knn McCoy, S. J., and Kamenos, N. A. (2015) Coralline algae (rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change. Journal of Phycology, 51(1). pp. 6-24. Copyright © 2015 The Authors http://eprints.gla.ac.uk/99956/ Deposited on: 06 February 2015 Enlighten – Research publications by members of the University of Glasgow http://eprints.gla.ac.uk J. Phycol. 51, 6–24 (2015) © 2015 The Authors. Journal of Phycology published by Wiley Periodicals, Inc. on behalf of Phycological Society of America. DOI: 10.1111/jpy.12262 R EVIEW CORALLINE ALGAE (RHODOPHYTA) IN A CHANGING WORLD: INTEGRATING ECOLOGICAL, PHYSIOLOGICAL, AND GEOCHEMICAL RESPONSES TO GLOBAL CHANGE1 Sophie J. McCoy2,3 Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th Street, Chicago, Illinois 60637, USA and Nicholas A. Kamenos School of Geographical and Earth Sciences, University of Glasgow University Avenue, Glasgow G12 8QQ, UK Abbreviations Coralline algae are globally distributed benthic : CaCO3, calcium carbonate; CCA, crustose coralline algae; CO , carbon dioxide; primary producers that secrete calcium carbonate À 2 CO 2 , carbonate; DIC, dissolved inorganic carbon; skeletons. In the context of ocean acidification, they 3 À have received much recent attention due to the HCO3 , bicarbonate; OA, ocean acidification; PAR, potential vulnerability of their high-Mg calcite photosynthetically active radiation; SST, sea surface skeletons and their many important ecological roles. temperature Herein, we summarize what is known about coralline algal ecology and physiology, providing context to understand their responses to global climate change. We review the impacts of these changes, including Coralline algae (Corallinales and Sporolithales, ocean acidification, rising temperatures, and Corallinophycidae, Rhodophyta) are receiving pollution, on coralline algal growth and calcification. renewed attention across the ecological and geologi- We also assess the ongoing use of coralline algae as cal sciences as important organisms in the context of marine climate proxies via calibration of skeletal global environmental change, especially ocean acidifi- morphology and geochemistry to environmental cation (OA). In addition to their important functional conditions. Finally, we indicate critical gaps in our roles in ecological systems across latitudes and habitat understanding of coralline algal calcification and types (e.g., reef frameworks, Adey 1998, Chisholm 2À physiology and highlight key areas for future 2000, carbonate (CO3 ) production, Bosence 1980, research. These include analytical areas that recently foundational species, Steneck and Dethier 1994, larval have become more accessible, such as resolving settlement, Daume et al. 1999, fish nurseries, Kame- phylogenetic relationships at all taxonomic ranks, nos et al. 2004a), coralline algae are increasingly used elucidating the genes regulating algal photosynthesis as paleoecological proxies (e.g., Cabioch et al. 1999, and calcification, and calibrating skeletal geochemical Braga and Aguirre 2001, Perry 2001, Aguirre et al. metrics, as well as research directions that are broadly 2007) and accurate paleoenvironmental recorders applicable to global change ecology, such as the (e.g., Halfar et al. 2000, Kamenos 2010, Williams et al. importance of community-scale and long-term 2011), thus providing a valuable mechanism for con- experiments in stress response. textualizing recent oceanic changes. Key index words: Coralline diversification reveals the ability of this calcification; climate change; coral- group to colonize a wide range of light, temperature, line algae; crustose coralline algae; ecology; ecosys- and energy conditions and to remain chief compo- tem services; ocean acidification; paleoclimate; nents of benthic marine communities through paleoclimate proxies; photosynthesis; physiology considerable fluctuations in temperature and light over geologic time (Aguirre et al. 2000). Much is known about coralline algal ecology and physiology, 1Received 18 April 2014. Accepted 3 October 2014. despite the great variety in ecological forms and cryp- 2Present address: Plymouth Marine Laboratory, Prospect Place, tic diversity emerging from molecular studies. Here, The Hoe, Plymouth, PL1 3DH, UK. we point the reader to previous reviews of the basic 3 Author for correspondence: e-mail [email protected]. ecology and physiology of coralline algae (Table 1) Editorial Responsibility: P. Gabrielson (Associate Editor) and focus on new insights into the potential This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and responses of coralline algae to environmental change reproduction in any medium, provided the original work is properly at different scales, including responses of physiology, cited. skeletal mineralogy, ecology, and ecosystem services. 6 CORALLINE ALGAE IN A CHANGING WORLD 7 CORALLINE ALGAL ECOLOGY Nongeniculate (crustose and rhodolith forms). Non- geniculate coralline algae, or coralline algae lacking Reference Littler 1984 Macintyre 1973 Nelson 2009 Adey et al.Foster 2013 et al. 2013 Aguirre et al.Foster 2000 2001 Wilson et al. 2004 Steneck 1983 Bosence 1983 Littler and Steneck 1985 Steneck 1986 Woelkerling 1988 Littler 1972 Adey and Johansen 1981 noncalcified articulations (genicula) between calci- fied segments (Fig. 1, A and B), are some of the most abundant organisms throughout the hard-bot- 9 9 tom marine photic zone (Adey and Macintyre 1973, Steneck 1986). This group includes crustose and rhodolith (or maerl) morphologies (Foster 2001). Nomenclature of free-living forms is often inconsis- R tent in the literature, which describes “coatings,” EVIEW “gravels,” “rhodolites,” and most commonly “maerl” and “rhodoliths” (Steneck 1986). This terminology can be confusing, given that several species of non- geniculate coralline algae have been observed within 99 an individual rhodolith or coated pebble (Basso 1998, Yabur-Pacheco and Riosmena-Rodrıguez 2006). We thus refer to all forms not attached to hard-bottom substratum or other macroalgae 9999 9999 999 99999 99999 99999 99999 (including coralline algae) as rhodoliths, following the nomenclature of Foster (2001). Correspond- ingly, we define the term crustose coralline to refer Growth form Latitude Timescale to all forms that grow roughly radially on hard sub- strates and exhibit determinate thickness <1 cm. Many nongeniculate species are thought to exist in both rhodolith and crustose forms. However, we will occasionally separate our discussion of these two morphological groups due to some important differ- ences in ecology and ecosystem services. Nongeniculate coralline algae can be found on any hard substrate where light penetrates (Bosence 1983). They thrive in areas of moderate disturbance 9 9 and often dominate in areas of high stress and dis- turbance potential where many other macrophytes are absent (Steneck 1986, Dethier 1994). This includes areas of high herbivory, wave action, sand scour, and low productivity potential such as the low photic zone, shaded understories of large macro- phyte beds, and the intertidal zone (Kendrick 1991, Dethier 1994, Steneck and Dethier 1994, Dethier and Steneck 2001). Crustose forms often cover a high proportion of primary space despite a relatively flat morphology that makes them easy to overgrow (Dethier and Steneck 2001). Such areas are referred 99 to as crustose coralline carpets (Paine 1984). Carbonate production Calcification Phylogenetics Taxonomy Sclerochronology Geniculate Nongeniculate Tropical Temperate Modern Paleo Citation Rhodoliths are a morphologically diverse group of nongeniculate coralline algae, shaped like spheres, branching twigs, or fans and ranging from roughly 1–100 cm in size (Foster et al. 2013). Rhodolith beds tend to form on fairly level bottoms that have suffi- cient, but often low light, and occur in areas with 99 9 99999 999 99 99 9 99 moderate water motion and high bioturbation to prevent the burial of rhodoliths in sediment (Steller and Foster 1995, Connell 2003, Wilson et al. 2004, 9 99 9 9Harrington et 9 al. 9 9 9 99 2005). Unlike crustose coralline carpets, rhodolith beds form in the absence of 1. Summary of previous reviews on the subject of coralline algae published in the last 40 years. intense water movement, which could scatter or bury 99 9 9 9 9 9 9 99 99 9 9 9 9 9 9 9 9 9 9 9999 9 9999 slow-growing rhodoliths (Nelson 2009, Foster et al. ABLE Life history Physiology Ecology Biogeography T Discipline 8 SOPHIE J. MCCOY AND NICHOLAS A. KAMENOS FIG.1.Examplesof(A)rhodo- lith (maerl), (B) crustose, and (C) geniculate growth forms of red coralline algae. Scale bars are 10 cm, 1 cm, and 5 mm, respectively. Source:(A)PhotobyN.A.Kamenos, (B and C) photos by S.J. McCoy. EVIEW R Rhodolith/Maerl Crustose Articulated Non-geniculate growth forms Geniculate growth form 2013). Rhodolith beds can range several square kilo- structure is generally hierarchical and dictated by meters in tropical and temperate settings (Foster thallus thickness, edge morphology, and growth 2001, Nelson 2009, Amado-Filho et al. 2012, Foster rate, reversals in the competitive hierarchy are com- et al. 2013), and therefore play a significant role in mon and typically mediated by herbivores (Paine calcium carbonate (CaCO3) production on conti- 1984, Steneck et al. 1991). A particular species’ nental shelves (Amado-Filho et al. 2012). competitive ability thus depends on its growth strat-