Macroalgal Responses to Ocean Acidification Depend on Nutrient and Light

Global Change and the Future Ocean Macroalgal responses to ocean acidification depend on nutrient and light levels Paula S.M. Celis-Plá, Jason M. Hall-Spencer, Paulo Horta, Marco Milazzo, Nathalie Korbee, Christopher E. Cornwall and Félix L. Figueroa Journal Name: Frontiers in Marine Science ISSN: 2296-7745 Article type: Original Research Article Received on: 05 Mar 2015 Accepted on: 04 May 2015 Provisional PDF published on: 04 May 2015 Frontiers website link: www.frontiersin.org Citation: Celis-plá P, Hall-spencer JM, Horta P, Milazzo M, Korbee N, Cornwall CE and Figueroa FL(2015) Macroalgal responses to ocean acidification depend on nutrient and light levels. Front. Mar. Sci. 2:26. doi:10.3389/fmars.2015.00026 Copyright statement: © 2015 Celis-plá, Hall-spencer, Horta, Milazzo, Korbee, Cornwall and Figueroa. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. This Provisional PDF corresponds to the article as it appeared upon acceptance, after rigorous peer-review. Fully formatted PDF and full text (HTML) versions will be made available soon. 1 Macroalgal responses to ocean acidification depend on nutrient and 2 light levels 3 4 5 6 Paula S.M. Celis-Plá1, 2*, Jason M. Hall-Spencer3, Paulo Horta4, Marco Milazzo5, Nathalie Korbee1, 7 Christopher E. Cornwall6, 7 and Félix L. Figueroa1 8 9 1Department of Ecology, Faculty of Science, University of Malaga, 29071 Malaga, Spain 10 2Laboratory of Botany, Faculty of Pharmacy, University of Barcelona, 08028 Barcelona, Spain 11 3Marine Biology and Ecology Research Centre, Plymouth University, Plymouth PL4 8AA, UK 12 4Department of Botany, University Federal of Santa Catarina, 88040-970 Trinidade, 39 Florianopolis, SC, Brazil 13 5Dipartimento di Scienze della Terra e del Mare, University of Palermo, via Archiraﬁ 28, 90123 Palermo, Italy 14 6Institute for Marine and Antarctic Studies (IMAS), University of Tasmania, Hobart, Tasmania 7001, Australia 15 7School of Earth and Environment & ARC Centre of Excellence for Coral Reef Studies, University of Western Australia, 16 Crawley, Western Australia 6009, Australia 17 18 *Corresponding author at: Tel: +34952131672; fax: +34952137386, e-mail address: [email protected] 19 20 Keywords: Ocean acidification, macroalgae, photosynthesis, phenolic compounds, nutrient 21 availability 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 1 38 ABSTRACT 39 Ocean acidification may benefit algae that are able to capitalise on increased carbon availability 40 for photosynthesis but is expected to have adverse effects on calcified algae through dissolution. 41 Shifts in dominance between primary producers will have knock-on effects on marine 42 ecosystems and will likely vary regionally, depending on factors such as irradiance (light vs 43 shade) and nutrient levels (oligotrophic vs eutrophic). Thus experiments are needed to evaluate 44 interactive effects of combined stressors in the field. In this study, we investigated the 45 physiological responses of macroalgae near a CO2 seep in oligotrophic waters off Vulcano 46 (Italy). The algae were incubated in situ at 0.2 m depth using a combination of three mean CO2 47 levels (500, 700-800 and 1200 µatm CO2), two light levels (100 and 70% of surface irradiance) 48 and two nutrient levels of N, P, and K (enriched vs non-enriched treatments) in the non-calcified 49 macroalga Cystoseira compressa (Phaeophyceae, Fucales) and calcified Padina pavonica 50 (Phaeophyceae, Dictyotales). A suite of biochemical assays and in vivo chlorophyll a 51 fluorescence parameters showed that elevated CO2 levels benefitted both of these algae, 52 although their responses varied depending on light and nutrient availability. In C. compressa, 53 elevated CO2 treatments resulted in higher carbon content and antioxidant activity in shaded 54 conditions both with and without nutrient enrichment - they had more Chla, phenolic and 55 fucoxanthin with nutrient enrichment and higher quantum yield (Fv/Fm) and photosynthetic 56 efficiency (αETR) without nutrient enrichment. In P. pavonica, elevated CO2 treatments had 57 higher carbon content, Fv/Fm, αETR, and Chla regardless of nutrient levels - they had higher 58 concentrations of phenolic compounds in nutrient enriched, fully-lit conditions and more 59 antioxidants in shaded, nutrient enriched conditions. Nitrogen content increased significantly in 60 fertilised treatments, confirming that these algae were nutrient limited in this oligotrophic part 61 of the Mediterranean. Our findings strengthen evidence that brown algae can be expected to 62 proliferate as the oceans acidify where physicochemical conditions, such as nutrient levels and 63 light, permit. 64 65 66 67 68 69 70 71 2 72 INTRODUCTION 73 Ocean acidification due to increased atmospheric CO2 levels is altering the concentrations 2– 74 of dissolved inorganic carbon (DIC) in surface waters; CO3 levels are falling, which is – 75 expected to corrode marine carbonates, whilst CO2 and HCO3 levels are rising which can 76 stimulate photosynthesis (Connell et al., 2013; Cornwall et al. 2015). As some primary 77 producers are better able to capitalize on increasing carbon availability than others, this is 78 expected to alter marine communities (Hepburn et al., 2011; Connell et al., 2013; Koch et al., 79 2013; Gaylord et al., 2015). In the Mediterranean, surveys of coastal CO2 seeps have repeatedly 2- 80 shown that coralline algae and sea urchins become less common as pH and CO3 fall, whereas 81 brown algae, such as Cystoseira spp., Dictyota spp., Sargassum vulgare and Padina pavonica, – 82 proliferate as CO2 and HCO3 levels rise (Porzio et al., 2011; Baggini et al., 2014). The ways 83 in which ocean acidification affects communities of primary producers is likely to vary 84 regionally, depending on the species present and abiotic factors such as temperature, light and 85 nutrient availability (Giordano et al., 2005; Brodie et al., 2014; Hofmann et al. 2014). 86 To begin to understand the influence of physicochemical factors on the responses of 87 macroalgae to ocean acidification, we grew common types of brown algae (from the Families 88 Fucales and Dictyotales) at CO2 seeps in a multifactorial experiment in which we manipulated 89 light (irradiance) and nutrient levels. At low light levels, macroalgae are thought to be more 90 likely to rely on carbon uptake via diffusion than use energetically expensive carbon 91 concentrating mechanisms (Raven and Beardall, 2014; Raven et al., 2014) which has led to the 92 idea that any benefits of ocean acidification on growth would only be seen at lower light levels 93 for the majority of species (Hepburn et al., 2011). However, ocean acidification also has the 94 potential to damage photoprotective mechanisms which kick-in at high light levels (Pierangelini 95 et al., 2014). Algae minimize damage from high irradiance by down-regulating photosystems, 96 they also produce chemicals, such as phenolic compounds in the brown algae, which screen 97 ultraviolet light and dissipate energy (Figueroa et al., 2014a). In oligotrophic waters, such as 98 those of the Mediterranean, nutrient availability generally limits macroalgal growth (Ferreira et 99 al., 2011), photosynthetic capacity (Pérez-Lloréns et al., 1996) and photoprotective 100 mechanisms (Celis-Plá et al., 2014b). 101 Our study centres upon a highly oligotrophic region (the Tyrrhenian Sea) which is 102 undergoing rapid changes in carbonate chemistry coupled with coastal eutrophication and 103 increased land run-off (Oviedo et al., 2015). In this region, as with elsewhere in the world, 104 canopy-forming brown algae have undergone a decline in abundance due to anthropogenic 105 perturbation (Scherner et al., 2013; Strain et al., 2014; Yesson et al., 2015). Here, we investigate 3 106 the interactive effects of increasing CO2 levels and eutrophication on Cystoseira compressa and 107 Padina pavonica using a pH gradient caused by volcanic seeps. These species were chosen 108 because they are abundant around Mediterranean CO2 seeps (Baggini et al., 2014), because 109 Cystoseira spp. are indicators of high water quality in the Mediterranean (Bermejo et al., 2013) 110 and since Padina spp. tolerate loss of external calcification as CO2 levels increase (Johnson et 111 al., 2012, Pettit et al., 2015). 112 Macroalgal responses to ocean acidification may well depend upon their nutrient 113 metabolism, which can vary widely between species (Hurd et al., 2014; Hofmann et al. 2014). 114 Here, we compared interspecific physiological and biochemical responses to ocean acidification 115 under different light and nutrient levels using standard methods for the study of multiple 116 physical stressors in algae (Martínez et al., 2012; Celis-Plá et al., 2014b). Our hypothesis was 117 that both brown algal species would benefit from ocean acidification in shaded conditions when 118 nutrient levels were elevated. We expected that high light levels would inhibit photosystems, 119 and that any benefits from high CO2 would only occur if sufficient nutrients were available. If 120 this were true we expected to observe increased photosynthetic activity (using electron transport 121 rates and carbon content as a proxy) and increases in phenolic and antioxidant production in 122 shaded nutrient-enriched treatments. 123 124 MATERIALS AND METHODS 125 Experimental design 126 Macroalgal incubations took place from 19 – 22 March 2013, along a CO2 gradient near 127 Vulcano, Italy (Figure 1). Cystoseira compressa and Padina pavonica were collected at 0.5 m 128 depth from a reference zone (Boatta et al., 2013). Thalli (5 g fresh weight) were held in 129 individual mesh cylinders (15 cm long × 5 cm in diameter) set one meter apart and suspended 130 at 0.2 m depth off a floating line that was anchored to the seabed perpendicular to the coast.

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