Annual Review of Marine Science

Time-series observations form a critical element of oceanography. New interdisciplinary efforts launched in the past two decades complement the few earlier, longer-running time series to build a better, though still poorly resolved, picture of lower-frequency ocean variability, the climate processes that drive variability, and the implications for food web dynamics, carbon storage, and climate feedbacks. Time series also enlarge our understanding of ecological processes and are integral for improving models of physical-biogeochemical-ecological ocean dynamics. The major time-series observatories go well beyond simple monitoring of core ocean properties, although that important activity forms the critical center of all time-series efforts. Modern ocean time series have major process and experimental components, entrain ancillary programs, and have integrated modeling programs for deriving a better understanding of the observations and the changing, three-dimensional ocean in which the observatories are embedded.

Oxygen minimum zones (OMZs) harbor unique microbial communities that rely on alternative electron acceptors for respiration. Conditions therein enable an almost complete nitrogen (N) cycle and substantial N-loss. N-loss in OMZs is attributable to anammox and heterotrophic denitrification, whereas nitrate reduction to nitrite along with dissimilatory nitrate reduction to ammonium are major remineralization pathways. Despite virtually anoxic conditions, nitrification also occurs in OMZs, converting remineralized ammonium to N-oxides. The concurrence of all these processes provides a direct channel from organic N to the ultimate N-loss, whereas most individual processes are likely controlled by organic matter. Many microorganisms inhabiting the OMZs are capable of multiple functions in the N- and other elemental cycles. Their versatile metabolic potentials versus actual activities present a challenge to ecophysiological and biogeochemical measurements. These challenges need to be tackled before we can realistically predict how N-cycling in OMZs, and thus oceanic N-balance, will respond to future global perturbations.

Extracellular enzymes initiate microbial remineralization of organic matter by hydrolyzing substrates to sizes sufficiently small to be transported across cell membranes. As much of marine primary productivity is processed by heterotrophic microbes, the substrate specificities of extracellular enzymes, the rates at which they function in seawater and sediments, and factors controlling their production, distribution, and active lifetimes, are central to carbon cycling in marine systems. In this review, these topics are considered from biochemical, microbial/molecular biological, and geochemical perspectives. Our understanding of the capabilities and limitations of heterotrophic microbial communities has been greatly advanced in recent years, in part through genetic and genomic approaches. New methods to measure enzyme activities in the field are needed to keep pace with these advances and to pursue intriguing evidence that patterns of enzyme activities in different environments are linked to differences in microbial community composition that may profoundly affect the marine carbon cycle.

Rising atmospheric carbon dioxide (CO2), primarily from human fossil fuel combustion, reduces ocean pH and causes wholesale shifts in seawater carbonate chemistry. The process of ocean acidification is well documented in field data, and the rate will accelerate over this century unless future CO2 emissions are curbed dramatically. Acidification alters seawater chemical speciation and biogeochemical cycles of many elements and compounds. One well-known effect is the lowering of calcium carbonate saturation states, which impacts shell-forming marine organisms from plankton to benthic molluscs, echinoderms, and corals. Many calcifying species exhibit reduced calcification and growth rates in laboratory experiments under high-CO2 conditions. Ocean acidification also causes an increase in carbon fixation rates in some photosynthetic organisms (both calcifying and noncalcifying). The potential for marine organisms to adapt to increasing CO2 and broader implications for ocean ecosystems are not well known; both are high priorities for future research. Although ocean pH has varied in the geological past, paleo-events may be only imperfect analogs to current conditions.

The persistence of carbonate structures on coral reefs is essential in providing habitats for a large number of species and maintaining the extraordinary biodiversity associated with these ecosystems. As a consequence of ocean acidification (OA), the ability of marine calcifiers to produce calcium carbonate (CaCO(3)) and their rate of CaCO(3) production could decrease while rates of bioerosion and CaCO(3) dissolution could increase, resulting in a transition from a condition of net accretion to one of net erosion. This would have negative consequences for the role and function of coral reefs and the eco-services they provide to dependent human communities. In this article, we review estimates of bioerosion, CaCO(3) dissolution, and net ecosystem calcification (NEC) and how these processes will change in response to OA. Furthermore, we critically evaluate the observed relationships between NEC and seawater aragonite saturation state (Ω(a)). Finally, we propose that standardized NEC rates combined with observed changes in the ratios of dissolved inorganic carbon to total alkalinity owing to net reef metabolism may provide a biogeochemical tool to monitor the effects of OA in coral reef environments. Expected final online publication date for the Annual Review of Marine Science Volume 5 is December 05, 2012. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.

Multiple natural and anthropogenic processes alter the carbonate chemistry of the coastal zone in ways that either exacerbate or mitigate ocean acidification effects. Freshwater inputs and multiple acid-base reactions change carbonate chemistry conditions, sometimes synergistically. The shallow nature of these systems results in strong benthic-pelagic coupling, and marine invertebrates at different life history stages rely on both benthic and pelagic habitats. Carbonate chemistry in coastal systems can be highly variable, responding to processes with temporal modes ranging from seconds to centuries. Identifying scales of variability relevant to levels of biological organization requires a fuller characterization of both the frequency and magnitude domains of processes contributing to or reducing acidification in pelagic and benthic habitats. We review the processes that contribute to coastal acidification with attention to timescales of variability and habitats relevant to marine bivalves. Expected final online publication date for the Annual Review of Marine Science Volume 6 is January 03, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.

Anthropogenic nutrient enrichment and physical characteristics result in low dissolved oxygen concentrations (hypoxia) in estuaries and semienclosed seas throughout the world. Published research indicates that within and near oxygen-depleted waters, finfish and mobile macroinvertebrates experience negative effects that range from mortality to altered trophic interactions. Chronic exposure to hypoxia and fluctuating oxygen concentrations impair reproduction, immune responses, and growth. We present an analysis of hypoxia, nitrogen loadings, and fisheries landings in 30 estuaries and semien-closed seas worldwide. Our results suggest that hypoxia does not typically reduce systemwide fisheries landings below what would be predicted from nitrogen loadings, except where raw sewage is released or particularly sensitive species lose critical habitat. A number of compensatory mechanisms limit the translation of local-scale effects of hypoxia to the scale of the whole system. Hypoxia is, however, a serious environmental challenge that should be considered in fisheries management strategies and be a direct target of environmental restoration.

Local adaptation in the sea was regarded historically as a rare phenomenon that was limited to a handful of species with exceptionally low dispersal potential. However, a growing body of experimental studies indicates that adaptive differentiation occurs in numerous marine invertebrates in response to selection imposed by strong gradients (and more complex mosaics) of abiotic and biotic conditions. Moreover, a surprisingly high proportion of the marine invertebrates known or suspected of exhibiting local adaptation are species with planktonic dispersal. Adaptive divergence among populations can occur over a range of spatial scales, including those that are fine-grained (i.e., meters to kilometers), reflecting a balance between scales of gene flow and selection. Addressing the causes and consequences of adaptive genetic differentiation among invertebrate populations promises to advance community ecology, climate change research, and the effective management of marine ecosystems.

Predicting the response of the biota to global change remains a formidable endeavor. Zooplankton face challenges related to global warming, ocean acidification, the proliferation of toxic algal blooms, and increasing pollution, eutrophication, and hypoxia. They can respond to these changes by phenotypic plasticity or genetic adaptation. Using the concept of the evolution of reaction norms, I address how adaptive responses can be unequivocally discerned from phenotypic plasticity. To date, relatively few zooplankton studies have been designed for such a purpose. As case studies, I review the evidence for zooplankton adaptation to toxic algal blooms, hypoxia, and climate change. Predicting the response of zooplankton to global change requires new information to determine (a) the trade-offs and costs of adaptation, (b) the rates of evolution versus environmental change, (c) the consequences of adaptation to stochastic or cyclic (toxic algal blooms, coastal hypoxia) versus directional (temperature, acidification, open ocean hypoxia) environmental change, and (d) the interaction of selective pressures, and evolutionary and ecological processes, in promoting or hindering adaptation.

The past decade has seen a substantial amount of research on air-sea gas exchange and its environmental controls. These studies have significantly advanced the understanding of processes that control gas transfer, led to higher quality field measurements, and improved estimates of the flux of climate-relevant gases between the ocean and atmosphere. This review discusses the fundamental principles of air-sea gas transfer and recent developments in gas transfer theory, parameterizations, and measurement techniques in the context of the exchange of carbon dioxide. However, much of this discussion is applicable to any sparingly soluble, non-reactive gas. We show how the use of global variables of environmental forcing that have recently become available and gas exchange relationships that incorporate the main forcing factors will lead to improved estimates of global and regional air-sea gas fluxes based on better fundamental physical, chemical, and biological foundations.

Recent advances in our understanding of estuarine circulation and salinity structure are reviewed. We focus on well- and partially mixed systems that are long relative to the tidal excursion. Dynamics of the coupled system of width- and tidally averaged momentum and salt equations are now better understood owing to the development of simple numerical solution techniques. These have led to a greater appreciation of the key role played by the time dependency of the length of the salt intrusion. Improved realism in simplified tidally averaged physics has been driven by simultaneous advances in our understanding of the detailed dynamics within the tidal cycle and across irregular channel cross-sections. The complex interactions of turbulence, stratification, and advection are now understood well enough to motivate a new generation of physically plausible mixing parameterizations for the tidally averaged equations.

Prochlorococcus is the key phytoplanktonic organism of tropical gyres, large ocean regions that are depleted of the essential macronutrients needed for photosynthesis and cell growth. This cyanobacterium has adapted itself to oligotrophy by minimizing the resources necessary for life through a drastic reduction of cell and genome sizes. This rarely observed strategy in free-living organisms has conferred on Prochlorococcus a considerable advantage over other phototrophs, including its closest relative Synechococcus, for life in this vast yet little variable ecosystem. However, this strategy seems to reach its limits in the upper layer of the S Pacific gyre, the most oligotrophic region of the world ocean. By losing some important genes and/or functions during evolution, Prochlorococcus has seemingly become dependent on co-occurring microorganisms. In this review, we present some of the recent advances in the ecology, biology, and evolution of Prochlorococcus, which because of its ecological importance and tiny genome is rapidly imposing itself as a model organism in environmental microbiology.

A basic problem in marine biogeochemistry is understanding material and elemental distributions and fluxes in the oceans, and a key part of this problem is understanding the processes that affect particulate material in the ocean. Aggregation of particulate material is a primary process because it alters the transport properties of particulate material and provides a mechanism for transferring material from the dissolved into the particulate pools. Aggregation theory not only provides a framework for understanding these processes, but it also provides a means for making predictions and has been successfully used to predict maximum particle concentrations in the oceans and the fate of diatom blooms (including those from iron fertilization), the size spectra of particles in the oceans, and the size distributions of trace metals. Here we review the basic theory involved, summarize recent developments, and explore unresolved issues.

The public health, tourism, fisheries, and ecosystem impacts from harmful algal blooms (HABs) have all increased over the past few decades. This has led to heightened scientific and regulatory attention, and the development of many new technologies and approaches for research and management. This, in turn, is leading to significant paradigm shifts with regard to, e.g., our interpretation of the phytoplankton species concept (strain variation), the dogma of their apparent cosmopolitanism, the role of bacteria and zooplankton grazing in HABs, and our approaches to investigating the ecological and genetic basis for the production of toxins and allelochemicals. Increasingly, eutrophication and climate change are viewed and managed as multifactorial environmental stressors that will further challenge managers of coastal resources and those responsible for protecting human health. Here we review HAB science with an eye toward new concepts and approaches, emphasizing, where possible, the unexpected yet promising new directions that research has taken in this diverse field.

Fixed nitrogen limits primary productivity in many parts of the global ocean, and it consequently plays a role in controlling the carbon dioxide content of the atmosphere. The concentration of fixed nitrogen is determined by the balance between two processes: the fixation of nitrogen gas into organic forms by diazotrophs, and the reconversion of fixed nitrogen to nitrogen gas by denitrifying organisms. However, current sedimentary denitrification rates are poorly constrained, especially in permeable sediments, which cover the majority of the continental margin. Also, anammox has recently been shown to be an additional pathway for the loss of fixed nitrogen in sediments. This article briefly reviews sedimentary fixed nitrogen loss by sedimentary denitrification and anammox, including in sediments in contact with oxygen-deficient zones. A simple extrapolation of existing rate measurements to the global sedimentary denitrification rate yields a value smaller than many existing measurement-based estimates but still larger than the rate of water column denitrification.

André Morel (1933-2012) was a prominent pioneer of modern optical oceanography, enabling significant advances in this field. Through his forward thinking and research over more than 40 years, he made key contributions that this field needed to grow and to reach its current status. This article first summarizes his career and then successively covers different aspects of optical oceanography where he made significant contributions, from fundamental work on optical properties of water and particles to global oceanographic applications using satellite ocean color observations. At the end, we share our views on André's legacy to our research field and scientific community. Expected final online publication date for the Annual Review of Marine Science Volume 6 is January 03, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.

The potential for antagonistic coevolution between marine viruses and their (primarily bacterial) hosts is well documented, but our understanding of the consequences of this rapid evolution is in its infancy. Acquisition of resistance against co-occurring viruses and the subsequent evolution of virus host range in response have implications for bacterial mortality rates as well as for community composition and diversity. Drawing on examples from a range of environments, we consider the potential dynamics, underlying genetic mechanisms and fitness costs, and ecological impacts of virus-host coevolution in marine waters. Given that much of our knowledge is derived from laboratory experiments, we also discuss potential challenges and approaches in scaling up to diverse, complex networks of virus-host interactions. Finally, we note that a variety of novel approaches for characterizing virus-host interactions offer new hope for a mechanistic understanding of antagonistic coevolution in marine plankton. Expected final online publication date for the Annual Review of Marine Science Volume 6 is January 03, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.

A significant impetus for recent ocean biogeochemical research has been to better understand the ocean's role as a sink for anthropogenic CO2. In the 1990s the global carbon survey of the World Ocean Circulation Experiment (WOCE) and the Joint Global Ocean Flux Study (JGOFS) inspired the development of several approaches for estimating anthropogenic carbon inventories in the ocean interior. Most approaches agree that the total global ocean inventory of Cant was around 120 Pg C in the mid-1990s. Today, the ocean carbon uptake rate estimates suggest that the ocean is not keeping pace with the CO2 emissions growth rate. Repeat occupations of the WOCE/JGOFS survey lines consistently show increases in carbon inventories over the last decade, but have not yet been synthesized enough to verify a slowdown in the carbon storage rate. There are many uncertainties in the future ocean carbon storage. Continued observations are necessary to monitor changes and understand mechanisms controlling ocean carbon uptake and storage in the future.

Interdisciplinary study of coastal archaeological sites provides a wealth of information on the ecology and evolution of ancient marine animal populations, the structure of past marine ecosystems, and the history of human impacts on coastal fisheries. In this paper, we review recent methodological developments in the archaeology and historical ecology of coastal regions around the world. Using two case studies, we examine (a) a deep history of anthropogenic effects on the marine ecosystems of California's Channel Islands through the past 12,000 years and (b) geographic variation in the effects of human fishing on Pacific Island peoples who spread through Oceania during the late Holocene. These case studies--the first focused on hunter-gatherers, the second on maritime horticulturalists-provide evidence for shifting baselines and timelines, documenting a much deeper anthropogenic influence on many coastal ecosystems and fisheries than considered by most ecologists, conservation biologists, and fisheries managers.

The use of clean sampling and incubation methods and the development of biomass-independent techniques for estimating the rates of growth and grazing mortality of phytoplankton in the ocean have resulted in estimates of phytoplankton growth rates that are approximately twice those reported prior to roughly 1980. Light-saturated growth rates in tropical and subtropical latitudes correspond to a doubling time of roughly 1 day. The results of mesoscale nutrient-enrichment experiments and comparison of growth rates with estimates of strictly temperature-limited rates indicate that light-saturated growth rates are no more than 50% of nutrient-saturated values, a conclusion consistent with the resiliency of food webs to perturbations. Phytoplankton growth rates in the euphotic zone of the ocean appear to be controlled largely by the grazing activities of micro- and mesozooplankton and the recycling of nutrients associated with the catabolism of consumed prey. Expected final online publication date for the Annual Review of Marine Science Volume 5 isDecember 5, 2012. Please see http://www.annualreviews .org/catalog/pubdates.aspx for revised estimates.

Recent changes in the timing of sea ice formation and retreat, along with increasing seawater temperatures, are driving shifts in marine species composition that may signal marine ecosystem reorganization in the Pacific Arctic sector. Interannual variability in seasonal sea ice retreat in the northern Bering Sea has been observed over the past decade; north of the Bering Strait, the Chukchi Sea ecosystem has had consistent earlier spring sea ice retreat and later fall sea ice formation. The latitudinal gradient in sea ice persistence, water column chlorophyll, and carbon export to the sediments has a direct impact on ecosystem structure in this Arctic/sub-Arctic complex. Large-scale decadal patterns in the benthic biological system are driven by sea ice extent, hydrographic forcing, and export production that influences benthic processes. Shifts in species composition and northward faunal range expansions indicate a changing system. The shifting patterns of life and change in key biological processes have the potential for a system-wide reorganization of the marine ecosystem.

The Arctic sea ice cover is in decline. The areal extent of the ice cover has been decreasing for the past few decades at an accelerating rate. Evidence also points to a decrease in sea ice thickness and a reduction in the amount of thicker perennial sea ice. A general global warming trend has made the ice cover more vulnerable to natural fluctuations in atmospheric and oceanic forcing. The observed reduction in Arctic sea ice is a consequence of both thermodynamic and dynamic processes, including such factors as preconditioning of the ice cover, overall warming trends, changes in cloud coverage, shifts in atmospheric circulation patterns, increased export of older ice out of the Arctic, advection of ocean heat from the Pacific and North Atlantic, enhanced solar heating of the ocean, and the ice-albedo feedback. The diminishing Arctic sea ice is creating social, political, economic, and ecological challenges.

Ocean history is largely read from deep-sea sediments, using microscopic fossils, notably foraminifers. Ice age fluctuations in the ocean's sediments provided for a new geologic understanding of climate change. The discovery of rapid decay of ice masses at the end of glacial periods was especially important, yielding rates of sea level rise reaching values of 1 to 2 m per century for millennia. Thanks to deep-ocean drilling, the overall planetary cooling trend in the Cenozoic was recognized as occurring in three large steps. The first step is at the Eocene-Oligocene boundary and is marked by a great change in sedimentation patterns; the second is in the middle Miocene, associated with a major pulse in the buildup of Antarctic ice masses and the intensification of upwelling regimes; and the third is within the late Pliocene and led into the northern ice ages. Evolution in the sea is linked to these various steps.

The global overturning of ocean waters involves the equatorward transport of cold, deep waters and the poleward transport of warm, near-surface waters. Such movement creates a net poleward transport of heat that, in partnership with the atmosphere, establishes the global and regional climates. Although oceanographers have long assumed that a reduction in deep water formation at high latitudes in the North Atlantic translates into a slowing of the ocean's overturning and hence in Earth's climate, observational and modeling studies over the past decade have called this assumed linkage into question. The observational basis for linking water mass formation with the ocean's meridional overturning is reviewed herein. Understanding this linkage is crucial to efforts aimed at predicting the consequences of the warming and freshening of high-latitude surface waters to the climate system.

Atmospheric inputs of iron to the open ocean are hypothesized to modulate ocean biogeochemistry. This review presents an integration of available observations of atmospheric iron and iron deposition, and also covers bioavailable iron distributions. Methods for estimating temporal variability in ocean deposition over the recent past are reviewed. Desert dust iron is estimated to represent 95% of the global atmospheric iron cycle, and combustion sources of iron are responsible for the remaining 5%. Humans may be significantly perturbing desert dust (up to 50%). The sources of bioavailable iron are less well understood than those of iron, partly because we do not know what speciation of the iron is bioavailable. Bioavailable iron can derive from atmospheric processing of relatively insoluble desert dust iron or from direct emissions of soluble iron from combustion sources. These results imply that humans could be substantially impacting iron and bioavailable iron deposition to ocean regions, but there are large uncertainties in our understanding.