Sea urchin larvae show resilience to ocean acidification at the time of settlement and metamorphosis
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.
Section snippets
Collection
Adult Evechinus chloroticus were collected by SCUBA in Doubtful Sound (Fjordland, New Zealand) from 10 to 14 m depth, and kept in sealed buckets containing seawater for transport. The collected specimens were taken to the Portobello Marine Laboratory (Dunedin, New Zealand), maintained in tanks with flow-through seawater and fed with freshly collected brown macroalgae for several weeks prior to experiments.
Spawning and fertilization
Mature adult E. chloroticus (80–100 mm test diameter) were induced to spawn by
Experimental treatments and sea water carbonate chemistry
The measured pH over the course of experiments 1 to 4 are reported in supplementary material (Tables S1–S4). Fig. S1 in supplementary material shows the evolution of the pH in the aquaria for the different experiments. The seawater carbonate chemistry is reported for experiments 1, 2 and 3. No water chemistry is available for experiment 4 due to logistical constraints (Table 1).
Substrate recognition and direct effects of OA (Experiment 1)
There was a significant difference in the settlement success on CCA versus bare rock substrates, although, we found no
Discussion
The range of experiments performed here showed no indication of an influence of reduced seawater pH on the settlement and metamorphosis in E. chloroticus larvae. Our experiments did not detect any effects of OA on the larval settlement that would be consistent with reduced seawater pH altering the physiology or sensory capacity of the larvae in a way that influences their settlement behaviour. In addition, we found no indication that short-term exposure of CCAs to reduced pH altered the larval
Conclusion
Our results provide further observations of the potential for OA to alter larval settlement in marine invertebrates. For E. chloroticus, we found little evidence of strong direct or indirect effects in this respect. Our observations of no direct effects on the larval settlement are consistent with results obtained in previous investigations on other species of sea urchins (Dupont et al., 2013; Wangensteen et al., 2013). On the other hand, our findings on (the absence of) indirect effects are in
CRediT authorship contribution statement
Nadjejda Espinel-Velasco: Conceptualization, Methodology, Formal analysis, Investigation, Writing - original draft, Writing - review & editing, Visualization, Project administration. Antonio Agüera: Methodology, Formal analysis, Writing - review & editing, Visualization. Miles Lamare: Conceptualization, Methodology, Writing - review & editing, Supervision.
Declaration of competing interest
The authors declare that they have no conflict of interest.
Acknowledgements
Thanks to Kim Currie and Judith Murdoch at the National Institute of Water and Atmospheric Research (NIWA), New Zealand, for the DIC and total alkalinity measurements. Thank you to two anonymous reviewers for their constructive suggestions. Miles Lamare contributions were supported by CARIM (Coastal Acidification: Rate, Impacts and Management), funded by the New Zealand Ministry of Business, Innovation and Employment.
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