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Calcification in a changing ocean: perspectives on a virtual symposium in The Biological Bulletin.

Biomineralization is an ancient evolutionally innovation that appeared independently in the major metazoan groups during the Cambrian explosion (Porter, 2007. Science 316: 1302). The rise of biocalcifying organisms and the evolutionary innovation of calcified structures over subsequent millennia was instrumental in generating the great diversity of marine plants, animals, and symbioses present today in our oceans. The selection pressures underlying the appearance of widespread biomineralization over 500 million years ago is not known, but it is thought to have been driven by the Cambrian calcium crisis when the massive rise of seawater [[Ca.sup.2+]] prompted the need for detoxification of this element and led to biological use of [Ca.sup.2+] to make skeletons and shells for protection and support (Brennan et al., 2004. Geology 32: 473-476). Today, modern calcifiers face a new and rapidly escalating crisis caused by warming and acidification of the oceans with a reduction in availability of carbonate minerals, a change driven by the increase in atmospheric C[O.sub.2] due to anthropogenic emissions and industrialization.

This virtual symposium issue of The Biological Bulletin focuses on the challenges that climatic change presents to calcifying marine species. In contributions that span from genomics to ecosystem impacts, we bring together experts that investigate a diversity of calcifying taxa. The first part of the virtual symposium presents a series of timely reviews on the responses of key taxa--foraminiferans, bryozoans, corals, molluscs, and echinoderms--to global change. Also included in this section is the first meta-analysis of the response of whole-organism gene expression to ocean acidification. In the second part of this virtual symposium, three research papers consider the impacts of ocean acidification on coralline algae, molluscan predator-prey interaction, and coccolithophore populations.

Although biomineralized structures appeared independently in many metazoan groups, the biochemical and physiological processes and molecular control have commonalities, and modern "omics" provides important powerful new approaches to tease apart the cellular and molecular mechanisms of building calcified structures (Ettensohn, 2014. Evol. Dev. 16: 139-148) and how this biomineralization "tool kit" will respond to changing ocean conditions. The meta-analysis by Evans and Watson-Wynn (this volume) uses sea urchin larvae as a model system for investigating how modern genomic resources can be used to tease out the effects of ocean acidification on calcification and other important biological processes. A key finding of this meta-analysis is the pervasive genetic changes across key biological functions from metabolism to ion transport and biomineralization. The down-regulation of genes provides a clear indication that metabolic depression, driven by increased organism pC[O.sub.2], and less so by the reduction in carbonate saturation, is the main driver of stunted larval growth seen in many sea urchins in response to ocean acidification (Byrne et al., 2013. Phil. Trans. K. Soc. B 368: 20120439). Biomineralization is impaired by the down-regulation of metabolism, ion transport, skeleton matrix proteins, and to a lesser extent, developmental delay. As more genomic resources become available for marine calcifiers, the emergence of RNA-sequencing technology will allow unprecedented insights into the underlying mechanisms of the "C[O.sub.2] problem" (Doney et al., 2009. Annu. Rev. Mar. Sci. 1 : 169-192).

Two reviews on the impacts of changing ocean conditions on ecologically important tropical symbiotic calcifiers provide a timely assessment on the impacts of climate change on benthic Foraminifera and scleractinian corals. The meta-analysis shows that large benthic foraminiferan species differ in their responses to warming and acidification and that the variation in responses may be influenced by differences in symbiont type (e.g., diatom, dinoflagellate, algae) (Doo et al., this volume). These authors also review carbonate production in these "living sands," stressing their importance in the maintenance of coral islands. The contrasting responses of benthic foraminiferans to warming and acidification are important in identifying species that are likely to be most vulnerable to changing ocean conditions, a feature essential to assessment of risk to the land masses that are maintained by these organisms (Dawson et al., 2014. Geomorphology, doi: 10.1016/j.geomorph.2014. 03.023). The other paper in the virtual symposium on a single cell organism--coccolithophores--found indications that the species diversity of populations of these organisms in the region of C[O.sub.2] vents will be altered in response to ocean acidification (Ziveri et al., this volume).

Tropical reef corals have received a lot of attention with respect to impacts of global change because of the crucial ecosystem services they provide to a plethora of species, including acting as a protective barrier for human populations (Moberg and Folke, 1999. Ecol. Econ. 29: 215-233). In this virtual symposium, the expansive review on coral growth shows the key insights that can be obtained from the historical data obtained from coral cores (Lough and Cantin, this volume). These data on the linear elongation of corals were mostly obtained from cores of massive corals that provide continuous growth records over centuries and can be used to identify the impacts of ocean warming and other stressors. For corals it is clear that increasing sea surface temperature has been the most important ocean change stressor for decades, with two types of responses evident: setbacks in growth due to thermal stress events that cause bleaching, and a general decline in growth as increasing temperatures take corals outside their environmental comfort zone. The susceptibility of calcification in corals to progressive ocean acidification is less clear due to the large background variability in reef carbonate chemistry. There remains much to learn about temporal variation in coral growth with respect to changing ocean conditions through the use of cores, and the authors provide a series of recommendations to enhance the value of the information that can be obtained.

Although bryozoans have been described as a minor phylum, carbonate production by these animals is regionally very important, especially where heavily calcified species provide framework habitat that enhances biodiversity and generate extensive sediment deposits such as in shelf environments (Smith, this volume). This review of growth and calcification in bryozoans and the effects of warming and acidification provides an assessment of the data available and stresses that understanding mineral composition and the surface area of these animals is particularly important to understanding dissolution rate.

While there are extensive data on the impacts of ocean change stressors on the skeleton of the planktonic life phase of echinoderms, impacts on the post-metamorphic echinoderm skeleton are less well understood (Dubois, this volume). It seems that juvenile and adult sea urchins can tolerate ocean acidification conditions, but it is important to consider functional consequences on the mechanical integrity of the skeleton. Sea urchins play key ecological roles, particularly in habitats when they are highly abundant, and so changes in the vulnerability of their skeleton to physical and biotic forces would be expected to impact many marine ecosystems.

There are two contributions on the impacts of ocean acidification on molluscs and the interaction between predator and prey (Kroeker et al., this volume; Wright et al., this volume). An important trend is emerging in the response of bivalves and their gastropod predators to ocean acidification--decreased shell thickness of bivalves makes them more vulnerable to predation on one hand, while increased energetic requirements of predators are likely to result in a per capita increase in predation rates, probably with significant ecosystem effects. The trend in the biomineralization response can be modulated by population genetics, indicating that some bivalve family lines may be more resilient to ocean acidification than others, thus providing the potential for adaptive responses.

Coralline algae are a key component of marine ecosystems and, as calcifiers that produce a high-magnesium calcite that is directly exposed to overlying water, these algae are particularly vulnerable to ocean acidification (Ordonez et al., this volume). In a long-term study of the impacts of ocean acidification on tropical crustose coralline algae (CCA), these authors report significant changes in community composition. In consideration of the essential role that CCAs play on coral reefs in cementing reef infrastructure and as a settlement cue for many marine invertebrate larvae, this change would have significant ecosystem effects.

Marine calcifiers provide key ecosystem services to humanity and it is imperative to understand how adult and planktonic stages of these species will fare in response to contemporary and future change. This virtual symposium issue of The Biological Bulletin presents a broad overview of the impacts of changing ocean conditions on a diverse suite of marine calcifiers. The contributors have identified key knowledge gaps in the fast-evolving field of marine global change biology--with a focus on biocalcification--and have provided many important insights. We, as editors, thank the authors for these insights, which will undoubtedly guide research on the many interesting questions and facets of the issue of Calcification in a Changing Ocean that remain to be addressed and answered.

MARIA BYRNE (1) * AND GRETCHEN E. HOFMANN (2)

(1) Schools of Medical and Biological Sciences, The University of Sydney, New South Wales 2006, Australia; (2) Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, California 93106, USA

* To whom correspondence should be addressed. E-mail: mbyme@ anatomy.usyd.edu.au
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Author:Byrne, Maria; Hofmann, Gretchen E.
Publication:The Biological Bulletin
Geographic Code:1USA
Date:Jun 1, 2014
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