A marine secondary producer respires and feeds more in a high CO₂ ocean

Abstract

Climate change mediates marine chemical and physical environments and therefore influences marine organisms. While increasing atmospheric CO₂ level and associated ocean acidification has been predicted to stimulate marine primary productivity and may affect community structure, the processes that impact food chain and biological CO₂ pump are less documented. We hypothesized that copepods, as the secondary marine producer, may respond to future changes in seawater carbonate chemistry associated with ocean acidification due to increasing atmospheric CO₂ concentration. Here, we show that the copepod, Centropages tenuiremis, was able to perceive the chemical changes in seawater induced under elevated CO₂ concentration (>1700 μatm, pH < 7.60) with avoidance strategy. The copepod’s respiration increased at the elevated CO₂ (1000 μatm), associated acidity (pH 7.83) and its feeding rates also increased correspondingly, except for the initial acclimating period, when it fed less. Our results imply that marine secondary producers increase their respiration and feeding rate in response to ocean acidification to balance the energy cost against increased acidity and CO₂ concentration.

Introduction

The ocean is known to absorb about one million tons of CO₂ per hour and have been acidified by 30% (increase in H⁺ concentration) since the industrial revolution and will be further acidified by 150% by the end of 2100 (Caldeira and Wickett, 2003) under the “business as usual” CO₂ emission. Chemical changes associated with the ocean acidification include increased concentrations of H⁺ and ${\text{HCO}}_3^{-}$ and decreased levels of ${\text{CO}}_3^{2-}$ and CaCO₃ saturation state, which negatively influence calcification of most marine calcifiers (Riebesell et al., 2000, Gao and Zheng, 2010, Beaufort et al., 2011). In addition, ocean acidification is known to influence olfactory functions of fish (Munday et al., 2009, Dixson et al., 2010) and can alter thermal windows of marine animals (Pörtner and Farrell, 2008).

Elevated seawater pCO₂ level is known to affect marine benthic and pelagic animal’s development, reproduction and metabolisms (Kurihara and Ishimatsu, 2008, Widdicombe and Spicer, 2008). Decreased pH was shown to reduce the sperm flagella motility of reef invertebrates (Morita et al., 2010) and echinoderm larval feeding efficiency (Dupont and Thorndyke, 2008). Additionally, low pH may affect respiratory carbon loss in plankton (Wu et al., 2010). The effects of low pH on marine animals are often due to acidosis and hypercapnia generated in the intracellular space (Widdicombe and Spicer, 2008), which will disturb the balance of acid–base (Pörtner et al., 2004) and result in influences on behavioral performance (Thistle et al., 2007) and physiological processes (Roos and Boron, 1981), such as neural signals (Waggett and Buskey, 2008), development, reproduction (Kikkawa et al., 2004), metabolism and even gene expressions (Pörtner et al., 2010).

Regulation of body acid–base is somewhat energy dependent and low pH induced acidosis or hypercapnia can be expected to affect the energy acquisition and allocation (Whiteley, 2011). Here we hypothesize that the increased partial pressure of CO₂ and acidity of seawater associated with ocean acidification may affect copepods’ respiration to cope with the chemical changes, and hence it would mediate its feeding rate to meet the energy demand. We chose a costal water calanoid copepod, Centropages tenuiremis, to test this hypothesis. This species is a major dominant copepod in the coastal South China Sea and plays an important role in the coastal ecosystem (Wang et al., 2005). In coastal waters where pH usually fluctuates during a daily cycle, the planktons usually experience wider ranges of pH compared to offshore species (Yamada and Ikeda, 1999). Therefore, we judge that response of a coastal copepod to changed seawater chemistry can be considered representative for offshore species that experience fewer changes in pH and should be more sensitive to changes in seawater carbonate system.