Chapter five – stress biology and immunology in Nephrops norvegicus

The Norway lobster Nephrops norvegicus lives at low-light depths, in muddy substrata of high organic content where water salinities are high and fluctuations in temperature are moderate. In this environment, the lobsters are naturally exposed to a number of potential stressors, many of them as a result of the surficial breakdown of organic material in the sediment. This process (early diagenesis) creates a heterogeneous environment with temporal and spatial fluctuations in a number of compounds such as oxygen, ammonia, metals, and hydrogen sulphide. In addition to this, there are anthropogenically generated stressors, such as human-induced climate change (resulting in elevated temperature and ocean acidification), pollution and fishing. The lobsters are thus exposed to several stressors, which are strongly linked to the habitat in which the animals live. Here, the capacity of Nephrops to deal with these stressors is summarised. Eutrophication-induced hypoxia and subsequent metal remobilisation from the sediment is a well-documented effect found in some wild Nephrops populations. Compared to many other crustacean species, Nephrops is well adapted to tolerate periods of hypoxia, but prolonged or severe hypoxia, beyond their tolerance level, is common in some areas. When the oxygen concentration in the environment decreases, the bioavailability of redox-sensitive metals such as manganese increases. Manganese is an essential metal, which, taken up in excess, has a toxic effect on several internal systems such as chemosensitivity, nerve transmission and immune defence. Since sediment contains high concentrations of metals in comparison to sea water, lobsters may accumulate both essential and non-essential metals. Different metals have different target tissues, though the hepatopancreas, in general, accumulates high concentrations of most metals. The future scenario of increasing anthropogenic influences on Nephrops habitats may have adverse effects on the fitness of the animals.

The marine carbon system and ocean acidification during Phanerozoic time

The global CO₂-carbonic acid-carbonate system of seawater, although certainly a well-researched topic of interest in the past, has risen to the fore in recent years because of the environmental issue of ocean acidification (often simply termed OA). Despite much previous research, there remain pressing questions about how this most important chemical system of seawater operated at the various time scales of the deep time of the Phanerozoic Eon (the past 545 Ma of Earth’s history), interglacial-glacial time, and the Anthropocene (the time of strong human influence on the behaviour of the system) into the future of the planet. One difficulty in any analysis is that the behaviour of the marine carbon system is not only controlled by internal processes in the ocean, but it is intimately linked to the domains of the atmosphere, continental landscape, and marine carbonate sediments.

For the deep-time behaviour of the system, there exists a strong coupling between the states of various material reservoirs resulting in an homeostatic and self-regulating system. As a working hypothesis, the coupling produces two dominant chemostatic modes: (Mode I), a state of elevated atmospheric CO₂, warm climate, and depressed seawater Mg∕Ca and SO₄∕Ca mol ratios, pH (extended geologic periods of ocean acidification), and carbonate saturation states, and elevated Sr concentrations, with calcite and dolomite as dominant minerals found in marine carbonate sediments (Hothouses, the calcite-dolomite seas), and (Mode II), a state of depressed atmospheric CO₂, cool climate, and elevated seawater Mg∕Ca and SO₄/Ca ratios, pH, and carbonate saturation states, and low Sr concentrations, with aragonite and high magnesian calcites as dominant minerals found in marine carbonate sediments (Icehouses, the aragonite seas).

Investigation of the impacts of deglaciation and anthropogenic inputs on the CO₂–H₂O–CaCO₃ system in global coastal ocean waters from the Last Glacial Maximum (LGM: the last great continental glaciation of the Pleistocene Epoch, 18,000 year BP) to the year 2100 shows that with rising sea level, atmospheric CO₂, and temperature, the carbonate system of coastal ocean water changed and will continue to change significantly. We find that 6,000 Gt of C were emitted as CO₂ to the atmosphere from the growing coastal ocean from the Last Glacial Maximum to late preindustrial time because of net heterotrophy (state of gross respiration exceeding gross photosynthesis) and net calcification processes. Shallow-water carbonate accumulation alone from the Last Glacial Maximum to late preindustrial time could account for ~24 ppmv of the ~100 ppmv rise in atmospheric CO₂, lending some support to the ‘‘coral reef hypothesis’’. In addition, the global coastal ocean is now, or soon will be, a sink of atmospheric CO₂, rather than a source. The pHT (pH values on the total proton scale) of global coastal seawater has decreased from ~8.35 to ~8.18 and the CO₃^2- ion concentration declined by ~19% from the Last Glacial Maximum to late preindustrial time. In comparison, the decrease in coastal water pHT from the year 1900 to 2000 was ~8.18 to ~8.08 and is projected to decrease further from about ~8.08 to ~7.85 between 2000 and 2100. During these 200 years, the CO₃^2- ion concentration will fall by ~ 45%. This decadal rate of decline of the CO₃^2- ion concentration in the Anthropocene is 214 times the average rate of decline for the entire Holocene!

In terms of the modern problem of ocean acidification and its effects, the “other CO₂ problem”, we emphasise that most experimental work on a variety of calcifying organisms has shown that under increased atmospheric CO₂ levels (which attempt to mimic those of the future), and hence decreased seawater CO₃^2- ion concentration and carbonate saturation state, most calcifying organisms will not calcify as rapidly as they do under present-day CO₂ levels. In addition, we conclude that dissolution of the highly reactive carbonate phases, particularly the biogenic and cementing magnesian calcite phases, on reefs will not be sufficient to alter significantly future changes in seawater pH and lead to a buffering of the CO₂-carbonic acid system in waters bathing reefs and other carbonate ecosystems on timescales of decades to centuries. Because of decreased calcification rates and increased dissolution rates in a future higher CO₂, warmer world with seas of lower pH and carbonate saturation state, the rate of accretion of carbonate structures is likely to slow and dissolution may even exceed calcification. The potential of increasing nutrient and organic carbon inputs from land, occurrences of mass bleaching events, and increasing intensity (and perhaps frequency of hurricanes and cyclones as a result of sea surface warming) will only complicate matters more. This composite of stresses will have severe consequences for the ecosystem services that reefs perform, including acting as a fishery, a barrier to storm surges, a source of carbonate sediment to maintain beaches, and an environment of aesthetic appeal to tourist and local populations. It seems obvious that increasing rates of dissolution and bioerosion owing to ocean acidification will result in a progressively increasing calcium carbonate (CaCO₃) deficit in the CaCO₃ budget for many coral reef environments. The major questions that require answers are: will this deficit occur and when and to what extent will the destructive processes exceed the constructive processes?

Potential acidification impacts on zooplankton in CCS leakage scenarios

Carbon capture and storage (CCS) technologies involve localized acidification of significant volumes of seawater, inhabited mainly by planktonic species. Knowledge on potential impacts of these techniques on the survival and physiology of zooplankton, and subsequent consequences for ecosystem health in targeted areas, is scarce. The recent literature has a focus on anthropogenic greenhouse gas emissions into the atmosphere, leading to enhanced absorption of CO₂ by the oceans and a lowered seawater pH, termed ocean acidification. These studies explore the effects of changes in seawater chemistry, as predicted by climate models for the end of this century, on marine biota. Early studies have used unrealistically severe CO₂/pH values in this context, but are relevant for CCS leakage scenarios. Little studied meso- and bathypelagic species of the deep sea may be especially vulnerable, as well as vertically migrating zooplankton, which require significant residence times at great depths as part of their life cycle.

Interactive effects of global climate change and pollution on marine microbes: the way ahead

Global climate change has the potential to seriously and adversely affect marine ecosystem functioning. Numerous experimental and modeling studies have demonstrated how predicted ocean acidification and increased ultraviolet radiation (UVR) can affect marine microbes. However, researchers have largely ignored interactions between ocean acidification, increased UVR and anthropogenic pollutants in marine environments. Such interactions can alter chemical speciation and the bioavailability of several organic and inorganic pollutants with potentially deleterious effects, such as modifying microbial-mediated detoxification processes. Microbes mediate major biogeochemical cycles, providing fundamental ecosystems services such as environmental detoxification and recovery. It is, therefore, important that we understand how predicted changes to oceanic pH, UVR, and temperature will affect microbial pollutant detoxification processes in marine ecosystems. The intrinsic characteristics of microbes, such as their short generation time, small size, and functional role in biogeochemical cycles combined with recent advances in molecular techniques (e.g., metagenomics and metatranscriptomics) make microbes excellent models to evaluate the consequences of various climate change scenarios on detoxification processes in marine ecosystems. In this review, we highlight the importance of microbial microcosm experiments, coupled with high-resolution molecular biology techniques, to provide a critical experimental framework to start understanding how climate change, anthropogenic pollution, and microbiological interactions may affect marine ecosystems in the future.

Impacts of ocean acidification on marine shelled molluscs

Over the next century, elevated quantities of atmospheric CO₂ are expected to penetrate into the oceans, causing a reduction in pH (−0.3/−0.4 pH unit in the surface ocean) and in the concentration of carbonate ions (so-called ocean acidification). Of growing concern are the impacts that this will have on marine and estuarine organisms and ecosystems. Marine shelled molluscs, which colonized a large latitudinal gradient and can be found from intertidal to deep-sea habitats, are economically and ecologically important species providing essential ecosystem services including habitat structure for benthic organisms, water purification and a food source for other organisms. The effects of ocean acidification on the growth and shell production by juvenile and adult shelled molluscs are variable among species and even within the same species, precluding the drawing of a general picture. This is, however, not the case for pteropods, with all species tested so far, being negatively impacted by ocean acidification. The blood of shelled molluscs may exhibit lower pH with consequences for several physiological processes (e.g. respiration, excretion, etc.) and, in some cases, increased mortality in the long term. While fertilization may remain unaffected by elevated pCO₂, embryonic and larval development will be highly sensitive with important reductions in size and decreased survival of larvae, increases in the number of abnormal larvae and an increase in the developmental time. There are big gaps in the current understanding of the biological consequences of an acidifying ocean on shelled molluscs. For instance, the natural variability of pH and the interactions of changes in the carbonate chemistry with changes in other environmental stressors such as increased temperature and changing salinity, the effects of species interactions, as well as the capacity of the organisms to acclimate and/or adapt to changing environmental conditions are poorly described.

Predicting the response of molluscs to the impact of ocean acidification

Elevations in atmospheric carbon dioxide (CO₂) are anticipated to acidify oceans because of fundamental changes in ocean chemistry created by CO₂ absorption from the atmosphere. Over the next century, these elevated concentrations of atmospheric CO₂ are expected to result in a reduction of the surface ocean waters from 8.1 to 7.7 units as well as a reduction in carbonate ion (CO₃²⁻) concentration. The potential impact that this change in ocean chemistry will have on marine and estuarine organisms and ecosystems is a growing concern for scientists worldwide. While species-specific responses to ocean acidification are widespread across a number of marine taxa, molluscs are one animal phylum with many species which are particularly vulnerable across a number of life-history stages. Molluscs make up the second largest animal phylum on earth with 30,000 species and are a major producer of CaCO₃. Molluscs also provide essential ecosystem services including habitat structure and food for benthic organisms (i.e., mussel and oyster beds), purification of water through filtration and are economically valuable. Even sub lethal impacts on molluscs due to climate changed oceans will have serious consequences for global protein sources and marine ecosystems.

Threats to ultraoligotrophic marine ecosystems

Ocean acidification is discussed in Section 3 of this book chapter.

Temperate reefs in a changing ocean: skeletal carbonate mineralogy of serpulids

We present a review of the published data about serpulid skeletal carbonate geochemistry, augmented with new data from the Southern Hemisphere. We know something about skeletal carbonate mineralogy of 15 % of extant species (n = 52); and about half of extant genera (n = 25). Serpulid worm tubes vary in their skeletal mineralogy from entirely aragonitic (about 24 % of species) to entirely high-Mg calcite (40 %) to mixtures of the two. Mg in calcite ranges from 7 to 15 wt% MgCO₃, with a mean of 11 wt% MgCO₃. Little mineralogical variation within individuals or species can be found in aragonitic specimens, whereas high-Mg calcitic species show somewhat more variability in both calcite and Mg content, and those with mixed mineralogies are highly variable. These three groups correspond broadly with currently accepted clades. Given this strong phylogenetic signal, we analysed the data using phylogenetically independent contrasts, a statistical approach that separates genotypic from phenotypic variability; we found that variations which might be ascribed to environment were generally weak. The mineralogy of serpulid tubes makes them particularly vulnerable to ocean chemistry changes. While some serpulids appear to be able to adjust their tube mineralogy in order to adapt to sea-water chemistry, overall strength and elasticity may be sacrificed when they do. The biodiverse reef habitat provided by serpulids in some temperate regions may be the only complex solid habitat available, and loss or compromise of these temperate reefs will most likely have deleterious flow-on effects on temperate benthic communities.

Addressing ocean acidification as part of sustainable ocean development

Many of the declarations and outcome documents from prior United Nations international meetings address ocean issues such as fishing, pollution, and climate change, but they do not address ocean acidification. This progressive alteration of seawater chemistry caused by uptake of atmospheric carbon dioxide (CO2) is an emerging issue of concern that has potential consequences for marine ecosystems and the humans that depend on them. Addressing ocean acidification will require mitigation of global CO2 emissions at the international level accompanied by regional marine resource use adaptations that reduce the integrated pressure on marine ecosystems while the global community works towards implementing permanent CO2 emissions reductions. Addressing ocean acidification head-on is necessary because it poses a direct challenge to sustainable development targets such as the Millennium Development Goals, and it cannot be addressed adequately with accords or geoengineering plans that do not specifically decrease atmospheric carbon dioxide levels. Here, we will briefly review the current state of ocean acidification knowledge and identify several mitigation and adaptation strategies that should be considered along with reductions in CO2 emissions to reduce the near-term impacts of ocean acidification. Our goal is to present potential options while identifying some of their inherent weaknesses to inform decisionmaking discussions, rather than to recommend adoption of specific policies. While the reduction of CO2 emissions should be the number one goal of the international community, it is unlikely that the widespread changes and infrastructure redevelopment necessary to accomplish this will be achieved soon, before ocean acidification’s short-term impacts become significant. Therefore, a multi-faceted approach must be employed to address this growing problem.

Climate change and intertidal wetlands

Intertidal wetlands are recognised for the provision of a range of valued ecosystem services. The two major categories of intertidal wetlands discussed in this contribution are saltmarshes and mangrove forests. Intertidal wetlands are under threat from a range of anthropogenic causes, some site-specific, others acting globally. Globally acting factors include climate change and its driving cause—the increasing atmospheric concentrations of greenhouse gases. One direct consequence of climate change will be global sea level rise due to thermal expansion of the oceans, and, in the longer term, the melting of ice caps and glaciers. The relative sea level rise experienced at any one locality will be affected by a range of factors, as will the response of intertidal wetlands to the change in sea level. If relative sea level is rising and sedimentation within intertidal wetlands does not keep pace, then there will be loss of intertidal wetlands from the seaward edge, with survival of the ecosystems only possible if they can retreat inland. When retreat is not possible, the wetland area will decline in response to the “squeeze” experienced. Any changes to intertidal wetland vegetation, as a consequence of climate change, will have flow on effects to biota, while changes to biota will affect intertidal vegetation. Wetland biota may respond to climate change by shifting in distribution and abundance landward, evolving or becoming extinct. In addition, impacts from ocean acidification and warming are predicted to affect the fertilisation, larval development, growth and survival of intertidal wetland biota including macroinvertebrates, such as molluscs and crabs, and vertebrates such as fish and potentially birds. The capacity of organisms to move and adapt will depend on their life history characteristics, phenotypic plasticity, genetic variability, inheritability of adaptive characteristics, and the predicted rates of environmental change.