Elsevier

Journal of Sea Research

Volume 90, July 2014, Pages 127-134
Journal of Sea Research

Differential response to ocean acidification in physiological traits of Concholepas concholepas populations

https://doi.org/10.1016/j.seares.2014.03.010Get rights and content

Highlights

  • We examined geographic variation in carbonate system parameters in snail phenotype.

  • We model the reaction norm of physiological traits using a mesocosm approach.

  • Elevated pCO2 increase metabolic rates in both populations of the snail juveniles.

  • Snails of southern population in high-pCO2 have a lesser expression of a HSP70.

  • Ocean acidification has a negative effect on organism functioning of juvenile snails.

Abstract

Phenotypic adaptation to environmental fluctuations frequently occurs by preexisting plasticity and its role as a major component of variation in physiological diversity is being widely recognized. Few studies have considered the change in phenotypic flexibility among geographic populations in marine calcifiers to ocean acidification projections, despite the fact that this type of study provides understanding about how the organism may respond to this chemical change in the ocean. We examined the geographic variation in CO2 seawater concentrations in the phenotype and in the reaction norm of physiological traits using a laboratory mesocosm approach with short-term acclimation in two contrasting populations (Antofagasta and Calfuco) of the intertidal snail Concholepas concholepas. Our results show that elevated pCO2 conditions increase standard metabolic rates in both populations of the snail juveniles, likely due to the higher energy cost of homeostasis. Juveniles of C. concholepas in the Calfuco (southern) population showed a lower increment of metabolic rate in high-pCO2 environments concordant with a lesser gene expression of a heat shock protein with respect to the Antofagasta (northern) population. Combined these results indicate a negative effect of ocean acidification on whole-organism functioning of C. concholepas. Finally, the significant Population × pCO2 level interaction in both studied traits indicates that there is variation between populations in response to high-pCO2 conditions.

Introduction

Phenotypic acclimatization to short-term environmental fluctuations should frequently occur by preexisting plasticity and underlying standing genetic variation (see Lande, 2009). Phenotypic flexibility is a particular kind of phenotypic plasticity and is defined as the possible selective advantage of those individuals that can show continuous but reversible changes in behavior, physiology and morphology in response to rapidly changing environmental conditions in timescales shorter than a lifetime (Piersma and Drent, 2003). Paleoclimate data provided evidence that wild populations rarely experienced such huge and rapid changes in environmental variables such as temperature, salinity or pH (Caldeira and Wickett, 2005, Hönisch et al., 2012). For instance, paleoclimate evidence about global warming and ocean acidification (OA) event over the past 300 MY suggest similarities with contemporaneous extinction and evolutionary turnover. However, none of these past events parallels the rapidity of the current increase of CO2 release and chemical changes in seawater (Hönisch et al., 2012). Thus, rapid evolution of phenotypic plasticity may be necessary to prevent extinction of species subjected to sudden environmental changes such as the present event of anthropogenic OA. This may be especially threatening to calcifying organisms, given that effects on calcification may delay developmental rates at critical early life stages and could restrict opportunities in many species for larval dispersal and/or changes in geographical range (Fabry et al., 2008, Kroeker et al., 2010).

Many morphological, life-history, and metabolic traits show signs of phenotypic flexibility (Lardies et al., 2011, Pigliucci and Preston, 2004). Furthermore, geographic variations in life-history and metabolic traits among populations are ubiquitous among ectotherms (see Gilchrist and Huey, 2004, Lardies et al., 2011). Physiological variation within the life history of an individual can have profound implications for fitness (Lardies and Bozinovic, 2006, Ricklefs and Wikelski, 2002), since physiological maintenance costs are a large component of animal energy budgets (Angilletta, 2009, Sibly and Calow, 1986). Different effects of the environment on the phenotype of different populations result in variation in reaction norms and a significant population (genotype) × environment interaction (Pigliucci, 2005). Genotype × environment interactions are the type of genetic variation required for the evolution of phenotypic flexibility (Lardies and Bozinovic, 2008, Via and Lande, 1985). The significance of phenotypic plasticity as a major component of geographic variation of biological responses among populations is now being widely recognized, as a consequence, it became one of the main topics in physiological studies (e.g. Angilletta, 2009, Piersma and Gils, 2011) and are particularly relevant in the perspective of elucidating how physiological differences among organisms may affect their responses to ocean acidification, with cascading ecological consequences (Chown and Gaston, 2008, Helmuth et al., 2005). Unfortunately, few studies have considered the variations in phenotypic flexibility among geographic populations of marine calcifying organisms in response to OA.

It is believed that OA levels projected for the near future will have an impact on every level of organization of biological systems: from molecular to ecosystemic (Fabry et al., 2008, Byrne, 2011). One of the molecular responses that are activated in a cell under temperature or acidification stress is the heat shock proteins response (HsP), an event of genetic activation that occurs in the cells in response to abnormal stressful temperatures or acidosis (Cummings et al., 2011, Hofmann, 2005). The genes that encode for Heat-Shock Proteins (HsPs) are highly conserved and have been found in all studied species (Feder and Hofmann, 1999). Among HsP families the group in the 70-kDa size range (HsP70) is the most extensively studied because of its prominent response to stresses (see reviews in Feder and Hofmann, 1999). The phenotypic expression of these protein patterns could explain not only differences in fitness but also the geographical distribution of the organisms (Hofmann and Todgham, 2010, Sorte and Hofmann, 2005). Recent studies in natural systems have shown that the patterns of expression in HsPs exhibit phenotypic flexibility related to the thermal history (Arias et al., 2011, Hammond and Hofmann, 2010). However, the patterns of expression of HsPs to different natural scenarios of pCO2 are practically unknown, only recent evidence showed that sea urchin larvae reared under elevated CO2 displayed compromised expression of HsP70 (see O’Donnell et al., 2009). Furthermore, the synthesis, degradation and replacement of these proteins imply an increase in energetic costs to the organism (Hartl and Hayer-Hartl, 2002, Sorensen and Loeschcke, 2002). Therefore, the pCO2 levels experienced by different populations, in their respective marine habitats, could condition trade-offs between traits or constraint of HsP expressions. Furthermore, phenotypic plasticity during development may provide a temporary response from this stress or there is a potential for further adaptation to changing ocean chemistry (Hofmann and Todgham, 2010).

In this study, we examined the effects of pCO2 variation on metabolic rate and in the expression of a gene belonging to the HSP70 family in a marine snail, the carnivorous gastropod C. concholepas (Brugière 1789), which is an economically and ecologically important component of the rocky intertidal and sub-tidal communities along the Chilean coast (Castilla, 1999). C. concholepas, has a shell with variable proportion of carbonate phases along the ontogeny: in juvenile stages calcite dominate (ca. 75%) over aragonite (ca. 25%), and the proportion of aragonite increased larval and post-settlement stages (Ramajo et al., 2013). Due to the broad geographic distribution of C. concholepas, it has been subjected to use in ecological and evolutionary research (i.e. Cardenas et al., 2009, Manríquez et al., 2009, Manríquez et al., 2012, Poulin et al., 2002). However, we are not aware of any study examining physiological trait plasticity among populations under projected pCO2 scenarios. Our study had the following two objectives: (1) to evaluate, experimentally, the effect of different pCO2 concentrations in seawater on oxygen consumption and expression of a stress related gene in juveniles of C. concholepas; and (2) to evaluate geographic variation in environmental variables (carbonate system parameters) as a source of variation in phenotype (phenotypic flexibility) and in the reaction norm.

Section snippets

Study sites and animals

Two regions along the coast of Chile were selected with inherent differences in physical and chemical properties of seawater (Fig. 1a). In Chile, sea surface temperature decreases from north to south with clear seasonal variability between regions: (i) Northern (23°38′S), has shown an annual average mean temperature of 17.03 °C ± 1.23 SD (Lagos et al., 2008), while (ii) Southern (39°42′S) has shown an average mean temperature of 11.2 °C ± 1.10 SD (Manríquez et al., 2012). Fluctuations in sea surface

Metabolic rate

Oxygen consumption was higher in the high-pCO2 condition but also was affected significantly by the population source (Fig. 2 and Table 3). A significant P × pCO2 interaction contributed to the observed variance for metabolic rate (Fig. 2) (Two-way ANCOVA, F1,52 = 4.20; P = 0.046). This interaction was evident from the intersecting reaction norms of the analyzed trait (Fig. 2). Mass-specific metabolic rate in juveniles of C. concholepas was significantly lower in the Calfuco population than in

Discussion

Our results show that elevated pCO2 concentrations in seawater resulted in higher standard metabolic rates and HsP70 family related gene expression in juvenile snails, likely due to the higher energy cost of homeostasis. In general terms, the observed reaction norm in C. concholepas metabolism when exposed to increased pCO2 levels were steep for the Antofagasta (northern) population and almost flat for Calfuco (southern) population. Since the deviation from the flat line parallel to the

Acknowledgments

This research was funded by Anillo Project ACT-132, FONDECYT 1090624, and Millennium Nucleus Project NC 1200286 "Center for the study of multiple-drivers on marine socio-ecological systems (MUSELS) from the Ministerio de Economia, Fomento y Turismo. MJ Poupin is supported by FONDECYT 11121306. This study complies with the current Chilean legislation regarding the collection and treatment of invertebrates.

References (74)

  • J.F. Ternon et al.

    A seasonal tropical sink for atmospheric CO2 in the Atlantic Ocean: the role of the Amazon River discharge

    Mar. Chem.

    (2000)
  • R. Torres et al.

    CO2 outgassing off Central Chile (31-30S) and northern Chile (24-23S) during austral summer 1997: The effect of wind intensity on the upwelling and ventilation of CO2-rich waters

    Deep-Sea Res. I

    (2002)
  • V. Amaral et al.

    The proteomes of Sydney rock oysters vary spatially according to exposure to acid sulfate runoff

    Mar. Freshw. Res.

    (2012)
  • M. Angilletta

    Thermal adaptation: a theoretical and empirical synthesis

    (2009)
  • M.B. Arias et al.

    Plasticity of life-cycle, physiological thermal traits and Hsp70 gene expression in an insect along the ontogeny: effect of temperature variability

    J. Therm. Biol.

    (2011)
  • E. Beniash et al.

    Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica

    Mar. Ecol. Prog. Ser.

    (2010)
  • A.M. Bronikowski et al.

    The evolutionary ecology of life history variation in the garter snake Thamnophis elegans

    Ecology

    (1999)
  • M. Byrne

    Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean

    Ocean Mar. Biol. Annu Rev.

    (2011)
  • K. Caldeira et al.

    Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean

    J. Geophys. Res.

    (2005)
  • P. Calosi et al.

    Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system

    Philos. Trans. R. Soc. Lond. B

    (2013)
  • L. Cardenas et al.

    A phylogeographical analysis across three biogeographical provinces of the south-eastern Pacific: the case of the marine gastropod Concholepas concholepas

    J. Biogeogr.

    (2009)
  • S. Chown et al.

    Macrophysiology for a changing world

    Proc. R. Soc. Lond. B

    (2008)
  • C.M. Crain et al.

    Interactive and cumulative effects of multiple human stressors in marine systems

    Ecol. Lett.

    (2008)
  • V. Cummings et al.

    Ocean Acidification at high latitudes: potential effects on functioning of the Antarctic bivalve Laternula elliptica

    PLoS ONE

    (2011)
  • C.M. Duarte et al.

    Is ocean acidification an open-syndrome? Undestanding anthropogenic impacts on seawater pH

    Estuar. Coasts

    (2013)
  • S. Dupont et al.

    Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis

    Mar. Biol.

    (2012)
  • V. Fabry et al.

    Impacts of ocean acidification on marine fauna and ecosystem processes

    ICES J. Mar. Sci.

    (2008)
  • M.E. Feder et al.

    Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology

    Annu. Rev. Physiol.

    (1999)
  • A.U. Form et al.

    Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophela pertusa

    Glob. Chang. Biol.

    (2012)
  • J.D. Fry

    The mixed-model analysis of variance applied to quantitative genetics: biological meaning of the parameters

    Evolution

    (1992)
  • G.W. Gilchrist et al.

    Plastic and genetic variation in wing loading as a function of temperature within and among parallel clines in Drosophila subobscura

    Integr. Comp. Biol.

    (2004)
  • L.M. Hammond et al.

    Thermal tolerance of Strongylocentrotus purpuratus early life history stages: mortality, stress-induced gene expression and biogeographic patterns

    Mar. Biol.

    (2010)
  • F.U. Hartl et al.

    Molecular chaperones in the cytosol: from nascent chain to folded protein

    Science

    (2002)
  • B. Helmuth et al.

    Biophysics, physiological ecology, and climate change: does mechanism matter?

    Annu. Rev. Physiol.

    (2005)
  • G.E. Hofmann

    Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales

    Integr. Comp. Biol.

    (2005)
  • G.E. Hofmann et al.

    Living in the now: physiological mechanisms to tolerate a rapidly changing environment

    Annu. Rev. Physiol.

    (2010)
  • G.E. Hofmann et al.

    High-frequency dynamics of ocean pH: a multi-ecosystem comparison

    PLoS ONE

    (2011)
  • Cited by (0)

    1

    Present address: Laboratorio de Ecología y Conducta de la Ontogenia Temprana (LECOT), Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, Chile.

    View full text