Annual Review of Marine Science - Volume 12, 2020

This narrative is a personal account of my evolution as a student of phytoplankton and the ocean. Initially I focused on phytoplankton nutrient physiology and uptake, later switching to photosynthetic physiology. Better models of photosynthesis naturally require a better understanding of spectral underwater light fields and absorption coefficients, which precipitated my involvement in the nascent field of bio-optical oceanography. Establishment of the now 34-year-old summer graduate course in ocean optics, which continues to attract students from around the globe, is a legacy of my jumping into optics. The importance of social interactions in advancing science cannot be underestimated; a prime example is how a TGIF gathering led to my immersion in the world of autonomous underwater vehicles for the past two decades of my career. Working with people who you like and respect is also critical; I believe collegial friendship played a major role in the great success of the 2008 North Atlantic Bloom Experiment.

Biogeochemical-Argo (BGC-Argo) is a network of profiling floats carrying sensors that enable observation of as many as six essential biogeochemical and bio-optical variables: oxygen, nitrate, pH, chlorophyll a, suspended particles, and downwelling irradiance. This sensor network represents today's most promising strategy for collecting temporally and vertically resolved observations of biogeochemical properties throughout the ocean. All data are freely available within 24 hours of transmission. These data fill large gaps in ocean-observing systems and support three ambitions: gaining a better understanding of biogeochemical processes (e.g., the biological carbon pump and air–sea CO2 exchanges) and evaluating ongoing changes resulting from increasing anthropogenic pressure (e.g., acidification and deoxygenation); managing the ocean (e.g., improving the global carbon budget and developing sustainable fisheries); and carrying out exploration for potential discoveries. The BGC-Argo network has already delivered extensive high-quality global data sets that have resulted in unique scientific outcomes from regional to global scales. With the proposed expansion of BGC-Argo in the near future, this network has the potential to become a pivotal observation system that links satellite and ship-based observations in a transformative manner.

The biogeochemical cycles of trace elements and their isotopes (TEIs) constitute an active area of oceanographic research due to their role as essential nutrients for marine organisms and their use as tracers of oceanographic processes. Selected TEIs also provide diagnostic information about the physical, geological, and chemical processes that supply or remove solutes in the ocean. Many of these same TEIs provide information about ocean conditions in the past, as their imprint on marine sediments can be interpreted to reflect changes in ocean circulation, biological productivity, the ocean carbon cycle, and more. Other TEIs have been introduced as the result of human activities and are considered contaminants. The development and implementation of contamination-free methods for collecting and analyzing samples for TEIs revolutionized marine chemistry, revealing trace element distributions with oceanographically consistent features and new insights about the processes regulating them. Despite these advances, the volume and geographic coverage of high-quality TEI data by the end of the twentieth century were insufficient to constrain their global biogeochemical cycles. To accelerate progress in this field of research, marine geochemists developed a coordinated international effort to systematically study the marine biogeochemical cycles of TEIs—the GEOTRACES program. Following a decade of planning and implementation, GEOTRACES launched its main field effort in 2010. This review, roughly midway through the field program, summarizes the steps involved in designing the program, its management structure, and selected findings.

In this article, we analyze the impacts of climate change on Antarctic marine ecosystems. Observations demonstrate large-scale changes in the physical variables and circulation of the Southern Ocean driven by warming, stratospheric ozone depletion, and a positive Southern Annular Mode. Alterations in the physical environment are driving change through all levels of Antarctic marine food webs, which differ regionally. The distributions of key species, such as Antarctic krill, are also changing. Differential responses among predators reflect differences in species ecology. The impacts of climate change on Antarctic biodiversity will likely vary for different communities and depend on species range. Coastal communities and those of sub-Antarctic islands, especially range-restricted endemic communities, will likely suffer the greatest negative consequences of climate change. Simultaneously, ecosystem services in the Southern Ocean will likely increase. Such decoupling of ecosystem services and endemic species will require consideration in the management of human activities such as fishing in Antarctic marine ecosystems.

Tides are changing worldwide at rates not explained by astronomical forcing. Rather, the observed evolution of tides and other long waves, such as storm surges, is influenced by shelf processes and changes to the roughness, depth, width, and length of embayments, estuaries, and tidal rivers. In this review, we focus on processes in estuaries and tidal rivers, because that is where the largest changes to tidal properties are occurring. Recent literature shows that changes in tidal amplitude have been ubiquitous worldwide over the past century, often in response to wetland reclamation, channel dredging, and other environmental changes. While tidal amplitude changes are sometimes slight (<1%) or even negative, we identify two types of systems that are particularly prone to tidal amplification: (a) shallow, strongly damped systems, in which a small increase in depth produces a large decrease in effective friction, and (b) systems in which wave reflection and resonance are strongly influenced by changes to depth, friction, and convergence. The largest changes in amplitude occur inland, some distance from the coast, and can sometimes be measured in meters. Tide changes are a leading indicator that the dynamics of storm surges and river flood waves have also changed and are often associated with shifts in sediment transport, salinity intrusion, and ecosystem properties. Therefore, the dynamics of tidal evolution have major implications for coastal management, particularly for systems that are sensitive to changes in geometry induced by sea-level rise and anthropogenic development.

The geographic distributions of marine species are changing rapidly, with leading range edges following climate poleward, deeper, and in other directions and trailing range edges often contracting in similar directions. These shifts have their roots in fine-scale interactions between organisms and their environment—including mosaics and gradients of temperature and oxygen—mediated by physiology, behavior, evolution, dispersal, and species interactions. These shifts reassemble food webs and can have dramatic consequences. Compared with species on land, marine species are more sensitive to changing climate but have a greater capacity for colonization. These differences suggest that species cope with climate change at different spatial scales in the two realms and that range shifts across wide spatial scales are a key mechanism at sea. Additional research is needed to understand how processes interact to promote or constrain range shifts, how the dominant responses vary among species, and how the emergent communities of the future ocean will function.

Experimental evolution and the associated theory are underutilized in marine microbial studies; the two fields have developed largely in isolation. Here, we review evolutionary tools for addressing four key areas of ocean global change biology: linking plastic and evolutionary trait changes, the contribution of environmental variability to determining trait values, the role of multiple environmental drivers in trait change, and the fate of populations near their tolerance limits. Wherever possible, we highlight which data from marine studies could use evolutionary approaches and where marine model systems can advance our understanding of evolution. Finally, we discuss the emerging field of marine microbial experimental evolution. We propose a framework linking changes in environmental quality (defined as the cumulative effect on population growth rate) with population traits affecting evolutionary potential, in order to understand which evolutionary processes are likely to be most important across a range of locations for different types of marine microbes.

We have known for more than 45 years that microplastics in the ocean are carriers of microbially dominated assemblages. However, only recently has the role of microbial interactions with microplastics in marine ecosystems been investigated in detail. Research in this field has focused on three main areas: (a) the establishment of plastic-specific biofilms (the so-called plastisphere); (b) enrichment of pathogenic bacteria, particularly members of the genus Vibrio, coupled to a vector function of microplastics; and (c) the microbial degradation of microplastics in the marine environment. Nevertheless, the relationships between marine microorganisms and microplastics remain unclear. In this review, we deduce from the current literature, new comparative analyses, and considerations of microbial adaptation concerning plastic degradation that interactions between microorganisms and microplastic particles should have rather limited effects on the ocean ecosystems. The majority of microorganisms growing on microplastics seem to belong to opportunistic colonists that do not distinguish between natural and artificial surfaces. Thus, microplastics do not pose a higher risk than natural particles to higher life forms by potentially harboring pathogenic bacteria. On the other hand, microplastics in the ocean represent recalcitrant substances for microorganisms that are insufficient to support prokaryotic metabolism and will probably not be microbially degraded in any period of time relevant to human society. Because we cannot remove microplastics from the ocean, proactive action regarding research on plastic alternatives and strategies to prevent plastic entering the environment should be taken promptly.

Photosynthesis evolved in the ocean more than 2 billion years ago and is now performed by a wide range of evolutionarily distinct organisms, including both prokaryotes and eukaryotes. Our appreciation of their abundance, distributions, and contributions to primary production in the ocean has been increasing since they were first discovered in the seventeenth century and has now been enhanced by data emerging from the Tara Oceans project, which performed a comprehensive worldwide sampling of plankton in the upper layers of the ocean between 2009 and 2013. Largely using recent data from Tara Oceans, here we review the geographic distributions of phytoplankton in the global ocean and their diversity, abundance, and standing stock biomass. We also discuss how omics-based information can be incorporated into studies of photosynthesis in the ocean and show the likely importance of mixotrophs and photosymbionts.

Advances in technologies for molecular observation are leading to novel types of data, including gene, transcript, protein, and metabolite levels, which are fundamentally different from the types traditionally compared with microbial ecosystem models, such as biomass (e.g., chlorophyll a) and nutrient concentrations. A grand challenge is to use these data to improve predictive models and use models to explain observed patterns. This article presents a framework that aligns observations and models along the dimension of abstraction or biological organization—from raw sequences to ecosystem patterns for observations, and from sequence simulators to ecological theory for models. It then reviews 16 studies that compared model results with molecular observations. Molecular data can and are being combined with microbial ecosystem models, but to keep up with and take advantage of the full scope of observations, models need to become more mechanistically detailed and complex, which is a technical and cultural challenge for the ecological modeling community.

Ocean ecosystems are experiencing unprecedented rates of climate and anthropogenic change, which can often initiate stress in marine organisms. Symbioses, or associations between different organisms, are plentiful in the ocean and could play a significant role in facilitating organismal adaptations to stressful ocean conditions. This article reviews current knowledge about the role of symbiosis in marine organismal acclimation and adaptation. It discusses stress and adaptations in symbioses from coral reef ecosystems, which are among the most affected environments in the ocean, including the relationships between corals and microalgae, corals and bacteria, anemones and clownfish, and cleaner fish and client fish. Despite the importance of this subject, knowledge of how marine organisms adapt to stress is still limited, and there are vast opportunities for research and technological development in this area. Attention to this subject will enhance our understanding of the capacity of symbioses to alleviate organismal stress in the oceans.

With the decline of reef-building corals on tropical reefs, sponges have emerged as an important component of changing coral reef ecosystems. Seemingly simple, sponges are highly diverse taxonomically, morphologically, and in terms of their relationships with symbiotic microbes, and they are one of nature's richest sources of novel secondary metabolites. Unlike most other benthic organisms, sponges have the capacity to disrupt boundary flow as they pump large volumes of seawater into the water column. This seawater is chemically transformed as it passes through the sponge body as a consequence of sponge feeding, excretion, and the activities of microbial symbionts, with important effects on carbon and nutrient cycling and on the organisms in the water column and on the adjacent reef. In this review, we critically evaluate developments in the recently dynamic research area of sponge ecology on tropical reefs and provide a perspective for future studies.

Compared with terrestrial ecosystems, marine ecosystems have a higher proportion of heterotrophic biomass. Building from this observation, we define the North Atlantic biome as the region where the large, lipid-rich copepod Calanus finmarchicus is the dominant mesozooplankton species. This species is superbly adapted to take advantage of the intense pulse of productivity associated with the North Atlantic spring bloom. Most of the characteristic North Atlantic species, including cod, herring, and right whales, rely on C. finmarchicus either directly or indirectly. The notion of a biome rests inherently on an assumption of stability, yet conditions in the North Atlantic are anything but stable. Humans have reduced the abundance of many fish and whales (though some recovery is underway). Humans are also introducing physical and chemical trends associated with global climate change. Thus, the future of the North Atlantic depends on the biome's newest species, Homo sapiens.

Apex predators play pivotal roles in marine ecosystems, mediated principally through diet and nutrition. Yet, compared with terrestrial animals, the nutritional ecology of marine predators is poorly understood. One reason is that the field has adhered to an approach that evaluates diet principally in terms of energy gain. Studies in terrestrial systems, by contrast, increasingly adopt a multidimensional approach, the nutritional geometry framework, that distinguishes specific nutrients and calories. We provide evidence that a nutritional approach is likewise relevant to marine apex predators, then demonstrate how nutritional geometry can characterize the nutrient and energy content of marine prey. Next, we show how this framework can be used to reconceptualize ecological interactions via the ecological niche concept, and close with a consideration of its application to problems in marine predator research.

Salt marshes are recognized as valuable resources that are threatened by climate change and human activities. Better management and planning for these ecosystems will depend on understanding which marshes are most vulnerable, what is driving their change, and what their future trajectory is likely to be. Both observations and models have provided inconsistent answers to these questions, likely in part because of comparisons among sites and/or models that differ significantly in their characteristics and processes. Some of these differences almost certainly arise from processes that are not fully accounted for in marsh morphodynamic models. Here, we review distinguishing properties of marshes, important processes missing from many morphodynamic models, and key measurements missing from many observational studies. We then suggest some comparisons between models and observations that will provide critical tests and insights to improve our ability to forecast future change in these coastal landscapes.

Bays in coastal upwelling regions are physically driven and biochemically fueled by their interaction with open coastal waters. Wind-driven flow over the shelf imposes a circulation in the bay, which is also influenced by local wind stress and thermal bay–ocean density differences. Three types of bays are recognized based on the degree of exposure to coastal currents and winds (wide-open bays, square bays, and elongated bays), and the characteristic circulation and stratification patterns of each type are described. Retention of upwelled waters in bays allows for dense phytoplankton blooms that support productive bay ecosystems. Retention is also important for the accumulation of larvae, which accounts for high recruitment in bays. In addition, bays are coupled to the shelf ecosystem through export of plankton-rich waters during relaxation events. Ocean acidification and deoxygenation are a concern in bays because local extrema can develop beneath strong stratification.

One major objective of aquatic microbial ecology is to understand the distribution of microbial populations over space and time and in response to environmental factors. Perhaps more importantly, it is crucial to quantify how those microbial cells affect biogeochemical processes of interest, such as primary production, nitrogen cycling, or the breakdown of pollutants. One valuable approach to link microbial identity to activity is to carry out incubations with stable-isotope-labeled substrates and then quantify the isotope incorporation by individual microbial cells using nanoscale secondary ion mass spectrometry (NanoSIMS). This review summarizes recent efforts in this field, highlights novel methods, describes studies investigating rare metabolisms as well as widespread microbial activity, and hopes to provide a framework to increase the use and capabilities of NanoSIMS for microbial biogeochemical studies in the future.

More than two-thirds of global biomass consists of vascular plants. A portion of the detritus they generate is carried into the oceans from land and highly productive blue carbon ecosystems—salt marshes, mangrove forests, and seagrass meadows. This large detrital input receives scant attention in current models of the global carbon cycle, though for blue carbon ecosystems, increasingly well-constrained estimates of biomass, productivity, and carbon fluxes, reviewed in this article, are now available. We show that the fate of this detritus differs markedly from that of strictly marine origin, because the former contains lignocellulose—an energy-rich polymer complex of cellulose, hemicelluloses, and lignin that is resistant to enzymatic breakdown. This complex can be depolymerized for nutritional purposes by specialized marine prokaryotes, fungi, protists, and invertebrates using enzymes such as glycoside hydrolases and lytic polysaccharide monooxygenases to release sugar monomers. The lignin component, however, is less readily depolymerized, and detritus therefore becomes lignin enriched, particularly in anoxic sediments, and forms a major carbon sink in blue carbon ecosystems. Eventual lignin breakdown releases a wide variety of small molecules that may contribute significantly to the oceanic pool of recalcitrant dissolved organic carbon. Marine carbon fluxes and sinks dependent on lignocellulosic detritus are important ecosystem services that are vulnerable to human interventions. These services must be considered when protecting blue carbon ecosystems and planning initiatives aimed at mitigating anthropogenic carbon emissions.

In the last few decades, numerous studies have investigated the impacts of simulated ocean acidification on marine species and communities, particularly those inhabiting dynamic coastal systems. Despite these research efforts, there are many gaps in our understanding, particularly with respect to physiological mechanisms that lead to pathologies. In this review, we trace how carbonate system disturbances propagate from the coastal environment into marine invertebrates and highlight mechanistic links between these disturbances and organism function. We also point toward several processes related to basic invertebrate biology that are severely understudied and prevent an accurate understanding of how carbonate system dynamics influence organismic homeostasis and fitness-related traits. We recommend that significant research effort be directed to studying cellular phenotypes of invertebrates acclimated or adapted to elevated seawater pCO2 using biochemical and physiological methods.