Ocean acidification and climate change are currently under high scrutiny due to the threat that they represent for the biodiversity and function of marine ecosystems. Current increases in atmospheric carbon dioxide (CO2) and temperature proceed at unprecedented rates in the recent history of the Earth. Atmospheric CO2 concentration has risen from 280 ppm prior to the beginning of the industrial revolution to a current value of 388 ppm due to human activities and is expected to reach more than 700 ppm by the end of this century considering the Intergovernmental Panel on Climate Change (IPCC) scenarios (Solomon et al. 2007). Global average temperature at Earth's surface has risen by 0.7°C during the last century and is expected to rise by 3°C by 2100 (Solomon et al. 2007). Similar trends are expected for surface ocean CO2 partial pressure (pCO2) and temperature due to the oceanic uptake of anthropogenic CO2 (Sabine et al., 2004) and to the warming of the surface mixed layer (Levitus et al. 2005).
Increasing pCO2 in the surface ocean is likely to decrease pH by 0.2–0.4 units over the course of this century (Caldeira and Wickett 2005) which will cause major shifts in seawater chemistry, with an increase in the concentration of bicarbonate ions (HCO3−) and a decrease in the concentration of carbonate ions (CO32−) and the saturation state of calcium carbonate (CaCO3). Such shifts are likely to affect both calcifying and photosynthetic marine organisms due to potential changes in their physiological processes of calcification and photosynthesis that both use dissolved inorganic carbon (CT: HCO3−, CO32− and CO2) as substrate. Although the physiological response of marine organisms to ocean acidification is variable among taxa and species (Doney et al. 2009; Ries et al. 2009), the decrease in the availability of CO32− is known to affect the ability of marine calcifiers to form their carbonate skeleton or shells by a decline in calcification rates. A recent meta-analysis demonstrated that calcification is generally negatively affected by ocean acidification (Kroeker et al. 2010). Seawater acidification is also likely to affect photosynthesis due to the shift in the relative proportions of CO2 and HCO3−, the two forms of CT that can be used for photosynthesis. Algae can use dissolved CO2 entering the cell by diffusion as the carbon source for photosynthesis but most of them have carbon concentrating mechanisms (CCMs) which actively take up HCO3− which is converted to CO2 in the cells. This is a powerful mechanism counteracting the limited availability of CO2 in seawater (Raven and Geider 2003). An increase in seawater pCO2 could thus enhance photosynthesis in plants that rely exclusively on CO2 diffusion (Kübler et al. 1999), while it would be less favorable to algae that use CCMs (Giordano et al. 2005).
The calcareous red coralline algae coralline algae (Corallinales, Rhodophyta) are of particular interest to investigate as they conduct both photosynthesis and calcification. They are also considered among the most sensitive calcifying organisms to respond to ocean acidification due to the high solubility for their high magnesian calcite skeleton. Coralline algae are absent in naturally acidified seawater where other calcifiers can survive (Hall-Spencer et al. 2008; Martin et al. 2008). Their recruitment (Agegian 1985; Kuffner et al. 2007) and growth (Agegian 1985; Jokiel et al. 2008; Hofmann et al. 2012) are both negatively affected under elevated pCO2. Most recent studies show that coralline calcification is negatively affected under elevated pCO2 (Anthony et al. 2008; Semesi et al. 2009; Gao and Zheng 2010; Büdenbender et al. 2011; Johnson and Carpenter 2012) and that this effect is exacerbated by further ocean warming (Anthony et al. 2008). However, some authors reported a significant pCO2 effect on calcification only in combination with increased temperature (Martin and Gattuso 2009) or a positive pCO2 effect under moderate levels with a parabolic response of calcification in response to increased pCO2 (Smith and Roth 1979; Ries et al. 2009). The response of photosynthesis and respiration to ocean acidification in coralline algae is poorly understood. To our knowledge, only one study has investigated the effect of increased pCO2 on respiration in coralline algae and showed no effect (Semesi et al. 2009). The response of coralline photosynthesis to ocean acidification is variable among species but most are negatively affected (Anthony et al. 2008; Gao and Zheng 2010; Hofmann et al. 2012) with a larger impact under elevated temperature (Anthony et al. 2008). Conversely, some authors found positive (Borowitzka 1981; Semesi et al. 2009) or parabolic (Borowitzka 1981) responses. Very few studies have investigated calcification, photosynthesis, and respiration all together in coralline algae. However, these processes are tightly linked and the formation of CaCO3 crystals in cell walls of coralline algae is suggested to be largely controlled by photosynthesis and respiration (Smith and Roth 1979; Borowitzka 1981; Gao et al. 1993; De Beer and Larkum 2001). Photosynthesis may stimulate calcification by providing an organic matrix in the cell walls where the nucleation of calcite crystals is thought to occur (Borowitzka 1981). Furthermore, photosynthesis and respiration are two processes that control pH and that may in turn influence calcification rates. Photosynthesis increases pH and thereby increases the CaCO3 saturation state, favoring calcification (Gao et al. 1993) while respiration decreases pH and act in the opposite direction by hindering calcification (De Beer and Larkum 2001). While most recent research has focused on the response of coralline algae to ocean acidification, their response to the combined rise in pCO2 and temperature has been poorly investigated. Marine organisms are adapted to live in specific environmental temperature ranges, and a rise in temperature is likely to have direct effects on their physiology. By making coralline algae more vulnerable to other stressors, elevated pCO2 could have a larger impact when combined with elevated temperature than alone (Anthony et al. 2008; Martin and Gattuso 2009; Diaz-Pulido et al. 2012).
Changes in calcification and primary production in coralline algae may have profound consequences for the ecosystems that they compose from polar regions to the tropics (Johansen 1981) and in which they are a major calcifying component of the marine benthos. Coralline algae are of particular ecological importance in shallow waters, inducing settlement and recruitment of numerous invertebrates and providing habitats for a high diversity of associated organisms (Johansen 1981). Their rigid structure contributes to the formation of numerous habitats such as rhodolith beds (Foster, 2001) or coralligenous habitats (Ballesteros 2006). Coralline algae are also of significant importance in the carbon and carbonate cycles of shallow coastal ecosystems, being major contributors to CO2 fluxes through high community photosynthesis and respiration (Martin et al. 2005, 2007) and through high CaCO3 production and dissolution (Barron et al. 2006; Martin et al. 2007).
A better understanding of how coralline algal photosynthesis, respiration, and calcification respond to ocean acidification and warming is critical to predicting how coralline algae-based community may change in response to global environmental changes. That response may also vary depending on changes in other environmental factors and in particular irradiance which is the third major physical variable that affects both photosynthesis and calcification. The response of coralline algae to ocean acidification and/or warming has mainly been investigated through short-term (a few days to a few weeks) experimental approach, therefore neglecting the potential for physiological acclimation. In this study, we investigate, through a long-term (1 year) experiment, the combined effects of elevated pCO2 and temperature on respiration, photosynthesis, and net calcification in the crustose coralline algae, Lithophyllum cabiochae, which is one of the main calcareous components of coralligenous communities in the Mediterranean Sea. We hypothesize that future changes in pCO2 and temperature will incur a physiological stress in L. cabiochae thereby affecting its metabolic rates. We report on the response to elevated pCO2 and temperature in the four seasons to assess how seasonal variations of temperature and irradiance may interact with global environmental changes.