Biochemical alterations in native and exotic oyster species in Brazil in response to increasing temperature

Abstract

The increase of temperature in marine coastal ecosystems due to atmospheric greenhouse gas emissions is becoming an increasing threat for biodiversity worldwide, and may affect organisms' biochemical performance, often resulting in biogeographical shifts of species distribution. At the same time, the introduction of non-native species into aquatic systems also threatens biodiversity and ecosystem functions. Oysters are among the most valuable socio economic group of bivalve species in global fishery landings, and also provide numerous ecosystem services. However, the introduction of non-native oyster species, namely Crassostrea gigas for aquaculture purposes may threaten native oyster species, mainly by out competing their native congeners. It is therefore of upmost importance to understand physiological and biochemical responses of native and introduced oyster species in a scenario of global temperature rise, in order to provide knowledge that may allow for better species management. Hence, we compared biochemical alterations of the introduced C. gigas and the native Crassostrea brasiliana, the most important oyster species in Brazil, in response to different thermal regimes for 28 days (24, 28 and 32 °C). For this, metabolism (ETS), energy content (GLY), antioxidant system (SOD, CAT and GSH/GSSG) and cellular damage (LPO) were assessed in adult and juvenile specimens of both species. Juvenile C. gigas were the most affected by increased temperatures, presenting higher mortality, more pronounced antioxidant response (SOD), whereas adults were more tolerant than juveniles, showing no mortality, no significant changes in antioxidant enzymes activity neither energy expenditure. Native C. brasiliana juveniles presented lower mortality and less pronounced biochemical alterations were noted at higher temperature comparing to non-native C. gigas juveniles. Adult C. brasiliana were the least responsive to tested temperatures. Results obtained in this study bring interesting new insights on different oyster species life stages' physiological and biochemical tolerance towards thermal stress. The native species C. brasiliana showed ability to maintain biochemical performance at higher temperatures, with less pronounced biochemical changes than the non-native species. The introduced (C. gigas) showed to be more sensitive, presenting biochemical alterations to cope with the increase of temperature. Despite the lower observed fitness of the introduced species to temperatures closer to those naturally experienced by the native species, the ability of C. gigas to cope with higher temperatures should still raise concerns towards the native species C. brasiliana management and protection.

Introduction

Rising anthropogenic greenhouse gas emissions have proven to lead to unprecedented oscillations in temperature regimes in several terrestrial and marine ecosystems (Greco et al., 2011, IPCC, 2013). Low lying coastal marine ecosystems such as mangroves and estuaries are particularly vulnerable to global warming, given that they are naturally subjected to high temperature fluctuation (Harley et al., 2006). Projections for temperature rise by the end of the 21st century of between 2 and 4 °C (Hansen et al., 2013, IPCC, 2013, Solomon, 2007) and 2.4 to 6.4 °C (Smith et al., 2009), are of particular concern regarding the impacts on aquatic ecosystems biodiversity and functions (Brierley and Kingsford, 2009, Doney et al., 2012). In particular, temperature is considered to be the key factor determining biogeographical patterns, with intertidal ecosystems showing to be particularly susceptible to pronounced and rapid changes (Somero, 2012). Studies have pointed out several consequences of increasing temperature at biological levels, such as changes in reproduction timing and success, growth performance, species mortality and shifts on species geographical distribution (Cheung et al., 2009, Smolders et al., 2004, Talmage and Gobler, 2011).

In addition to global warming due to anthropogenic activities, the introduction of exotic species is another important factor threatening biodiversity worldwide (Hansen et al., 2013, Occhipinti-Ambrogi, 2007). In this respect, bivalves are among the most invading faunal groups (Francis, 2012), and the impacts due to their introduction, mainly for aquaculture purposes, have been a topic of concern (Mckindsey et al., 2007). Several biological characteristics of introduced bivalve species, often inherent to their aquaculture interest, such as high growth rates, adaptability to a wide range of environmental conditions, tolerance to physiological stress and high fertility, enable for their establishment and posterior expansion into new environments, and consequent dominance over native species. Other impacts of introducing non-native bivalve species can include alterations on ecosystem functioning (e.g. Kerckhof et al., 2007), introduction of pathogenic agents (e.g. Grizel and Héral, 1991), and deleterious interactions with other organisms (e.g. Diederich et al., 2005).

Among non-native bivalve species, oysters are one of the most invading groups and in addition to their ecological importance (Coen et al., 2007, Grabowski et al., 2012), they also represent major socio economic resources, and are among the most important group of mollusc species in global aquaculture landings (FAO, 2012). In fact, as a result of the increase of shellfish demand, non-native oyster species have been successfully introduced in a number of countries in an attempt to enhance production (Carranza et al., 2009). Presently, the most important cultured species Crassostrea gigas has been successfully introduced into aquaculture systems worldwide (Miossec et al., 2009). The introduction of this species may however threaten native oyster species given its potential to become invasive, as proven in several countries (Ruesink et al., 2005). The introduction of exotic oyster species can cause deleterious impacts on native oyster populations by introducing pathogenic agents and consequent mortality events (Ruesink et al., 2005, Mckindsey et al., 2007) and by outcompeting of native oyster species (Krassoi et al., 2008). In Brazil, C. gigas seeds are currently produced and grown in the southern state of Santa Catarina (Melo et al., 2010), while native oyster species are mainly extracted from natural environments, from which Crassostrea brasiliana presents higher economic and zootechnical yield (Mendonça and Machado, 2010, Neto et al., 2013). The introduction of C. gigas in Brazil has become particularly concerning, especially since the natural occurrence of this species has already been reported (Melo et al., 2010, Pie et al., 2006).

In light of this, the study of differences in performance between native and non-native species, in a scenario of global temperature rise if of upmost importance in order to better understand the underlying tolerance mechanisms that enable species to survive and compete in a changing environment (Parker et al., 2013, Somero, 2010). Therefore, the present study aimed to assess the biochemical responses of the native C. brasiliana and the introduced C. gigas oyster species to increasing water temperatures, in both juvenile and adult specimens, by use of a set of biomarkers (metabolism, energetic reserves, antioxidant capacity and membrane damage). A comparative analysis between different species and different life stages responses was conducted. The Pacific oyster C. gigas is the most important oyster species produced in aquaculture systems, providing annual global landings exceeding 40 million tonnes (Miossec et al., 2009). The mangrove oyster C. brasiliana is the most important native oyster species in Brazilian coastal waters, and is mainly extracted from the natural environment (Gomes et al., 2014). The most productive C. brasiliana natural banks are located in the southern coast of Brazil, in the Cananéia estuary (Galvão et al., 2013, Ristori et al., 2007). This mangrove dominated ecosystem is internationally recognized as one of the most productive ecosystems of the South Atlantic, having been declared Natural Heritage Site for knowledge and conservation of human values based on sustainable development standards, and included in the Atlantic Forest Biosphere by UNESCO in 1999 and 2005 respectively. In this mangrove dominated ecosystem the native oyster is one of the main fishery resources for the local communities, representing an important socio economic resource (Mendonça and Machado, 2010).