Sea urchin larvae show resilience to ocean acidification at the time of settlement and metamorphosis

Highlights

• Settlement success of E. chloroticus was unaffected when left to settle in a range of reduced seawater pH (7.0 to 8.1).

• Larval settlement success remained unaltered in presence of CCA pre-conditioned for 28 days at either ambient or reduced pH (7.7).

• Larvae did not lose their ability to recognize their preferred settlement substrate in presence of reduced seawater pH.

• No interactive effects were observed between seawater pH and preconditioned substrates on the larval settlement success.

Abstract

Extensive research has shown that the early life stages of marine organisms are sensitive to ocean acidification (OA). Less is known, however, on whether larval settlement and metamorphosis may be affected, or by which mechanisms. These are key processes in the life cycle of most marine benthic organisms, since they mark the transition between the free swimming larval stage to benthic life. We investigated whether OA could affect the larval settlement success of the sea urchin Evechinus chloroticus, a key coastal species with ecological, economic and cultural importance in New Zealand. We performed four settlement experiments to test whether reduced seawater pH (ranging from 8.1 to 7.0, at an interval of ~0.2 pH units) alters larval settlement and metamorphosis success. Our results show that settlement success was not significantly reduced when the larvae were exposed to a range of reduced seawater pH treatments (8.1–7.0) at time of settlement (on direct effects). Similarly, when presented with crustose coralline algae (CCA) pre-conditioned in seawater pH of either pH 8.1 or 7.7 for 28 days, larval settlement success remained unaltered (on indirect effects). We conclude that competent larvae in this species are resilient to OA at time of settlement. Further research on a range of taxa that vary in settlement selectivity and behaviour is needed in order to fully understand the effects of OA on the life cycle of marine invertebrates and the consequences it might have for future coastal marine ecosystems.

Introduction

Future ocean acidification (OA) conditions have been found to impact marine ecosystems and those organisms that they support (Gattuso et al., 2015; Stocker et al., 2013). It has already been shown that OA negatively affects multiple marine taxa (Kroeker et al., 2013; Przeslawski et al., 2015), with the developmental and early life stages particularly sensitive to reduced pH or elevated pCO₂ (Byrne, 2012; Byrne et al., 2017; Ross et al., 2011). In this respect, most marine benthic organisms reproduce through an indirect life cycle that is characterised by a free-living larval stage that ends with the pivotal processes of larval settlement and metamorphosis. Free-swimming larvae that result from external fertilization spend days to weeks in the water column. When ready to settle, the competent larvae typically selectively search for preferred settlement substrates and environments that have characteristic chemical, biological or physical properties (Hadfield and Paul, 2001). Coralline algae (CCA) and marine biofilms, in particular, are key settlement inducers for many marine species. CCAs and their associated microbial communities play an important role in the settlement process of many marine invertebrate larvae (McCoy and Kamenos, 2015), and microbial biofilms are known to induce settlement on their own (e.g. Whalan and Webster, 2014).

Settlement and metamorphosis are key life-history events, since they not only mark the transition between the planktonic larval stage into the benthic juvenile form, but most importantly, for sessile and benthic species, determine the place where the organisms will spend their post-settlement lives. As such, altered settlement and metamorphosis rates as a result of OA could directly affect distributions, abundances and ecology of future marine communities. Little is known, however, on how OA may affect larval settlement processes in marine invertebrates, and the mechanisms that might drive it (reviewed in Espinel-Velasco et al., 2018), although OA-related effects on oyster metamorphosis have previously been documented, possibly due to effects on the larval history and specific metabolic changes during metamorphosis (Dineshram et al., 2016; Ko et al., 2014). Reduced seawater pH could affect larval settlement through direct pathways, by altering larval morphology or physiology in such a way that larvae will not be capable of successfully settling onto the substrate (e.g. not being able to physically settle or differentiate between substrates). Specifically, OA could affect the molecular signalling pathways (Pecquet et al., 2017), as well as the molecular structure of the receptors, therefore altering cue sensing and settlement and metamorphosis success. Indirect pathways of altering larval settlement could be through OA-induced changes in the nature of settlement substrates (such as CCA or marine biofilms) and their associated chemical signals (waterborne or adsorbed), therefore altering settlement success. Indeed, OA could alter the distribution and composition of the settlement substrates, as well as their associated chemical signals (waterborne or adsorbed), therefore altering settlement success. Furthermore, effects on settlement success due to the exposure to OA could be caused by the interactive effects of both direct and indirect mechanisms (Espinel-Velasco et al., 2018; Kroeker et al., 2013). The outcomes of these impacts may be reduced settlement rates, loss of settlement selectivity or a total inhibition of the larval settlement.

Sea urchins (Echinodermata, Echinoidea) and their developmental stages have been extensively used as model organisms in OA research (Dupont and Thorndyke, 2013). The adults are relatively easy to spawn, and sea urchin development is well-described. Echinoids also have a high socio-economic value (Branch et al., 2013) and often play a key ecological role in many marine ecosystems, such as kelp forests and coral reefs, through their relatively high abundances and feeding activities (Lawrence and Sammarco, 1982). Spatial and temporal variability in sea urchin population abundances has been related to differences in settlement, metamorphosis and recruitment rates (Lamare and Barker, 2001; Rowley, 1989). Therefore, any process that significantly affects the process of settlement in these keystone taxa, such as ocean acidification, might lead to ecological shifts in coastal ecosystems where they play a key role.

In New Zealand, the sea urchin Evechinus chloroticus Valenciennes (Echinometridae) is a key coastal species, commonly found at the low intertidal or subtidal areas of the rocky shore ecosystem (Andrew, 1988; Barker, 2013). The species has an annual reproductive cycle, with spawning taking place between November to February (Brewin et al., 2000). The resulting planktotrophic larvae reach competency in 3–6 weeks (Lamare and Barker, 1999). Larvae settle and metamorphose preferentially on to CCA and aged biofilms, although other substrates will induce metamorphosis over time (Lamare and Barker, 2001), possibly due to the larvae losing substrate selectivity, such as seen in polychaete larvae (Knight-Jones, 1951; Wilson, 1953).

In this study we examine the potential for OA to alter larval settlement and metamorphosis in E. chloroticus. We test two hypotheses: (1) OA will affect the settlement process of competent larvae through direct effects that will alter their settlement behaviour (changes in larval fitness or perception), and (2) OA will alter the settlement through indirect mechanisms whereby the settlement substrates and associated settlement cues are no longer inducive to settlement.