Effects of Ocean Acidification on Sediment Fauna

The vast majority of the seafloor is covered not in rocky or biogenic reefs but in unconsolidated sediments and, consequently, the majority of marine biodiversity consists of invertebrates either residing in (infauna) or on (epifauna) sediments (Snelgrove 1999). The biodiversity within these sediments is a result of complex interactions between the underlying environmental conditions (e.g. depth, temperature, organic supply, and granulometry) and the biological interactions operating between organisms (e.g. predation and competition). Not only are sediments important depositories of biodiversity but they are also critical components in many key ecosystem functions. Nowhere is this more apparent than in shallow coastal seas and oceans which, despite covering less than 10% of the earth’s surface, deliver up to 30% of marine production and 90% of marine fisheries (Gattuso et al. 1998). These areas are also the site for 80% of organic matter burial and 90% of sedimentary mineralization and nutrient–sediment biogeochemical processes. They also act as the sink for up to 90% of the suspended load in the world’s rivers and the many associated contaminants this material contains (Gattuso et al. 1998). Human beings depend heavily on the goods and services provided, for free, by the marine realm (Hassan et al. 2005 ) and it is no coincidence that nearly 70% of all humans live within 60 km of the sea or that 75% of all cities with more than 10 million inhabitants are in the coastal zone (Small and Nicholls 2003; McGranahan et al. 2007) Given these facts, it is clear that any broad-scale environmental impact that affects the diversity, structure, and function of sediment ecosystems could have a considerable impact on human health and well-being. It is therefore essential that the impacts of ocean acidification on sediment fauna, and the ecosystem functions they support, are adequately considered. This chapter will first describe the geochemical environment within which sediment organisms live. It will then explore the role that sediment organisms play as ecosystem engineers and how they alter the environment in which they live and the overall biodiversity of sediment communities.

Effects of Ocean Acidification on Nektonic Organisms

The average surface-ocean pH is reported to have declined by more than 0.1 units from the pre-industrial level ( Orr et al. 2005 ), and is projected to decrease by another 0.14 to 0.35 units by the end of this century, due to anthropogenic CO2 emissions (Caldeira and Wickett 2005 ; see also Chapters 3 and 14). These global-scale predictions deal with average surface-ocean values, but coastal regions are not well represented because of a lack of data, complexities of nearshore circulation processes, and spatially coarse model resolution (Fabry et al. 2008 ; Chapter 3 ). The carbonate chemistry of coastal waters and of deeper water layers can be substantially different from that in surface water of offshore regions. For instance, Frankignoulle et al. ( 1998 ) reported pCO2 (note 1) levels ranging from 500 to 9400 μatm in estuarine embayments (inner estuaries) and up to 1330 μatm in river plumes at sea (outer estuaries) in Europe. Zhai et al. (2005) reported pCO2 values of > 4000 μatm in the Pearl River Estuary, which drains into the South China Sea. Similarly, oxygen minimum layers show elevated pCO2 levels, associated with the degree of hypoxia (Millero 1996). These findings suggest that some coastal and mid-water animals, both pelagic and benthic, are regularly experiencing hypercapnic hypercapnic conditions (i.e. elevated pCO2 levels), that reach beyond those projected in the offshore surface ocean. These organisms might, therefore, be preadapted to relatively high ambient pCO2 levels. The anthropogenic signal will nonetheless be superimposed on the pre-existing natural variability. These phenomena lead to the question of whether future changes in the ocean’s carbonate chemistry pose a serious problem for marine organisms. Those with calcareous skeletons or shells, such as corals and some plankton, have been at the centre of scientific interest. However, elevated CO2 levels may also have detrimental effects on the survival, growth, and physiology of marine animals more generally (Pörtner and Reipschläger 1996; Seibel and Fabry 2003; Fabry et al. 2008; Pörtner 2008; Melzner et al. 2009a).

Past Changes in Ocean Carbonate Chemistry

Over the period from 1750 to 2000, the oceans have absorbed about one-third of the carbon dioxide (CO2) emitted by humans. As the CO2 dissolves in seawater, the oceans become more acidic and between 1750 and 2000, anthropogenic CO2 emissions have led to a decrease of surface-ocean total pH (pH T) by ~0.1 units from ~8.2 to ~8.1 (see Chapters 1 and 3). Surface-ocean pHT has probably not been below ~8.1 during the past 2 million years (Hönisch et al. 2009). If CO2 emissions continue unabated, surface-ocean pH T could decline by about 0.7 units by 2300 (Zeebe et al. 2008). With increasing CO2 and decreasing pH, carbonate ion (CO32–) concentrations decrease and those of bicarbonate (HCO-3) rise. With declining CO32– concentration ([CO32–]), the stability of the calcium carbonate (CaCO3) mineral structure, used extensively by marine organisms to build shells and skeletons, is reduced. Other geochemical consequences include changes in trace metal speciation (Millero et al. 2009 ) and even sound absorption ( Hester et al. 2008 ; Ilyina et al. 2010 ). Do marine organisms and ecosystems really ‘care’ about these chemical changes? We know from a large number of laboratory, shipboard, and mesocosm experiments, that many marine organisms react in some way to changes in their geochemical environment like those that might occur by the end of this century (see Chapters 6 and 7). Generally (but not always), calcifying organisms produce less CaCO3, while some may put on more biomass. Extrapolating such experiments would lead us to expect potentially significant changes in ecosystem structure and nutrient cycling. But can one really extrapolate an instantaneous environmental change to one occurring on a timescale of a century? What capability, if any, do organisms have to adapt to future ocean acidification which is occurring on a slower timescale than can be replicated in the laboratory? Simultaneous changes in ocean temperature and nutrient supply as well as in organisms’ predation environment may create further stresses or work to ameliorate the effect of changes in ocean chemistry.

Biogeochemical Consequences of Ocean Acidification and Feedbacks to the Earth System

By the year 2008, the ocean had taken up approximately 140 Gt carbon corresponding to about a third of the total anthropogenic CO2 emitted to the atmosphere since the onset of industrialization (Khatiwala et al. 2009 ). As the weak acid CO2 invades the ocean, it triggers changes in ocean carbonate chemistry and ocean pH (see Chapter 1). The pH of modern ocean surface waters is already 0.1 units lower than in pre-industrial times and a decrease by 0.4 units is projected by the year 2100 in response to a business-as- usual emission pathway (Caldeira and Wickett 2003). These changes in ocean carbonate chemistry are likely to affect major ocean biogeochemical cycles, either through direct pH effects or indirect impacts on the structure and functioning of marine ecosystems. This chapter addresses the potential biogeochemical consequences of ocean acidification and associated feedbacks to the earth system, with focus on the alteration of element fluxes at the scale of the global ocean. The view taken here is on how the different effects interact and ultimately alter the atmospheric concentration of radiatively active substances, i.e. primarily greenhouse gases such as CO2 and nitrous oxide (N2O). Changes in carbonate chemistry have the potential for interacting with ocean biogeochemical cycles and creating feedbacks to climate in a myriad of ways (Box 12.1). In order to provide some structure to the discussion, direct and indirect feedbacks of ocean acidification on the earth system are distinguished. Direct feedbacks are those which directly affect radiative forcing in the atmosphere by altering the air–sea flux of radiatively active substances. Indirect feedbacks are those that first alter a biogeochemical process in the ocean, and through this change then affect the air–sea flux and ultimately the radiative forcing in the atmosphere. For example, when ocean acidification alters the production and export of organic matter by the biological pump, then this is an indirect feedback. This is because a change in the biological pump alters radiative forcing in the atmosphere indirectly by first changing the nearsurface concentrations of dissolved inorganic carbon and total alkalinity.

Effects of Ocean Acidification on Marine Biodiversity and Ecosystem Function

The biodiversity of the oceans, including the striking variation in life forms from microbes to whales and ranging from surface waters to hadal trenches, forms a dynamic biological framework enabling the flow of energy that shapes and sustains marine ecosystems. Society relies upon the biodiversity and function of marine systems for a wide range of services as basic as producing the seafood we consume or as essential as generating much of the oxygen we breathe. Perhaps most obvious is the global seafood harvest totalling over 100 Mt yr–1 (82 and 20 Mt in 2008 for capture and aquaculture, respectively; FAO 2009) from fishing effort that expands more broadly and deeper each year as fishery stocks are depleted (Pauly et al. 2003). Less apparent ecosystem services linked closely to biodiversity and ecosystem function are waste processing and improved water quality, elemental cycling, shoreline protection, recreational opportunities, and aesthetic or educational experiences (Cooley et al. 2009). There is growing concern that ocean acidification caused by fossil fuel emissions, in concert with the effects of other human activities, will cause significant changes in the biodiversity and function of marine ecosystems, with important consequences for resources and services that are important to society. Will the effects of ocean acidification on ecosystems be similar to those arising from other environmental perturbations observed during human or earth history? Although changes in biodiversity and ecosystem function due to ocean acidification have not yet been widely observed, their onset may be difficult to detect amidst the variability associated with other human and non-human factors, and the greatest impacts are expected to occur as acidification intensifies through this century. In theory, large and rapid environmental changes are expected to decrease the stability and productivity of ecosystems due to a reduction in biodiversity caused by the loss of sensitive species that play important roles in energy flow (i.e. food web function) or other processes (e.g. ecosystem engineers; Cardinale et al. 2006). In practice, however, most research concerning the biological effects of ocean acidification has focused on aspects of the performance and survival of individual species during short-term studies, assuming that a change in individual performance will influence ecosystem function.

Ocean Acidification: Knowns, Unknowns, and Perspectives

Although the changes in the chemistry of seawater driven by the uptake of CO2 by the oceans have been known for decades, research addressing the effects of elevated CO2 on marine organisms and ecosystems has only started recently (see Chapter 1). The first results of deliberate experiments on organisms were published in the mid 1980s (Agegian 1985) and those on communities in 2000 (Langdon et al. 2000; Leclercq et al. 2000 ). In contrast, studies focusing on the response of terrestrial plant communities began much earlier, with the first results of free-air CO2 enrichment experiments (FACE) being published in the late 1960s (see Allen 1992 ). Not surprisingly, knowledge about the effects of elevated CO2 on the marine realm lags behind that concerning the terrestrial realm. Yet ocean acidification might have significant biological, ecological, biogeochemical, and societal implications and decision-makers need to know the extent and severity of these implications in order to decide whether they should be considered, or not, when designing future policies. The goals of this chapter are to summarize key information provided in the preceding chapters by highlighting what is known and what is unknown, identify and discuss the ecosystems that are most at risk, as well as discuss prospects and recommendation for future research. The chemical, biological, ecological, biogeochemical, and societal implications of ocean acidification have been comprehensively reviewed in the previous chapters with one minor exception. Early work has shown that ocean acidification significantly affects the propagation of sound in seawater and suggested possible consequences for marine organisms sensitive to sound (Hester et al . 2008). However, sub sequent studies have shown that the changes in the upper-ocean sound absorption coefficient at future pH levels will have no or a small impact on ocean acoustic noise (Joseph and Chiu 2010; Udovydchenkov et al . 2010). The goal of this section is to condense the current knowledge about the consequences of ocean acidification in 15 key statements. Each statement is given levels of evidence and, when possible, a level of confidence as recommended by the Intergovernmental Panel on Climate Change (IPCC) for use in its 5th Assessment Report (Mastrandrea et al. 2010).

The Ocean Acidification Challenges Facing Science and Society

Human development, inspiration, invention, and aspiration have resulted in a rapidly growing population, with each generation aspiring to greater wealth and well-being, so having greater needs than the previous generation. Amongst the resulting negative impacts are over-exploitation of planetary resources and the build-up of gases in the atmosphere and oceans to the extent that they are changing earth’s climate and ocean chemistry (IPCC 2007). However, the history of humanity’s relationship to the environment has shown that, if threatened, society can respond rapidly to environmental risks, introducing better practices, controls, regulations, and even global protocols, for example the reduction of city smog, the move from leaded to unleaded petrol, and reduction of chlorofluorocarbon (CFC) production to reduce loss of the ozone layer. Nearly all of these changes have led to direct and obvious positive gain to human health and well-being which has been a driving force in the production, agreement and implementation of the policies and laws that have brought them about. The spatial scale or ‘ecological footprint’ of these risks has increased with time, such that international agreements and protocols, like the Montreal Protocol for CFCs, have been increasingly necessary for reducing them. Along with the globalization of agriculture, business, industry, and financial markets and the expansion of the human population goes the globalization of risk to the environment. Climate change and ocean acidification are global issues with solutions that are only possible through global agreements and action. Substantial proportions of nations’ gross domestic product (GDP) were used to secure the banks and major industries in the economic crises that have swept the world in the last few years, far greater than the 1 to 2% per annum estimated to be required to mitigate climate change (Stern 2006). However, the response to the economic crisis does show that global society can react rapidly when it believes it is necessary. The question is, when do society and governments deem it necessary to act, and to act together? One issue may be time, the perceived immediacy of the crisis.

Effects of Ocean Acidification on the Marine Source of Atmospherically Active Trace Gases

A wide range of trace gases, including dimethyl sulphide (DMS) and organohalogens, are formed in the surface oceans via biological and/or photochemical processes. Consequently, these gases become supersaturated in seawater relative to the overlying marine air, leading to a net flux to the atmosphere. Upon entering the atmosphere, they are subject to rapid oxidation or radical attack to produce highly reactive radical species which are involved in a number of important atmospheric and climatic processes. Organohalogens can affect the oxidizing capacity of the atmosphere by interacting with ozone, with implications for air quality, stratospheric ozone levels, and global radiative forcing. DMS and iodine-containing organohalogens (iodocarbons) can both contribute to direct and indirect impacts of aerosols on climate through the production of new particles and cloud condensation nuclei (CCN) in the clean marine atmosphere. Therefore, marine trace gases are considered a vital component of the earth’s climate system, and changes in the net production rate and subsequent sea-to-air flux could have an impact on globally important processes. In recent years, attention has turned to the impact that future ocean acidification may have on the production of such gases, with the greatest focus on DMS and organohalogens. In this chapter, the current state-of-the-art in this growing area of research is outlined. The oceans are a major source of sulphur (S), an element essential to all life, and marine emissions of the gas DMS (chemical formula (CH3)2S) represent a key pathway in the global biogeochemical sulphur cycle. The surface oceans are supersaturated with DMS relative to the atmosphere, resulting in a oneway flux from sea to air (Lovelock et al. 1972; Watson and Liss 1998). DMS is a breakdown product of the biogenically produced dimethyl sulphoniopropionate (DMSP): . . . (CH3)2S+CH2CH2COO- → (CH3)2S + CH2CHCOOH (acrylic acid) (11.1) . . . Single-celled marine phytoplankton are the chief producers of DMSP, and this reaction is catalysed intra- and extracellularly by the enzyme DMSP-lyase (Malin et al. 1992; Liss et al. 1997). The capacity of phytoplankton to produce DMSP varies between species, with prymnesiophytes considered to be the most prolific (Malin et al. 1992 ; Liss et al. 1997 ; Watson and Liss 1998).

Effects of Ocean Acidification on the Diversity and Activity of Heterotrophic Marine Microorganisms

Microbe-mediated processes are crucial for biogeochemical cycles and the functioning of marine ecosystems (Azam and Malfatti 2007 ). If these processes are affected by ocean acidification, major consequences can be expected for the functioning of the global ocean and the systems that it influences, such as the atmosphere. In contrast to phytoplankton, which have been relatively well studied (see Chapter 6), there is comparatively little information on the effect of ocean acidification on heterotrophic microorganisms. Two reviews on the potential effects of ocean acidification on microbial plankton have recently been published (Liu et al. 2010 ; Joint et al. 2011) . In a recent perspective paper, Joint et al. (2011) concluded that marine microbes possess the flexibility to accommodate pH change and that major changes in marine biogeochemical processes that are driven by microorganisms are unlikely. Narrative reviews, which look at some of the relevant literature, are potentially biased and could lead to misleading conclusions (Gates 2002). Metaanalysis was developed to overcome most biases of narrative reviews. It statistically combines the results (effect size) of several studies that address a shared research hypothesis. Liu et al. (2010) used a metaanalytic approach to comprehensively review the current understanding of the effect of ocean acidification on microbes (including phytoplankton) and microbial processes, and to highlight the gaps that need to be addressed in future research. In the following, a brief digest on oceanic microbes and their role is provided for readers unfamiliar with this topic. Then the research that has been performed to assess the effects of ocean acidification on the diversity and activity of heterotrophic marine microorganisms is reviewed. Finally, scenarios are developed and potential implications are discussed. Microorganisms are defined as organisms that are microscopic, i.e. too small to be seen by the naked human eye, and mostly comprise single-celled organisms. Viruses are sometimes also included in this definition but it is hotly debated whether viruses are alive or not (Raoult and Forterre 2008). The current phylogeny considers three domains of cellular life, the Bacteria, the Archaea and the Eukarya.

Recent and Future Changes in Ocean Carbonate Chemistry

This chapter is about the ongoing human-induced shifts in fundamental ocean carbonate chemistry that are occurring globally and are a growing concern to scientists studying marine organisms. It reviews the current state of ocean pH and related carbonate system variables, how they have changed during the industrial era, and how they are expected to continue to change during this century and beyond. Surface-ocean pH has been relatively stable for millions of years, until recently. Over the 800 000 years prior to industrialization, average surfacewater pH oscillated between 8.3 during cold periods (e.g. during the Last Glacial Maximum, 20 000 yr ago) and 8.2 during warm periods (e.g. just prior to the Industrial Revolution), as reviewed by Zeebe and Ridgwell in Chapter 2. But human activities are upsetting this stability by adding large quantities of a weak acid to the ocean at an ever increasing rate. This anthropogenic problem is referred to as ocean acidification because ocean acidity is increasing (i.e. seawater pH is declining), even though surface-ocean waters are alkaline and will remain so. The cause of the decline in seawater pH is the atmospheric increase in the same gas that is the main driver of climate change, namely carbon dioxide (CO2). Due to increasing atmospheric CO2 concentrations, the ocean takes up large amounts of anthropogenic CO2, currently at a rate of about 106 metric tons of CO2 per hour (Brewer 2009), which is equivalent to one-fourth of the current global CO2 emissions from combustion of fossil fuels, cement production, and deforestation (Canadell et al. 2007 ; Le Quéré et al. 2009 ). If we would partition these emissions equally per capita, each person on the planet would be responsible for 4 kg per day of anthropogenic CO2 invading the ocean. To grasp the size of the problem, this invisible invasion may be compared with a recent, highly visible environmental disaster. The ocean currently absorbs anthropogenic carbon at a rate that is about a thousand times greater than from when carbon escaped from the BP Deepwater Horizon oil well that exploded on 20 April 2010, releasing 57 000 barrels of petroleum per day into the Gulf of Mexico until it was capped almost 3 months later.