The effects of elevated CO₂ on shell properties and susceptibility to predation in mussels Mytilus edulis

Highlights

• Ocean acidification is a major threat to marine ecosystem structure and functioning.

• 2100 pCO₂ scenario reduced Mytilus shell thickness & area, body volume and feeding rate.

• Predation risk susceptibility changes under future climate scenarios.

• Large prey not susceptible to predation today 8x more at risk under OA scenarios.

• Significant changes to ecosystem structure and functioning predicted for future.

Abstract

For many species, ocean acidification (OA) is having negative physiological consequences on their fitness and resilience to environmental change, but less is known about the ecosystem effects of these changes. Here, we assess how OA conditions predicted for 2100 affects the biological functioning of an important habitat-forming species Mytilus edulis and its susceptibility to predation by a key predator, the gastropod Nucella lapillus. Change in three physiological parameters in Mytilus were assessed: (1) shell thickness and cross-sectional surface area, (2) body volume and (3) feeding rate, as well as susceptibility to predation by N. lapillus. Shell thickness and cross-section area, body volume and feeding rate of Mytilus all reduced under OA conditions indicating compromised fitness. Predation risk increased by ∼26% under OA, suggesting increased susceptibility of mussels to predation and/or altered predator foraging behaviour. Notably, predation of large Mytilus – that were largely free from predation under control conditions – increased by more than 8x under OA, suggesting that body size was no longer a refuge. Our results suggest OA will impact upon ecosystem structure and functioning and the continued provision of ecosystem services associated with Mytilus reefs and the communities associated with them.

Introduction

Climate change is one of the greatest threats to biodiversity globally (Thomas et al., 2004) altering population and community dynamics (Parmesan and Yohe, 2003) and increasing risks of species extinction (Thomas et al., 2004). There is overwhelming evidence that human activities are driving rates of climate change (Henson et al., 2017); the continued emission of greenhouse gases is a primary driver of increasing global temperatures and ocean acidification (Caldeira and Wickett, 2003). Predictions of global environmental conditions for the end of the century (e.g. RCP8.5 scenario; Stocker et al., 2013) coupled with ever-increasing experimental evidence suggest wide-ranging impacts of future ocean acidification and warming (OAW) scenarios on marine life (Poloczanska et al., 2016).

Climate change may benefit some organisms. A wide-range of taxa including jellyfish, macroalgae, invertebrates and some fish (e.g. Aprahamian et al., 2010; Hall-Spencer and Allen, 2015), especially those with Lusitanian evolutionary origins (Lavergne et al., 2010), are demonstrating increased fitness over wider geographic ranges (e.g. Calosi et al., 2017). But wide-ranging negative effects of OAW have also been shown or are predicted to alter ecology, behaviour and physiology (Gazeau et al., 2013; Hughes, 2000; Lemasson et al., 2017a, 2017b). For instance, OA has been shown to alter predator-prey dynamics (Dixson et al., 2010; Harvey and Moore, 2017), intracellular pH, biological functioning (Pörtner et al., 2004), metabolism (Thomsen and Melzner, 2010), and individual energetic needs (Gray et al., 2017; Leung et al., 2017). These changes could change ecosystem structure by amplifying range shifts (Calosi et al., 2017) or cause trophic cascades through lower abundances of key species and reduced trophic transfer (Rossoll et al., 2012). In addition, a decrease in critical ecosystem services (ESs) may also occur (Lemasson et al., 2017a; b).

Molluscs and other calcifying organisms are particularly prone to environmental change and especially OA (Gazeau et al., 2013; Parker et al., 2013). Increased pCO₂ has been shown to reduce calcification (but see Ries et al., 2009), alter crystalline ultrastructure (Duquette et al., 2017; Fitzer et al., 2016; Leung et al., 2017) and increase dissolution rates in oysters and mussels (Berge et al., 2006; Gazeau et al., 2007; Ries et al., 2009). These changes are predicted to alter the capacity of individuals to maintain their exoskeleton via biomineralisation of calcium carbonate mechanisms; an effect illustrated by a reduction in shell thickness (e.g. Chen et al., 2015) and strength (Speights et al., 2017; Welladsen et al., 2010) in some bivalves. The effect of these changes may extend beyond the fitness of the individual, affecting the wider ecosystem by changing survivorship and/or increasing susceptibility of prey to predation (Dixson et al., 2010; Freeman and Byers, 2006) with consequences that cascade up the food chain.

Many calcifying organisms are of ecological and economic importance, and provide numerous ecosystem services (MEA, 2005). Often ecosystem engineers (sensu Jones et al., 1994) or habitat-forming species, they create habitat for other species and support disproportionately high biodiversity in comparison to other habitats (Gutierrez et al., 2003). Bivalve molluscs, which include the mussel Mytilus spp., are especially important. Abundant worldwide, mussels account for 30% of global mollusc aquaculture, and in 2015, global production was ∼16.5 million tonnes with a market value of ∼$18 billion (FAO, 2015). They also provide a number of other important supporting ecosystem services including nutrient cycling and improving water quality (Asmus and Asmus, 1991; Dame and Dankers, 1988; Pejchar and Mooney, 2009).

Here, we test the effect of future OA scenarios of the functioning of Mytilus spp. Firstly, we consider how OA impacts the fitness of individuals, specifically their shell thickness, body volume, and feeding rate. We then test if changes in individual fitness alters trophic interactions strength between Mytilus and one of its key predators.