Henry A. Ruhl

Climate, carbon cycling, and deep-ocean ecosystems

Climate variation affects surface ocean processes and the production of organic carbon, which ultimately comprises the primary food supply to the deep-sea ecosystems that occupy ≈60% of the Earths surface. Warming trends in atmospheric and upper ocean temperatures, attributed to anthropogenic influence, have occurred over the past four decades. Changes in upper ocean temperature influence stratification and can affect the availability of nutrients for phytoplankton production. Global warming has been predicted to intensify stratification and reduce vertical mixing. Research also suggests that such reduced mixing will enhance variability in primary production and carbon export flux to the deep sea. The dependence of deep-sea communities on surface water production has raised important questions about how climate change will affect carbon cycling and deep-ocean ecosystem function. Recently, unprecedented time-series studies conducted over the past two decades in the North Pacific and the North Atlantic at >4,000-m depth have revealed unexpectedly large changes in deep-ocean ecosystems significantly correlated to climate-driven changes in the surface ocean that can impact the global carbon cycle. Climate-driven variation affects oceanic communities from surface waters to the much-overlooked deep sea and will have impacts on the global carbon cycle. Data from these two widely separated areas of the deep ocean provide compelling evidence that changes in climate can readily influence deep-sea processes. However, the limited geographic coverage of these existing time-series studies stresses the importance of developing a more global effort to monitor deep-sea ecosystems under modern conditions of rapidly changing climate.

Temporal change in deep-sea benthic ecosystems: a review of the evidence from recent time-series studies

Societal concerns over the potential impacts of recent global change have prompted renewed interest in the long-term ecological monitoring of large ecosystems. The deep sea is the largest ecosystem on the planet, the least accessible, and perhaps the least understood. Nevertheless, deep-sea data collected over the last few decades are now being synthesised with a view to both measuring global change and predicting the future impacts of further rises in atmospheric carbon dioxide concentrations. For many years, it was assumed by many that the deep sea is a stable habitat, buffered from short-term changes in the atmosphere or upper ocean. However, recent studies suggest that deep-seafloor ecosystems may respond relatively quickly to seasonal, inter-annual and decadal-scale shifts in upper-ocean variables. In this review, we assess the evidence for these long-term (i.e. inter-annual to decadal-scale) changes both in biologically driven, sedimented, deep-sea ecosystems (e.g. abyssal plains) and in chemosynthetic ecosystems that are partially geologically driven, such as hydrothermal vents and cold seeps. We have identified 11 deep-sea sedimented ecosystems for which published analyses of long-term biological data exist. At three of these, we have found evidence for a progressive trend that could be potentially linked to recent climate change, although the evidence is not conclusive. At the other sites, we have concluded that the changes were either not significant, or were stochastically variable without being clearly linked to climate change or climate variability indices. For chemosynthetic ecosystems, we have identified 14 sites for which there are some published long-term data. Data for temporal changes at chemosynthetic ecosystems are scarce, with few sites being subjected to repeated visits. However, the limited evidence from hydrothermal vents suggests that at fast-spreading centres such as the East Pacific Rise, vent communities are impacted on decadal scales by stochastic events such as volcanic eruptions, with associated fauna showing complex patterns of community succession. For the slow-spreading centres such as the Mid-Atlantic Ridge, vent sites appear to be stable over the time periods measured, with no discernable long-term trend. At cold seeps, inferences based on spatial studies in the Gulf of Mexico, and data on organism longevity, suggest that these sites are stable over many hundreds of years. However, at the Haakon Mosby mud volcano, a large, well-studied seep in the Barents Sea, periodic mud slides associated with gas and fluid venting may disrupt benthic communities, leading to successional sequences over time. For chemosynthetic ecosystems of biogenic origin (e.g. whale-falls), it is likely that the longevity of the habitat depends mainly on the size of the carcass and the ecological setting, with large remains persisting as a distinct seafloor habitat for up to 100 years. Studies of shallow-water analogs of deep-sea ecosystems such as marine caves may also yield insights into temporal processes. Although it is obvious from the geological record that past climate change has impacted deep-sea faunas, the evidence that recent climate change or climate variability has altered deep-sea benthic communities is extremely limited. This mainly reflects the lack of remote sensing of this vast seafloor habitat. Current and future advances in deep-ocean benthic science involve new remote observing technologies that combine a high temporal resolution (e.g. cabled observatories) with spatial capabilities (e.g. autonomous vehicles undertaking image surveys of the seabed).

Connections between climate, food limitation, and carbon cycling in abyssal sediment communities

Diverse faunal groups inhabit deep-sea sediments over much of Earths surface, but our understanding of how interannual-scale climate variation alters sediment community components and biogeochemical processes remains limited. The vast majority of deep-sea communities depend on a particulate organic carbon food supply that sinks from photosynthetically active surface waters. Variations in food supply depend, in part, on surface climate conditions. Proposed ocean iron fertilization efforts are also intended to alter surface production and carbon export from surface waters. Understanding the ecology of the abyssal sediment community and constituent metazoan macrofauna is important because they influence carbon and nutrient cycle processes at the seafloor through remineralization, bioturbation, and burial of the sunken material. Results from a 10-year study in the abyssal NE Pacific found that climate-driven variations in food availability were linked to total metazoan macrofauna abundance, phyla composition, rank-abundance distributions, and remineralization over seasonal and interannual scales. The long-term analysis suggests that broad biogeographic patterns in deep-sea macrofauna community structure can change over contemporary timescales with changes in surface ocean conditions and provides significant evidence that sediment community parameters can be estimated from atmospheric and upper-ocean conditions. These apparent links between climate, the upper ocean, and deep-sea biogeochemistry need to be considered in determining the long-term carbon storage capacity of the ocean.

Biotic and Human Vulnerability to Projected Changes in Ocean Biogeochemistry over the 21st Century

Mora and colleagues show that ongoing greenhouse gas emissions are likely to have a considerable effect on several biogeochemical properties of the worlds oceans, with potentially serious consequences for biodiversity and human welfare.

ABUNDANCE AND SIZE DISTRIBUTION DYNAMICS OF ABYSSAL EPIBENTHIC MEGAFAUNA IN THE NORTHEAST PACIFIC

The importance of interannual variation in deep-sea abundances is now becoming recognized. There is, however, relatively little known about what processes dominate the observed fluctuations. The abundance and size distribution of the megabenthos have been examined here using a towed camera system at a deep-sea station in the northeast Pacific (Station M) from 1989 to 2004. This 16-year study included 52 roughly seasonal transects averaging 1.2 km in length with over 35600 photographic frames analyzed. Mobile epibenthic megafauna at 4100 m depth have exhibited interannual scale changes in abundance from one to three orders of magnitude. Increases in abundance have now been significantly linked to decreases in mean body size, suggesting that accruals in abundance probably result from the recruitment of young individuals. Examinations of size-frequency histograms indicate several possible recruitment events. Shifts in size-frequency distributions were also used to make basic estimations of individual growth rates from 1 to 6 mm/month, depending on the taxon. Regional intensification in reproduction followed by recruitment within the study area could explain the majority of observed accruals in abundance. Although some adult migration is certainly probable in accounting for local variation in abundances, the slow movements of benthic life stages restrict regional migrations for most taxa. Negative competitive interactions and survivorship may explain the precipitous declines of some taxa. This and other studies have shown that abundances from protozoans to large benthic invertebrates and fishes all have undergone significant fluctuations in abundance at Station M over periods of weeks to years.

Global reductions in seafloor biomass in response to climate change

Seafloor organisms are vital for healthy marine ecosystems, contributing to elemental cycling, benthic remineralization, and ultimately sequestration of carbon. Deep-sea life is primarily reliant on the export flux of particulate organic carbon from the surface ocean for food, but most ocean biogeochemistry models predict global decreases in export flux resulting from 21st century anthropogenically induced warming. Here we show that decadal-to-century scale changes in carbon export associated with climate change lead to an estimated 5.2% decrease in future (2091–2100) global open ocean benthic biomass under RCP8.5 (reduction of 5.2 Mt C) compared with contemporary conditions (2006–2015). Our projections use multi-model mean export flux estimates from eight fully coupled earth system models, which contributed to the Coupled Model Intercomparison Project Phase 5, that have been forced by high and low representative concentration pathways (RCP8.5 and 4.5, respectively). These export flux estimates are used in conjunction with published empirical relationships to predict changes in benthic biomass. The polar oceans and some upwelling areas may experience increases in benthic biomass, but most other regions show decreases, with up to 38% reductions in parts of the northeast Atlantic. Our analysis projects a future ocean with smaller sized infaunal benthos, potentially reducing energy transfer rates though benthic multicellular food webs. More than 80% of potential deep-water biodiversity hotspots known around the world, including canyons, seamounts, and cold-water coral reefs, are projected to experience negative changes in biomass. These major reductions in biomass may lead to widespread change in benthic ecosystems and the functions and services they provide.

LONG-TERM CHANGE IN BENTHOPELAGIC FISH ABUNDANCE IN THE ABYSSAL NORTHEAST PACIFIC OCEAN

Food web structure, particularly the relative importance of bottom-up and top-down control of animal abundances, is poorly known for the Earths largest habitats: the abyssal plains. A unique 15-yr time series of climate, productivity, particulate flux, and abundance of primary consumers (primarily echinoderms) and secondary consumers (fish) was examined to elucidate the response of trophic levels to temporal variation in one another. Towed camera sled deployments in the abyssal northeast Pacific (4100 m water depth) showed that annual mean numbers of the dominant fish genus (Coryphaenoides spp.) more than doubled over the period 1989-2004. Coryphaenoides spp. abundance was significantly correlated with total abundance of mobile epibenthic megafauna (echinoderms), with changes in fish abundance lagging behind changes in the echinoderms. Direct correlations between surface climate and fish abundances, and particulate organic carbon (POC) flux and fish abundances, were insignificant, which may be related to the varied response of the potential prey taxa to climate and POC flux. This study provides a rare opportunity to study the long-term dynamics of an unexploited marine fish population and suggests a dominant role for bottom-up control in this system.

Deep ocean communities impacted by changing climate over 24 y in the abyssal northeast Pacific Ocean

Significance Global warming is now a well-documented phenomenon that is influencing every aspect of our world, from increased storm intensity to melting of polar ice sheets and rising sea level. The impact of such changes in climate is least known for the deep ocean, which covers over 60% of the earth’s surface. An unprecedented 24-y time series measuring changes in food supply and utilization by benthic communities at 4,000-m depth in the deep northeast Pacific reveal strong connectivity with changing surface ocean conditions, which have broad implications for the global carbon cycle. The deep ocean, covering a vast expanse of the globe, relies almost exclusively on a food supply originating from primary production in surface waters. With well-documented warming of oceanic surface waters and conflicting reports of increasing and decreasing primary production trends, questions persist about how such changes impact deep ocean communities. A 24-y time-series study of sinking particulate organic carbon (food) supply and its utilization by the benthic community was conducted in the abyssal northeast Pacific (∼4,000-m depth). Here we show that previous findings of food deficits are now punctuated by large episodic surpluses of particulate organic carbon reaching the sea floor, which meet utilization. Changing surface ocean conditions are translated to the deep ocean, where decadal peaks in supply, remineralization, and sequestration of organic carbon have broad implications for global carbon budget projections.

Long-term reductions in anthropogenic nutrients link to improvements in Chesapeake Bay habitat

Great effort continues to focus on ecosystem restoration and reduction of nutrient inputs thought to be responsible, in part, for declines in estuary habitats worldwide. The ability of environmental policy to address restoration is limited, in part, by uncertainty in the relationships between costly restoration and benefits. Here, we present results from an 18-y field investigation (1990–2007) of submerged aquatic vegetation (SAV) community dynamics and water quality in the Potomac River, a major tributary of the Chesapeake Bay. River and anthropogenic discharges lower water clarity by introducing nutrients that stimulate phytoplankton and epiphyte growth as well as suspended sediments. Efforts to restore the Chesapeake Bay are often viewed as failing. Overall nutrient reduction and SAV restoration goals have not been met. In the Potomac River, however, reduced in situ nutrients, wastewater-treatment effluent nitrogen, and total suspended solids were significantly correlated to increased SAV abundance and diversity. Species composition and relative abundance also correlated with nutrient and water-quality conditions, indicating declining fitness of exotic species relative to native species during restoration. Our results suggest that environmental policies that reduce anthropogenic nutrient inputs do result in improved habitat quality, with increased diversity and native species abundances. The results also help elucidate why SAV cover has improved only in some areas of the Chesapeake Bay.

Community change in the variable resource habitat of the abyssal northeast Pacific.

Research capable of differentiating resource-related community-level change from random ecological drift in natural systems has been limited. Evidence for nonrandom, resource-driven change is presented here for an epibenthic megafauna community in the abyssal northeast Pacific Ocean from 1989 to 2004. The sinking particulate organic carbon food supply is linked not only to species-specific abundances, but also to species composition and equitability. Shifts in rank abundance distributions (RADs) and evenness, from more to less equitable, correlated to increased food supply during La Niña phases of the El Niño Southern Oscillation. The results suggest that each taxon exhibited a differential response to a sufficiently low dimension resource, which led to changes in community composition and equitability. Thus the shifts were not likely due to random ecological drift. Although the community can undergo population-level variations of one or more orders of magnitude, and the shape of the RADs was variable, the organization retained a significant consistency, providing evidence of limits for such changes. The growing evidence for limited resource-driven changes in RADs and evenness further emphasizes the potential importance of temporally variable disequilibria in understanding why communities have certain basic attributes.