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Argopecten Purpuratus) to Isolated and Combined Environmental Drivers of Coastal Upwelling

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Argopecten Purpuratus) to Isolated and Combined Environmental Drivers of Coastal Upwelling ICES Journal of Marine Science (2019), 76(6), 1836–1849. doi:10.1093/icesjms/fsz080 Downloaded from https://academic.oup.com/icesjms/article-abstract/76/6/1836/5487735 by Universidad Adolfo Ibanez user on 02 January 2020 Original Article Physiological responses of juvenile Chilean scallops (Argopecten purpuratus) to isolated and combined environmental drivers of coastal upwelling Laura Ramajo 1,2,3,4*, Carolina Ferna´ndez1,3, Yolanda Nu´nez~ 5, Paz Caballero2, Marco A. Lardies1,3, and Marı´a Josefina Poupin6,7 1Departamento de Ciencias, Facultad de Artes Liberales, Universidad Adolfo Iba´~nez, Avenida Diagonal Las Torres 2640, Pe~nalole´n, Santiago, Chile 2Centro de Estudios Avanzados en Zonas A´ridas, Avenida Ossando´n 877, Coquimbo, Chile 3Center for the Study of Multiple-drivers on Marine Socio-Ecological Systems (MUSELS), Universidad de Concepcio´n, Chile 4Centro de Investigacio´n e Innovacio´n para el Cambio Clima´tico (CiiCC), Avenida Eje´rcito 146, Santiago, Chile 5Facultad de Ciencias Biolo´gicas, Pontificia Universidad de Chile (PUC), Av Libertador Bernardo O’Higgins 340, Santiago, Chile 6Laboratorio de Bioingenierı´a, Facultad de Ingenierı´a and Ciencias, Universidad Adolfo Iba´~nez, Avenida Diagonal Las Torres 2640, Pe~nalole´n, Santiago, Chile 7Center of Applied Ecology and Sustainability (CAPES), Av Libertador Bernardo O’Higgins 340, Santiago, Chile *Corresponding author: tel: þ 56 51 2673259; e-mail: [email protected]. Ramajo, L., Ferna´ndez, C., Nu´nez,~ Y., Caballero, P., Lardies, M. A., and Poupin, M. J. Physiological responses of juvenile Chilean scallops (Argopecten purpuratus) to isolated and combined environmental drivers of coastal upwelling. – ICES Journal of Marine Science, 76: 1836–1849. Received 16 November 2018; revised 13 March 2019; accepted 1 April 2019; advance access publication 10 May 2019. Coastal biota is exposed to continuous environmental variability as a consequence of natural and anthropogenic processes. Responding to heterogeneous conditions requires the presence of physiological strategies to cope with the environment. Ecosystems influenced by upwelling endure naturally cold, acidic and hypoxic conditions, nevertheless they sustain major fisheries worldwide. This suggests that species inhabiting upwelling habitats possess physiological adaptations to handle high environmental variability. Here, we assessed the impact of the main up- welling drivers (temperature, pH and oxygen) in isolation and combined on eco-physiological responses of Chilean scallop Argopecten purpur- atus. A. purpuratus responded to hypoxia by increasing their metabolic performance to maintain growth and calcification. Calcification was only affected by pH and increased under acidic conditions. Further, A. purpuratus juveniles prioritized calcification at the expense of growth under upwelling conditions. Increasing temperature had a significant impact by enhancing the physiological performance of A. purpuratus juveniles independently of oxygen and pH conditions, but this was associated with earlier and higher mortalities. Our results suggest that A. purpuratus is acclimated to short-term colder, acidic and hypoxic conditions, and provide important information of how this species responds to the heterogeneous environment of upwelling, which is significantly relevant in the climatic context of upwelling intensification. Keywords: environmental drivers, environmental heterogeneity, global change, metabolism, multi-stressor, physiology, tolerance, upwelling Introduction drivers that impact a large number of eco-physiological processes Coastal oceans experience elevated environmental variability in (Lachkar, 2014; Gunderson et al., 2016). In particular, coastal temperature, pH, salinity, oxygen, food supply, and nutrients areas impacted by permanent (or seasonal) upwelling are sub- conditions (Duarte et al., 2013). Consequently, resident biota of jected to a high variability as a consequence of the biogeochemi- coastal habitats face a combination of multiple environmental cal properties of upwelled waters. Deeper upwelled waters are VC International Council for the Exploration of the Sea 2019. All rights reserved. For permissions, please email: [email protected] Scallop physiology under upwelling drivers 1837 colder and present lower oxygen saturations (hypoxic/anoxic extremely relevant in upwelling systems, especially because the fre- concentrations) and higher CO2 concentrations (acidic) in com- quency and intensity of upwellings are predicted to increase as a parison to surface coastal waters (Feely et al., 2004; Lachkar, consequence of changes in wind patterns due to the increase in at- 2014). Still, even under such physiologically stressful conditions, mospheric temperatures (Bakun 1990; Sydeman et al., 2014)orby upwelling ecosystems are highly productive and support the larg- poleward shifts in major atmospheric high-pressure Hadley cells est fisheries worldwide (Bakun, 1990). This makes upwelling eco- (Lu et al., 2007; Rykaczewski et al., 2015). Recent studies show an systems a particularly relevant interesting and valuable research increase in the duration and magnitude of upwelling events has al- Downloaded from https://academic.oup.com/icesjms/article-abstract/76/6/1836/5487735 by Universidad Adolfo Ibanez user on 02 January 2020 models to assess the biological strategies that evidence the toler- ready been reported for two of the major world upwelling systems, ance (and resistance) to multiple environmental drivers such as the Humboldt (HCS) and California Current Systems (Belkin, oxygen, pH, or temperature (Lagos et al., 2016; Ramajo, Marba´, 2009; Falvey and Garreaud, 2009; Lima and Wethey, 2012; Aravena et al., 2016). et al., 2014; Jacob et al., 2018). Consequently, the marine species Multiple studies, on a large amount of different marine species, currently living at upwelling-influenced habitats will be affected by have observed different levels of adaptation, resistance, and vulner- intensified environmental conditions in both, average and variance, ability to natural environmental conditions occurring in upwelling in pH, oxygen, and temperature conditions. These conditions will systems, river-influenced habitats, or CO2 vents ecosystems. be also exacerbated by intensified and more frequent El Nino–~ Coastal species (or populations) can be affected positive or nega- Southern Oscillation (ENSO) events (Cai et al., 2014). Hence, we tively by changes in the environmental conditions showing in- are facing an immediate requirement to understand which are the creased or decreased growth (Ramajo, Marba´, et al., 2016; Ramajo, physiological impacts and the biological mechanisms that coastal Prado, et al., 2016) and calcification rates (Heinemann et al., 2012; species show to counteract the current (and predicted) environ- Ramajo, Prado, et al., 2016). Also, some species present increased mental conditions of their habitats. metabolic rates or metabolic depression (Ramajo, Prado, et al., Argopecten purpuratus, the northern Chilean scallop, is one of 2016; Osores et al., 2017), changes in periostracum thickness the most important and successful marine resources cultured along (Ramajo, Marba´, et al., 2016; Ramajo, Prado, et al.,2016;Osoreset HCS. This species is a filter feeding bivalve inhabiting a geographic al., 2017), differential patterns in shell carbonate precipitation area ranging from Panama (10N) to northern-central Chile (Ramajo et al., 2015), oxidative stress (Bednarsek et al., 2018), (30S) (Avendano,~ 1993) which holds significant socio-economic decreased fertilization success (Boch et al., 2017), or even better go- importance along the Peruvian and Chilean coasts (Ya´nez~ et al., nadal development (Vilchis et al., 2005). These studies demonstrate 2017). In northern Chile, Tongoy Bay (30150S71340W) is the that the direction and the magnitude of the physiological impacts principal area where A. purpuratus is intensively cultured with due to the environmental variability are species-specific (Kroeker >3330 tons obtained in 2016 (SERNAPESCA, 2016). Tongoy Bay et al., 2013; Boch et al., 2017), but also evidence the existence (or is a closed bay influenced seasonally by one of the most important the absence) of physiological (i.e. up-metabolic regulation), miner- and active upwelling centres of the Chilean coast, Lengua de Vaca alogical (i.e. changes in organic periostracum composition), molec- Point (PLV, 30180S) (Strub et al., 1998; Figueroa and Moffat, ular responses [i.e. up-regulation of heat shock proteins and chitin 2000; Aravena et al., 2014). During spring–summer seasons, synthase (CHS)], or evolutionary mechanisms (i.e. higher pheno- favourable-upwelling winds generate the rise of deeper upwelled typic plasticity) that help to cope with environmental conditions waters that increase the variability in temperature (18–13C), pH such as low pH, hypoxia, or increasing temperatures (Cummings (8.1–7.6), and oxygen (7–0.5 mlLÀ1)(Torres et al., 1999; Torres et al., 2011; Hendriks et al., 2015; Ramajo, Marba´, et al., 2016; and Ampuero, 2009). In addition, ENSO enhances this variability Ramajo, Pe´rez-Leo´n, et al., 2016). Most of these studies concluded with important impacts on the A. purpuratus fishery (Mendo and that the display of these physiological and genetical mechanisms, as Wolff, 2003). well as the phenotypic plasticity expression, are a consequence of To date, several efforts have been made to improve and extend evolutionary processes such as acclimation or local adaption A. purpuratus fisheries
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