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Aquaculture Environment Interactions 10:267 See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/325162755 High pCO2 levels affect metabolic rate, but not feeding behavior and fitness of farmed giant mussel Choromytilus chorus Article in Aquaculture Environment Interactions · June 2018 DOI: 10.3354/aei00271 CITATION READS 1 195 7 authors, including: Samanta Benítez Nelson A Lagos University Santo Tomás (Chile) University Santo Tomás (Chile) 8 PUBLICATIONS 57 CITATIONS 75 PUBLICATIONS 1,361 CITATIONS SEE PROFILE SEE PROFILE Sebastian Jorge Osores Tania Opitz Universidad Adolfo Ibáñez Universidad Adolfo Ibáñez 9 PUBLICATIONS 53 CITATIONS 7 PUBLICATIONS 37 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Tidal Flat Ecology View project DIRECT AND INDIRECT EFFECTS OF ARTIFICIAL LIGHT POLLUTION ON A SANDY BEACH ARTHROPOD GUILD View project All content following this page was uploaded by Marco A Lardies on 26 June 2018. The user has requested enhancement of the downloaded file. Vol. 10: 267–278, 2018 AQUACULTURE ENVIRONMENT INTERACTIONS Published June 26 https://doi.org/10.3354/aei00271 Aquacult Environ Interact OPENPEN ACCESSCCESS High pCO2 levels affect metabolic rate, but not feeding behavior and fitness, of farmed giant mussel Choromytilus chorus Samanta Benítez1,2, Nelson A. Lagos1,2, Sebastián Osores3, Tania Opitz3, Cristian Duarte2,4, Jorge M. Navarro5, Marco A. Lardies2,3,* 1Centro de Investigación e Innovación para el Cambio Climático (CiiCC), Facultad de Ciencias, Universidad Santo Tomás, 837003 Santiago, Chile 2Center for the Study of Multiple-drivers on Marine Socio-ecological Systems (MUSELS), Universidad de Concepción, 4070386 Concepción, Chile 3Facultad de Artes Liberales, Universidad Adolfo Ibáñez, 7941169 Santiago, Chile 4Departamento de Ecología y Biodiversidad, Facultad de Ecología y Recursos Naturales, Universidad Andrés Bello, 8370035 Santiago, Chile 5Instituto de Ciencias Marinas y Limnológicas & Centro Fondap de Investigación de Ecosistemas Marinos de Altas Latitudes (IDEAL), Universidad Austral de Chile, 5110566 Valdivia, Chile ABSTRACT: Benthic habitats such as intertidal areas, sandy or rocky shores, upwelling zones, and estuaries are characterized by variable environmental conditions. This high variability of environ- mental stressors such as temperature, salinity, and pH/pCO2 levels have been shown to impose restrictions on organismal performance. The giant mussel Choromytilus chorus forms intertidal and subtidal mussel beds in estuarine zones associated with fjords occurring in southern Chile and is an important aquacultural resource in Patagonia. In this study, we estimated the sensitivity of physiological traits and energy balance of C. chorus juveniles exposed to 3 pCO2 treatments (500, 750, and 1200 µatm) for 30 d. Results showed that in acidified, high pCO2 conditions, C. chorus juveniles had increased metabolic rates; however, other physiological traits (clearance and inges- tion rates, ammonia excretion, absorption efficiency, growth rate, biomass production, net calcifi- cation, and dissolution rates) were not affected. These results suggest that when subjected to acid- ification, the adaptive response of C. chorus triggers tradeoffs among physiological traits that favor sustained feeding and growth in order to combat increased metabolic stress. As has been reported for other marine organisms, chronic exposure to variable pH/pCO2 in their native habi- tats, such as estuarine zones, could explain the differential acclimatization capacity of giant mus- sels to cope with the increase in pCO2. Additionally, the fact that the mussels did not suffer from mortality indicates that increased pCO2 levels may have chronic, but not lethal, effects on this spe- cies under these experimental conditions. KEY WORDS: Estuaries · pH · Physiological traits · Acclimation · Phenotypic plasticity · Aquaculture INTRODUCTION by the ocean (Sabine et al. 2004), triggering a chem- ical process called ocean acidification (OA) (Caldeira The increasing concentration of carbon dioxide & Wickett 2003, Orr et al. 2005, Gattuso et al. 2015), a (CO2) in the atmosphere has caused major changes global stressor with widespread consequences for in the global climatic system. Nearly one-third of calcifying organisms (Cooley & Doney 2009, Nien- total anthropogenic CO2 emission has been absorbed huis et al. 2010). Due to the long-term projected © The authors 2018. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are unrestricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 268 Aquacult Environ Interact 10: 267–278, 2018 changes in carbonate system parameters (pCO2, pH, specific (Miller et al. 2009, Wang et al. 2015, Vargas alkalinity, etc.) in the ocean and the differences in et al. 2017), and strongly dependent on the environ- temporal scales operating over populations and mental variability experienced by species in their organisms, a description of organismal responses as local habitats (Osores et al. 2017). evidence of CO2-sensitivity of the se lected study Bivalves dominate the macrofauna of many estuar- models has recently been proposed, showing impacts ies and coastal environments and have been shown of OA on species abundance and distribution to play an important ecological role in benthic eco- (MacElhany 2017). Studies carried out with bivalve systems (Vihtakari et al. 2013, Duarte et al. 2015, species have shown clear CO2-sensitivity in several Gazeau et al. 2015, Osores et al. 2017). Additionally, physiological traits. For instance, higher pCO2 levels bivalves provide ecosystem services to aquaculture have been shown to negatively affect net calcifica- industries (Dame 2011, Lemasson et al. 2017). In tion rates (e.g. Mytilus chilensis; Duarte et al. 2015) Chile, ap proximately 60% of mussel production by increasing the dissolution rates of many calcifying occurs in northern Patagonia (Avendaño et al. 2017). organisms (Doney et al. 2009). Furthermore, high In this geographical zone, significant sequestration of pCO2 levels have been shown to alter the metabolic atmospheric pCO2 occurs in the surface seawater, rate and growth of M. galloprovincialis (e.g. Michae- and precipitation introduces acidic freshwater to the lidis et al. 2005) and M. chilensis (e.g. Navarro et al. fjord ecosystems (Torres et al. 2011, Vargas et al. 2016). Similarly, OA has been shown to negatively 2018). As such, these areas are vulnerable to pro- affect the feeding rates of M. chilensis (e.g. Navarro gressive acidification, which could potentially impact et al. 2013) and physiological traits and the health of the structure and function of the Patagonian ecosys- M. edulis (Beesley et al. 2008, Thomsen et al. 2013). tem, as well as the aquacultural activities performed Despite this, it has been proposed that species inhab- there (Navarro et al. 2013). iting environments where naturally increased pCO2 Recent studies performed in southern Chile have levels occur regularly (i.e. lower pH or more acidic focused on the physiological responses of cultured conditions) should be better adapted to cope with M. chilensis when exposed to high pCO2 conditions future ocean acidification (Thomsen et al. 2013, (Navarro et al. 2013, 2016, Duarte et al. 2014, 2015, Lardies et al. 2014, Duarte et al. 2014, 2015). For Osores et al. 2017). However, less effort has been example, Fernández-Reiriz et al. (2012) reported no made to determine the effects of elevated pCO2 on apparent change in clearance, ingestion, and respi- the giant mussel Choromytilus chorus. This species ration rates of juvenile M. galloprovincialis from forms dense mussel beds in subtidal and intertidal highly alkaline coastal waters and exposed to in- habitats (Barria et al. 2012) and is distributed from creased pCO2 levels. Furthermore, Thomsen et al. Callao (Peru) to the Strait of Magellan and the Beagle (2013) showed that M. edulis may be able to cope channel in southern Chile (Bellolio et al. 1996). Along with high pCO2 levels when food supply is ensured. this wide distributional range, C. chorus inhabits In addition, it has recently been demonstrated that coastal areas subject to variable marine and estuar- some of the above effects of OA may be modified by ine conditions (Navarro 1988), the mixing of which concurrent exposure to other stressors, such as regulates the pH and carbonate saturation state in changes in salinity (Freitas et al. 2017), reduced food these ecosystems (see Duarte et al. 2013). Despite supply (Thomsen et al. 2013, Ramajo et al. 2016), and being an important commercial species in Chile, in warming (Harvey et al. 2013, Lagos et al. 2016). In which production increased from 339 t of biomass general, these studies suggest that exposure to a in 2012 to 2090 t in 2014 (SERNAPESCA 2014), wide range of environmental conditions and natu- the pCO2 sensitivity of the physiological traits and rally high and variable pH/pCO2 conditions (Thom- energy balance of C. chorus have not been ad - sen et al. 2013, Duarte et al. 2015) explain the vari- dressed. Previous studies carried out with C. chorus ability and even neutral responses of species to have mainly focused on farming (Avendaño et al. experimental pCO2 manipulations (Vargas et al. 2017), feeding behavior (e.g. Ibarrola et al. 2012), 2017). Thus, it has been proposed that the species accumulation of toxic compounds
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