopnarine,Seth Finnegan,James F Gillooly,Noel A Heim,David R Lindberg,Craig R Mcclain,Jonathan L Payne,Bernd R Schöne

doi:10.1017/pab.2019.20

Abstract

AbstractOrganismal metabolic rates reflect the interaction of environmental and physiological factors. Thus, calcifying organisms that record growth history can provide insight into both the ancient environments in which they lived and their own physiology and life history. However, interpreting them requires understanding which environmental factors have the greatest influence on growth rate and the extent to which evolutionary history constrains growth rates across lineages. We integrated satellite measurements of sea-surface temperature and chlorophyll-a concentration with a database of growth coefficients, body sizes, and life spans for 692 populations of living marine bivalves in 195 species, set within the context of a new maximum-likelihood phylogeny of bivalves. We find that environmental predictors overall explain only a small proportion of variation in growth coefficient across all species; temperature is a better predictor of growth coefficient than food supply, and growth coefficient is somewhat more variable at higher summer temperatures. Growth coefficients exhibit moderate phylogenetic signal, and taxonomic membership is a stronger predictor of growth coefficient than any environmental predictor, but phylogenetic inertia cannot fully explain the disjunction between our findings and the extensive body of work demonstrating strong environmental control on growth rates within taxa. Accounting for evolutionary history is critical when considering shells as historical archives. The weak relationship between variation in food supply and variation in growth coefficient in our data set is inconsistent with the hypothesis that the increase in mean body size through the Phanerozoic was driven by increasing productivity enabling faster growth rates.

Highlights

Several lines of evidence suggest that the mean energy requirements and metabolic rates of metazoans have generally increased through time (Bambach 1993; Payne and Finnegan 2006; Finnegan et al 2011; Payne et al 2014; Smith et al 2016)
Excluding non–suspension feeding bivalves has a negligible effect on the strength of the predictors under study, including chlorophyll-a concentration (Supplementary Table S2)
Fossilized growth rates are one of the best and most widely available proxies for studying the history and evolution of metabolic rates, though they have rarely been used for this purpose

Summary

Introduction

Several lines of evidence suggest that the mean energy requirements and metabolic rates of metazoans have generally increased through time (Bambach 1993; Payne and Finnegan 2006; Finnegan et al 2011; Payne et al 2014; Smith et al 2016). Extrinsic (environmental) drivers have been invoked to explain this long-term trend (Bambach 1993; Vermeij 1995; Bush and Bambach 2011; Klompmaker et al 2017), but no consensus view has yet emerged This is due, in part, to the inherent limitations of studying fossil organisms: in most cases metabolic rates must be inferred from a combination of bodymass estimates, independent estimates of important environmental parameters, and physiological inferences from comparison with extant relatives (Finnegan et al 2011; Payne et al 2014; Heim et al 2015; Strotz et al 2018). These organisms commonly preserve their ontogenetic histories as seasonal variation in the physical properties and/or isotopic composition of accreted skeletal material (Jones and Quitmyer 1996) and can provide a detailed record of individual growth rate through time and ultimate longevity

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Conclusion