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Annual Review of Marine Science - Volume 16, 2024
Volume 16, 2024
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A Life Outside
Vol. 16 (2024), pp. 1–23More LessHow do the morphologies of organisms affect their physical interactions with the environment and other organisms? My research in marine systems couples field studies of the physical habitats, life history strategies, and ecological interactions of organisms with laboratory analyses of their biomechanics. Here, I review how we pursued answers to three questions about marine organisms: (a) how benthic organisms withstand and utilize the water moving around them, (b) how the interaction between swimming and turbulent ambient water flow affects where small organisms go, and (c) how hairy appendages catch food and odors. I also discuss the importance of different types of mentors, the roadblocks for women in science when I started my career, the challenges and delights of interdisciplinary research, and my quest to understand how I see the world as a dyslexic.
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The Physical Oceanography of Ice-Covered Moons
Vol. 16 (2024), pp. 25–53More LessIn the outer solar system, a growing number of giant planet satellites are now known to be abodes for global oceans hidden below an outer layer of ice. These planetary oceans are a natural laboratory for studying physical oceanographic processes in settings that challenge traditional assumptions made for Earth's oceans. While some driving mechanisms are common to both systems, such as buoyancy-driven flows and tides, others, such as libration, precession, and electromagnetic pumping, are likely more significant for moons in orbit around a host planet. Here, we review these mechanisms and how they may operate across the solar system, including their implications for ice–ocean interactions. Future studies should continue to advance our understanding of each of these processes as well as how they may act together in concert. This interplay also has strong implications for habitability as well as testing oceanic hypotheses with future missions.
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Marine Transgression in Modern Times
Vol. 16 (2024), pp. 55–79More LessMarine transgression associated with rising sea levels causes coastal erosion, landscape transitions, and displacement of human populations globally. This process takes two general forms. Along open-ocean coasts, active transgression occurs when sediment-delivery rates are unable to keep pace with accommodation creation, leading to wave-driven erosion and/or landward translation of coastal landforms. It is highly visible, rapid, and limited to narrow portions of the coast. In contrast, passive transgression is subtler and slower, and impacts broader areas. It occurs along low-energy, inland marine margins; follows existing upland contours; and is characterized predominantly by the landward translation of coastal ecosystems. The nature and relative rates of transgression along these competing margins lead to expansion and/or contraction of the coastal zone and—particularly under the influence of anthropogenic interventions—will dictate future coastal-ecosystem response to sea-level rise, as well as attendant, often inequitable, impacts on human populations.
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Hidden Threat: The Influence of Sea-Level Rise on Coastal Groundwater and the Convergence of Impacts on Municipal Infrastructure
Vol. 16 (2024), pp. 81–103More LessSea-level rise (SLR) is influencing coastal groundwater by both elevating the water table and shifting salinity profiles landward, making the subsurface increasingly corrosive. Low-lying coastal municipalities worldwide (potentially 1,546, according to preliminary analysis) are vulnerable to an array of impacts spurred by these phenomena, which can occur decades before SLR-induced surface inundation. Damage is accumulating across a variety of infrastructure networks that extend partially and fully beneath the ground surface. Because the resulting damage is largely concealed and imperceptible, it is largely overlooked as part of infrastructure management and planning. Here, we provide an overview of SLR-influenced coastal groundwater and related processes that have the potential to damage societally critical infrastructure and mobilize urban contamination. In an effort to promote research efforts that can inform effective adaptation and management, we discuss various impacts to critical infrastructure and propose actions based on literature focused specifically on SLR-influenced coastal groundwater.
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The Global Turbidity Current Pump and Its Implications for Organic Carbon Cycling
Vol. 16 (2024), pp. 105–133More LessSubmarine turbidity currents form the largest sediment accumulations on Earth, raising the question of their role in global carbon cycles. It was previously inferred that terrestrial organic carbon was primarily incinerated on shelves and that most turbidity current systems are presently inactive. Turbidity currents were thus not considered in global carbon cycles, and the burial efficiency of global terrestrial organic carbon was considered low to moderate (∼10–44%). However, recent work has shown that burial of terrestrial organic carbon by turbidity currents is highly efficient (>60–100%) in a range of settings and that flows occur more frequently than once thought, although they were far more active at sea-level lowstands. This leads to revised global estimates for mass flux (∼62–90 Mt C/year) and burial efficiency (∼31–45%) of terrestrial organic carbon in marine sediments. Greatly increased burial fluxes during sea-level lowstands are also likely underestimated; thus, organic carbon cycling by turbidity currents could play a role in long-term changes in atmospheric CO2 and climate.
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Modeling the Vertical Flux of Organic Carbon in the Global Ocean
Vol. 16 (2024), pp. 135–161More LessThe oceans play a fundamental role in the global carbon cycle, providing a sink for atmospheric carbon. Key to this role is the vertical transport of organic carbon from the surface to the deep ocean. This transport is a product of a diverse range of physical and biogeochemical processes that determine the formation and fate of this material, and in particular how much carbon is sequestered in the deep ocean. Models can be used to both diagnose biogeochemical processes and predict how the various processes will change in the future. Global biogeochemical models use simplified representations of food webs and processes but are converging on values for the export of organic carbon from the surface ocean. Other models concentrate on understanding specific processes and can be used to develop parameterizations for global models. Model development is continuing by adding representations and parameterizations of higher trophic levels and mesopelagic processes, and these are expected to improve model performance.
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The Four-Dimensional Carbon Cycle of the Southern Ocean
Vol. 16 (2024), pp. 163–190More LessThe Southern Ocean plays a fundamental role in the global carbon cycle, dominating the oceanic uptake of heat and carbon added by anthropogenic activities and modulating atmospheric carbon concentrations in past, present, and future climates. However, the remote and extreme conditions found there make the Southern Ocean perpetually one of the most difficult places on the planet to observe and to model, resulting in significant and persistent uncertainties in our knowledge of the oceanic carbon cycle there. The flow of carbon in the Southern Ocean is traditionally understood using a zonal mean framework, in which the meridional overturning circulation drives the latitudinal variability observed in both air–sea flux and interior ocean carbon concentration. However, recent advances, based largely on expanded observation and modeling capabilities in the region, reveal the importance of processes acting at smaller scales, including basin-scale zonal asymmetries in mixed-layer depth, mesoscale eddies, and high-frequency atmospheric variability. Assessing the current state of knowledge and remaining gaps emphasizes the need to move beyond the zonal mean picture and embrace a four-dimensional understanding of the carbon cycle in the Southern Ocean.
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The Impact of Fine-Scale Currents on Biogeochemical Cycles in a Changing Ocean
Vol. 16 (2024), pp. 191–215More LessFine-scale currents, O(1–100 km, days–months), are actively involved in the transport and transformation of biogeochemical tracers in the ocean. However, their overall impact on large-scale biogeochemical cycling on the timescale of years remains poorly understood due to the multiscale nature of the problem. Here, we summarize these impacts and critically review current estimates. We examine how eddy fluxes and upscale connections enter into the large-scale balance of biogeochemical tracers. We show that the overall contribution of eddy fluxes to primary production and carbon export may not be as large as it is for oxygen ventilation. We highlight the importance of fine scales to low-frequency natural variability through upscale connections and show that they may also buffer the negative effects of climate change on the functioning of biogeochemical cycles. Significant interdisciplinary efforts are needed to properly account for the cross-scale effects of fine scales on biogeochemical cycles in climate projections.
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Climate, Oxygen, and the Future of Marine Biodiversity
Vol. 16 (2024), pp. 217–245More LessThe ocean enabled the diversification of life on Earth by adding O2 to the atmosphere, yet marine species remain most subject to O2 limitation. Human industrialization is intensifying the aerobic challenges to marine ecosystems by depleting the ocean's O2 inventory through the global addition of heat and local addition of nutrients. Historical observations reveal an ∼2% decline in upper-ocean O2 and accelerating reports of coastal mass mortality events. The dynamic balance of O2 supply and demand provides a unifying framework for understanding these phenomena across scales from the global ocean to individual organisms. Using this framework, we synthesize recent advances in forecasting O2 loss and its impacts on marine biogeography, biodiversity, and biogeochemistry. We also highlight three outstanding uncertainties: how long-term global climate change intensifies ocean weather events in which simultaneous heat and hypoxia create metabolic storms, how differential species O2 sensitivities alter the structure of ecological communities, and how global O2 loss intersects with coastal eutrophication. Projecting these interacting impacts on future marine ecosystems requires integration of climate dynamics, biogeochemistry, physiology, and ecology, evaluated with an eye on Earth history. Reducing global and local impacts of warming and O2 loss will be essential if humankind is to preserve the health and biodiversity of the future ocean.
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Impacts of Climate Change on Marine Foundation Species
Vol. 16 (2024), pp. 247–282More LessMarine foundation species are the biotic basis for many of the world's coastal ecosystems, providing structural habitat, food, and protection for myriad plants and animals as well as many ecosystem services. However, climate change poses a significant threat to foundation species and the ecosystems they support. We review the impacts of climate change on common marine foundation species, including corals, kelps, seagrasses, salt marsh plants, mangroves, and bivalves. It is evident that marine foundation species have already been severely impacted by several climate change drivers, often through interactive effects with other human stressors, such as pollution, overfishing, and coastal development. Despite considerable variation in geographical, environmental, and ecological contexts, direct and indirect effects of gradual warming and subsequent heatwaves have emerged as the most pervasive drivers of observed impact and potent threat across all marine foundation species, but effects from sea level rise, ocean acidification, and increased storminess are expected to increase. Documented impacts include changes in the genetic structures, physiology, abundance, and distribution of the foundation species themselves and changes to their interactions with other species, with flow-on effects to associated communities, biodiversity, and ecosystem functioning. We discuss strategies to support marine foundation species into the Anthropocene, in order to increase their resilience and ensure the persistence of the ecosystem services they provide.
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Neutral Theory and Plankton Biodiversity
Vol. 16 (2024), pp. 283–305More LessThe biodiversity of the plankton has been interpreted largely through the monocle of competition. The spatial distancing of phytoplankton in nature is so large that cell boundary layers rarely overlap, undermining opportunities for resource-based competitive exclusion. Neutral theory accounts for biodiversity patterns based purely on random birth, death, immigration, and speciation events and has commonly served as a null hypothesis in terrestrial ecology but has received comparatively little attention in aquatic ecology. This review summarizes basic elements of neutral theory and explores its stand-alone utility for understanding phytoplankton diversity. A theoretical framework is described entailing a very nonneutral trophic exclusion principle melded with the concept of ecologically defined neutral niches. This perspective permits all phytoplankton size classes to coexist at any limiting resource level, predicts greater diversity than anticipated from readily identifiable environmental niches but less diversity than expected from pure neutral theory, and functions effectively in populations of distantly spaced individuals.
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Using the Fossil Record to Understand Extinction Risk and Inform Marine Conservation in a Changing World
Vol. 16 (2024), pp. 307–333More LessUnderstanding the long-term effects of ongoing global environmental change on marine ecosystems requires a cross-disciplinary approach. Deep-time and recent fossil records can contribute by identifying traits and environmental conditions associated with elevated extinction risk during analogous events in the geologic past and by providing baseline data that can be used to assess historical change and set management and restoration targets and benchmarks. Here, we review the ecological and environmental information available in the marine fossil record and discuss how these archives can be used to inform current extinction risk assessments as well as marine conservation strategies and decision-making at global to local scales. As we consider future research directions in deep-time and conservationpaleobiology, we emphasize the need for coproduced research that unites researchers, conservation practitioners, and policymakers with the communities for whom the impacts of climate and global change are most imminent.
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The Microbial Ecology of Estuarine Ecosystems
Vol. 16 (2024), pp. 335–360More LessHuman civilization relies on estuaries, and many estuarine ecosystem services are provided by microbial communities. These services include high rates of primary production that nourish harvests of commercially valuable species through fisheries and aquaculture, the transformation of terrestrial and anthropogenic materials to help ensure the water quality necessary to support recreation and tourism, and mutualisms that maintain blue carbon accumulation and storage. Research on the ecology that underlies microbial ecosystem services in estuaries has expanded greatly across a range of estuarine environments, including water, sediment, biofilms, biological reefs, and stands of seagrasses, marshes, and mangroves. Moreover, the application of new molecular tools has improved our understanding of the diversity and genomic functions of estuarine microbes. This review synthesizes recent research on microbial habitats in estuaries and the contributions of microbes to estuarine food webs, elemental cycling, and interactions with plants and animals, and highlights novel insights provided by recent advances in genomics.
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Predation in a Microbial World: Mechanisms and Trade-Offs of Flagellate Foraging
Vol. 16 (2024), pp. 361–381More LessHeterotrophic nanoflagellates are the main consumers of bacteria and picophytoplankton in the ocean and thus play a key role in ocean biogeochemistry. They are found in all major branches of the eukaryotic tree of life but are united by all being equipped with one or a few flagella that they use to generate a feeding current. These microbial predators are faced with the challenges that viscosity at this small scale impedes predator–prey contact and that their foraging activity disturbs the ambient water and thus attracts their own flow-sensing predators. Here, I describe some of the diverse adaptations of the flagellum to produce sufficient force to overcome viscosity and of the flagellar arrangement to minimize fluid disturbances, and thus of the various solutions to optimize the foraging–predation risk trade-off. I demonstrate how insights into this trade-off can be used to develop robust trait-based models of microbial food webs.
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Life in the Midwater: The Ecology of Deep Pelagic Animals
Vol. 16 (2024), pp. 383–416More LessThe water column of the deep ocean is dark, cold, low in food, and under crushing pressures, yet it is full of diverse life. Due to its enormous volume, this mesopelagic zone is home to some of the most abundant animals on the planet. Rather than struggling to survive, they thrive—owing to a broad set of adaptations for feeding, behavior, and physiology. Our understanding of these adaptations is constrained by the tools available for exploring the deep sea, but this tool kit is expanding along with technological advances. Each time we apply a new method to the depths, we gain surprising insights about genetics, ecology, behavior, physiology, diversity, and the dynamics of change. These discoveries show structure within the seemingly uniform habitat, limits to the seemingly inexhaustible resources, and vulnerability in the seemingly impervious environment. To understand midwater ecology, we need to reimagine the rules that govern terrestrial ecosystems. By spending more time at depth—with whatever tools are available—we can fill the knowledge gaps and better link ecology to the environment throughout the water column.
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Phaeocystis: A Global Enigma
Vol. 16 (2024), pp. 417–441More LessThe genus Phaeocystis is globally distributed, with blooms commonly occurring on continental shelves. This unusual phytoplankter has two major morphologies: solitary cells and cells embedded in a gelatinous matrix. Only colonies form blooms. Their large size (commonly 2 mm but up to 3 cm) and mucilaginous envelope allow the colonies to escape predation, but data are inconsistent as to whether colonies are grazed. Cultured Phaeocystis can also inhibit the growth of co-occurring phytoplankton or the feeding of potential grazers. Colonies and solitary cells use nitrate as a nitrogen source, although solitary cells can also grow on ammonium. Phaeocystis colonies might be a major contributor to carbon flux to depth, but in most cases, colonies are rapidly remineralized in the upper 300 m. The occurrence of large Phaeocystis blooms is often associated with environments with low and highly variable light and high nitrate levels, with Phaeocystis antarctica blooms being linked additionally to high iron availability. Emerging results indicate that different clones of Phaeocystis have substantial genetic plasticity, which may explain its appearance in a variety of environments. Given the evidence of Phaeocystis appearing in new systems, this trend will likely continue in the near future.
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The Evolution, Assembly, and Dynamics of Marine Holobionts
Vol. 16 (2024), pp. 443–466More LessThe holobiont concept (i.e., multiple living beings in close symbiosis with one another and functioning as a unit) is revolutionizing our understanding of biology, especially in marine systems. The earliest marine holobiont was likely a syntrophic partnership of at least two prokaryotic members. Since then, symbiosis has enabled marine organisms to conquer all ocean habitats through the formation of holobionts with a wide spectrum of complexities. However, most scientific inquiries have focused on isolated organisms and their adaptations to specific environments. In this review, we attempt to illustrate why a holobiont perspective—specifically, the study of how numerous organisms form a discrete ecological unit through symbiosis—will be a more impactful strategy to advance our understanding of the ecology and evolution of marine life. We argue that this approach is instrumental in addressing the threats to marine biodiversity posed by the current global environmental crisis.
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Viruses in Marine Invertebrate Holobionts: Complex Interactions Between Phages and Bacterial Symbionts
Vol. 16 (2024), pp. 467–485More LessMarine invertebrates are ecologically and economically important and have formed holobionts by evolving symbiotic relationships with cellular and acellular microorganisms that reside in and on their tissues. In recent decades, significant focus on symbiotic cellular microorganisms has led to the discovery of various functions and a considerable expansion of our knowledge of holobiont functions. Despite this progress, our understanding of symbiotic acellular microorganisms remains insufficient, impeding our ability to achieve a comprehensive understanding of marine holobionts. In this review, we highlight the abundant viruses, with a particular emphasis on bacteriophages; provide an overview of their diversity, especially in extensively studied sponges and corals; and examine their potential life cycles. In addition, we discuss potential phage–holobiont interactions of various invertebrates, including participating in initial bacterial colonization, maintaining symbiotic relationships, and causing or exacerbating the diseases of marine invertebrates. Despite the importance of this subject, knowledge of how viruses contribute to marine invertebrate organisms remains limited. Advancements in technology and greater attention to viruses will enhance our understanding of marine invertebrate holobionts.
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Microbialite Accretion and Growth: Lessons from Shark Bay and the Bahamas
Vol. 16 (2024), pp. 487–511More LessMicrobialites provide geological evidence of one of Earth's oldest ecosystems, potentially recording long-standing interactions between coevolving life and the environment. Here, we focus on microbialite accretion and growth and consider how environmental and microbial forces that characterize living ecosystems in Shark Bay and the Bahamas interact to form an initial microbialite architecture, which in turn establishes distinct evolutionary pathways. A conceptual three-dimensional model is developed for microbialite accretion that emphasizes the importance of a dynamic balance between extrinsic and intrinsic factors in determining the initial architecture. We then explore how early taphonomic and diagenetic processes modify the initial architecture, culminating in various styles of preservation in the rock record. The timing of lithification of microbial products is critical in determining growth patterns and preservation potential. Study results have shown that all microbialites are not created equal; the unique evolutionary history of an individual microbialite matters.
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