Altered epiphyte community and sea urchin diet in Posidonia oceanica meadows in the vicinity of volcanic CO2 vents
Introduction
The concentration of carbon dioxide (CO2) in the atmosphere is increasing mainly due to fossil fuel combustion and industrial processes. Oceans absorb approximately 30% of the anthropogenic CO2 released to the atmosphere, which has caused a pH decrease in surface waters of 0.1 units since pre-industrial times in a process commonly known as ocean acidification (OA). An additional decrease in pH of 0.06–0.32 units is expected by the end of the century according to the different scenarios of CO2 emissions used for projections (IPCC, 2014). Together with reduced pH, changes in the relative proportion of total dissolved inorganic carbon forms co-occur, including a reduced concentration of carbonate ions (CO32−). These changes may negatively affect the formation of carbonate structures, shells and skeletons by calcifying organisms, as well as their metabolism (e.g. acid-base regulation), survival or abundance (Pörtner, 2008, Kroeker et al., 2011, Kroeker et al., 2013a). At the same time, increased availability of photosynthesis substrates (CO2 and/or HCO3−) may enhance the photosynthesis and growth of non-calcifying primary producers such as phytoplankton, cyanobacteria, fleshy algae and seagrasses (Doney et al., 2009, Kroeker et al., 2010).
The above-mentioned responses and sensitivities of species to OA have mostly been identified by means of CO2 enrichment experiments in laboratory or mesocosms. More recently, in situ observations of submarine volcanic CO2 vents have provided data on marine ecosystems long-term adapted to high CO2/low pH levels, which integrate complex species interactions within entire communities (e.g. Fabricius et al., 2011, Kroeker et al., 2011, Kroeker et al., 2013a, Linares et al., 2015). In some of the most studied CO2 vents around the world, seagrass meadows are exposed to pH conditions similar to future levels of ocean acidification, thus allowing to investigate long-term OA effects on such relevant ecosystems (Hall-Spencer et al., 2008, Vizzini et al., 2010, Apostolaki et al., 2014).
Seagrass meadows provide key ecosystem services such as stabilization of coastal sediments, provision of habitat and nursery for species (including several taxa of commercial interest), maintenance of biodiversity, and long-term removal of CO2 from the atmosphere (Orth et al., 2006, Fourqurean et al., 2012). A highly diverse community of epiphytes (as defined by Steel and Wilson, 2003) colonizes seagrass leaves, which include calcareous and non-calcareous algae, hydrozoans, bryozoans, and polychaetes (Mazzella et al., 1989, Prado et al., 2007, Piazzi et al., 2016). Epiphytes are important contributors to total aboveground biomass and primary production in seagrass meadows (Champenois and Borges, 2012) and they play a major role in seagrass food webs (Mazzella et al., 1992, Williams and Heck, 2001, Vizzini, 2009). Particularly, the foraging behaviour of key herbivorous sea urchins on seagrasses has been reported to be largely driven by the occurrence of leaf epiphytes (Vergés et al., 2011, Marco-Méndez et al., 2012, Marco-Méndez et al., 2015).
The dominance of coralline algae and other calcifying organisms and their high sensitivity to OA render the epiphyte community especially vulnerable to a high-CO2 ocean. Previous studies, including observations in CO2 vents as well as laboratory and mesocosm experiments, have shown a marked decline in the abundance of coralline algae and/or other calcifying taxa under high pCO2/low pH, often associated to a proliferation of non-calcareous taxa (e.g. Hall-Spencer et al., 2008, Kuffner et al., 2008, Fabricius et al., 2011). Whilst such direct effects on single species or taxa are relevant in structuring marine communities, indirect effects of OA involving species interactions (e.g. trophic interactions) can also be of importance for the overall response of ecosystem diversity and function (Kroeker et al., 2011, Kroeker et al., 2013a, Russell et al., 2012). How OA indirectly affects key ecological meadow functions such as provision of food to herbivores has been scarcely investigated (but see Ricevuto et al., 2015, Tomas et al., 2015). Both, direct and indirect OA effects may have relevant consequences in the maintenance of the key ecological functions and ecosystem services delivered by these priority habitats.
Among herbivores inhabiting seagrass meadows, sea urchins play a major role in controlling the composition and abundance of seagrass and macroalgal communities (Palacín et al., 1998, Valentine and Heck, 1999, Poore et al., 2012). They also have a relevant commercial value around the world since sea urchin gonads are very appreciated culinary delicacies (Lawrence, 2007). Sea urchins at different development stages appear to be more resistant to near future OA than previously thought, as revealed by studies using realistic pH scenarios based on IPCC (2014) predictions for the end of the century (i.e. a decrease lower or equal than 0.32 units of pH). Reports of OA effects on early developmental stages of sea urchins are contradictory, indicating either larvae and juvenile vulnerability or resistance (reviewed by Dupont et al., 2010; see also Yu et al., 2011, Moulin et al., 2011). Furthermore, adult sea urchins appear to be more clearly resistant to OA under realistic predictions, as only highly species-specific sublethal effects have been reported by studies in which extreme pH reductions are not considered (Dupont et al., 2010, Hazan et al., 2014, Moulin et al., 2015). As a result, adult sea urchins metabolically adapted to CO2/pH levels predicted for 2100 are expected to be sensitive to indirect effects of OA-induced changes in the availability and quality of their food. However, very few studies have investigated these indirect effects, being most of them focused on how experimentally CO2-induced changes on seagrass traits alter urchin consumption disregarding seagrass epiphytes (Tomas et al., 2015), or on effects of monospecific macroalgal diets at different CO2 levels on calcite structures of sea urchins (Asnaghi et al., 2013). Given the pivotal role that sea urchins play in structuring communities through grazing (Carpenter, 1986, Bulleri et al., 1999), indirect OA effects on these grazers' impacts may cause cascading effects on ecosystem functioning and diversity.
In this study, we compared the composition and abundance of the epiphyte community of the seagrass Posidonia oceanica in a control site and in two sites affected by high pCO2/low pH in volcanic vents at the Ischia Island (NW Mediterranean Sea). We hypothesized that altered seawater chemistry close to the vents shifts the epiphyte community towards the dominance of more tolerant taxa (e.g. non-calcifying species), and that these shifts are propagated into indirect effects on the diet of the commercially important sea urchin Paracentrotus lividus that inhabits P. oceanica meadows.
Section snippets
Study area
This study was conducted in the Ischia Island, which is located in the Gulf of Naples (Italy) in the Tyrrhenian Sea (NW Mediterranean Sea). Submarine CO2 vents of volcanic origin occur at 0.5–3 m depth in the north and south sides of a small islet (Castello Aragonese), where Posidonia oceanica meadows are naturally exposed to a gradient of CO2 enrichment and pH reduction. Gas composition in this area consists of 90.1–95.3% CO2, 3.2–6.6% N2, 0.6–0.8% O2, 0.2–0.8% CH4 and 0.08–0.1 Ar, and do not
Epiphyte community
A total of 34 taxa of epiphytes were identified on P. oceanica leaves (mostly to genus level), among which 13 were calcifying organisms (Table A.1). A taxa richness of 21 taxa was found in both the control and the low pH-north sites, whereas only 12 taxa were found in the low pH-south site. No significant differences were detected between sites in taxa richness (ANOVA F = 2.0, df = 2, p = 0.192). Total epiphyte cover (mean ± SE) was significantly higher in the low pH-north (85.9 ± 7.5% of the
Discussion
Our study reveals that epiphyte communities of seagrass inside and outside the influence of CO2 vents significantly differ in composition and abundance. A marked reduction in the abundance of the crustose coralline algae has been widely reported as a major effect of ocean acidification by manipulative experiments conducted on different seagrass species (Campbell and Fourqurean, 2014, Martínez-Crego et al., 2014, Cox et al., 2015). Our results partially support this observation, as we found a
Acknowledgements
The research was funded by an ASSEMBLE Access project within the EU FP7/2007–2013 program (grant agreement n° 227799) hosted by MCG at the SZN. BMC was supported by a postdoctoral fellowship of the Portuguese Foundation for Science and Technology (FCT; SFRH/BPD/75307/2010). PN was involved in the International Master of Science in Marine Biodiversity and Conservation (EMBC+). The funders had no role in study design, data collection and analysis, preparation of the manuscript, or decision to
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2017, Science of the Total EnvironmentCitation Excerpt :Low C:N is a proxy of high nutritional quality of seagrass organic matter (Riebesell et al., 2007; Ricevuto et al., 2015). The low C:N ratio in leaves of the acidified site was associated with higher protein and lower starch contents, whereas the cell wall components, lignin and holocellulose, were not affected by pH. Moreover, the reduced leaf phenolic compounds (Arnold et al., 2012) and the lower abundance of leaf covering calcareous epiphytes reported for our (Garrard, 2013) and other (Hall-Spencer et al., 2008; Donnarumma et al., 2014; Kamenos et al., 2016; Nogueira et al., 2017) acidified sites may favor leaf grazing (Apostolaki et al., 2014). The increased grazing rate in the acidified site would cause the P. oceanica stand to lose a higher amount of leaf biomass over time than the meadow standing in the control site.