Andrew K. Sweetman

Trophic Structure and Community Stability in an Overfished Ecosystem

Gobbled by Gobies A common feature of overfished marine ecosystems is a tendency for biomass to become dominated by jellyfish and microbes, and for the habitat to become anoxic or hypoxic as large fish species are removed. The Benguela ecosystem off the coast of Namibia is a case in point. Utne-Palm et al. (p. 333) describe how the loss of overfished sardines from the Benguela fishery has provided an opportunity for an endemic fish species, the bearded goby, to exploit jellyfish and microbial biomass and to increase in number. These small fish have in turn become the predominant prey species for the larger fish, birds, and mammals in the region. The significance of the goby lies in its ability to forage on resources traditionally regarded as “dead-ends.” The bearded goby has thus become a key stabilizing component to the turnover of energy in the Benguela ecosystem. An endemic goby exploits jellyfish and microbial biomass, partially restoring the food chain in the Benguela ecosystem. Since the collapse of the pelagic fisheries off southwest Africa in the late 1960s, jellyfish biomass has increased and the structure of the Benguelan fish community has shifted, making the bearded goby (Sufflogobius bibarbatus) the new predominant prey species. Despite increased predation pressure and a harsh environment, the gobies are thriving. Here we show that physiological adaptations and antipredator and foraging behaviors underpin the success of these fish. In particular, body-tissue isotope signatures reveal that gobies consume jellyfish and sulphidic diatomaceous mud, transferring “dead-end” resources back into the food chain.

A Call for Deep-Ocean Stewardship

The precautionary approach and collaborative governance must balance deep-ocean use and protection. Covering more than half the planet, the deep ocean sequesters atmospheric CO2 and recycles major nutrients; is predicted to hold millions of yet-to-be-described species; and stores mind-boggling quantities of untapped energy resources, precious metals, and minerals (1). It is an immense, remote biome, critical to the health of the planet and human well-being. The deep ocean (defined here as below a typical continental shelf break, >200 m) faces mounting challenges as technological advances—including robotics, imaging, and structural engineering—greatly improve access. We recommend a move from a frontier mentality of exploitation and single-sector management to a precautionary system that balances use of living marine resources, energy, and minerals from the deep ocean with maintenance of a productive and healthy marine environment, while improving knowledge and collaboration.

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.

Environmental Impacts of the Deep-Water Oil and Gas Industry: A Review to Guide Management Strategies

The industrialization of the deep sea is expanding worldwide. Expanding oil and gas exploration activities in the absence of sufficient baseline data in these ecosystems has made environmental management challenging. Here, we review the types of activities that are associated with global offshore oil and gas development in water depths over 200 m, the typical impacts of these activities, some of the more extreme impacts of accidental oil and gas releases, and the current state of management in the major regions of offshore industrial activity including 18 exclusive economic zones. Direct impacts of infrastructure installation, including sediment resuspension and burial by seafloor anchors and pipelines, are typically restricted to a radius of approximately 100 m on from the installation on the seafloor. Discharges of water-based and low-toxicity oil-based drilling muds and produced water can extend over 2 km, while the ecological impacts at the population and community levels on the seafloor are most commonly on the order of 200-300 m from their source. These impacts may persist in the deep sea for many years and likely longer for its more fragile ecosystems, such as cold-water corals. This synthesis of information provides the basis for a series of recommendations for the management of offshore oil and gas development. An effective management strategy, aimed at minimizing risk of significant environmental harm, will typically encompass regulations of the activity itself (e.g. discharge practices, materials used), combined with spatial (e.g. avoidance rules and marine protected areas) and temporal measures (e.g. restricted activities during peak reproductive periods). Spatial management measures that encompass representatives of all of the regional deep-sea community types is important in this context. Implementation of these management strategies should consider minimum buffer zones to displace industrial activity beyond the range of typical impacts: at least 2 km from any discharge points and surface infrastructure and 200 m from seafloor infrastructure with no expected discharges. Although managing natural resources is, arguably, more challenging in deep-water environments, inclusion of these proven conservation tools contributes to robust environmental management strategies for oil and gas extraction in the deep sea.

Rapid scavenging of jellyfish carcasses reveals the importance of gelatinous material to deep-sea food webs

Jellyfish blooms are common in many oceans, and anthropogenic changes appear to have increased their magnitude in some regions. Although mass falls of jellyfish carcasses have been observed recently at the deep seafloor, the dense necrophage aggregations and rapid consumption rates typical for vertebrate carrion have not been documented. This has led to a paradigm of limited energy transfer to higher trophic levels at jelly falls relative to vertebrate organic falls. We show from baited camera deployments in the Norwegian deep sea that dense aggregations of deep-sea scavengers (more than 1000 animals at peak densities) can rapidly form at jellyfish baits and consume entire jellyfish carcasses in 2.5 h. We also show that scavenging rates on jellyfish are not significantly different from fish carrion of similar mass, and reveal that scavenging communities typical for the NE Atlantic bathyal zone, including the Atlantic hagfish, galatheid crabs, decapod shrimp and lyssianasid amphipods, consume both types of carcasses. These rapid jellyfish carrion consumption rates suggest that the contribution of gelatinous material to organic fluxes may be seriously underestimated in some regions, because jelly falls may disappear much more rapidly than previously thought. Our results also demonstrate that the energy contained in gelatinous carrion can be efficiently incorporated into large numbers of deep-sea scavengers and food webs, lessening the expected impacts (e.g. smothering of the seafloor) of enhanced jellyfish production on deep-sea ecosystems and pelagic–benthic coupling.

Biological responses to disturbance from simulated deep-sea polymetallic nodule mining

Commercial-scale mining for polymetallic nodules could have a major impact on the deep-sea environment, but the effects of these mining activities on deep-sea ecosystems are very poorly known. The first commercial test mining for polymetallic nodules was carried out in 1970. Since then a number of small-scale commercial test mining or scientific disturbance studies have been carried out. Here we evaluate changes in faunal densities and diversity of benthic communities measured in response to these 11 simulated or test nodule mining disturbances using meta-analysis techniques. We find that impacts are often severe immediately after mining, with major negative changes in density and diversity of most groups occurring. However, in some cases, the mobile fauna and small-sized fauna experienced less negative impacts over the longer term. At seven sites in the Pacific, multiple surveys assessed recovery in fauna over periods of up to 26 years. Almost all studies show some recovery in faunal density and diversity for meiofauna and mobile megafauna, often within one year. However, very few faunal groups return to baseline or control conditions after two decades. The effects of polymetallic nodule mining are likely to be long term. Our analyses show considerable negative biological effects of seafloor nodule mining, even at the small scale of test mining experiments, although there is variation in sensitivity amongst organisms of different sizes and functional groups, which have important implications for ecosystem responses. Unfortunately, many past studies have limitations that reduce their effectiveness in determining responses. We provide recommendations to improve future mining impact test studies. Further research to assess the effects of test-mining activities will inform ways to improve mining practices and guide effective environmental management of mining activities.

First assessment of flux rates of jellyfish carcasses (jelly-falls) to the benthos reveals the importance of gelatinous material for biological C-cycling in jellyfish-dominated ecosystems

There is accumulating evidence that jellyfish contribute significantly to biological carbon cycling and that their carcasses can have controversial effects on seafloor ecosystems. Moreover, changes in the thermal properties of the ocean, ocean chemistry and direct anthropogenic effects can seriously modify jellyfish populations in surface waters and potentially alter the importance of jellyfish in the biological pump relative to other forms of detritus. However, no studies have ever quantified the flux rate of jellyfish carcasses (jelly-falls) to the seafloor, or quantified how jelly-fall C and N fluxes compare to phytodetrital fluxes. In this study, we documented the seafloor abundance of jelly-falls over a 1-year period in the jellyfish-dominated Lurefjord, western Norway. A total of 9 jelly-falls were documented from 768 seafloor images over the course of the study, equivalent to 0-13.4 mg C m-2 and 0-2.1 mg N m-2 of jellyfish material being deposited in the deep fjord basin. Assuming that jellyfish removal rates and phytodetrital flux rates from nearby fjord environments are similar to Lurefjorden, we estimate that the jellyfish C and N fluxes to the seafloor were 0-72.8 mg C m-2 d-1 and 0-11.2 mg N m-2 d-1 at the time of sampling. In addition, we estimate that the maximum jellyfish carcass flux rates were equivalent to 96 and 160% of the phytodetrital C and N flux that would arrive at the seafloor where the jelly-falls were recorded. These results imply that jelly-falls most likely contribute significantly to detrital C and N fluxes in at least one jellyfish-dominated environment, despite often being recorded in low abundances. If more fjord environments become jellyfish hotspots as a result of water column darkening, the contribution of jellyfish C and N in the biological pump will potentially increase, necessitating the conceptual inclusion of a jelly-pump in future fjord biogeochemical cycling studies.

Environmental factors structuring Arctic megabenthos—a case study from a shelf and two fjords

From photographic samples, we describe the benthic megafaunal communities in two north Svalbard fjords and on the adjacent continental shelf. We analyze the fauna in relation to abiotic factors of depth, bottom water temperature, percent cover of hard substratum, heterogeneity of stone size, and bottom-water turbidity to explore how these factors might affect the fauna and how they are related to the functional traits (size, morphology, mobility, colonial/solitary, and feeding type) of the megabenthos. Depth and bottom water temperature were consistently the strongest correlates with faunal composition and functional traits of the constituent species. A greater proportion of the variability in the functional traits of the megabenthos could be explained by abiotic factors rather than faunal composition, indicating that the abiotic factors of depth and temperature were strongly related to the functional traits of the megabenthos. On a local scale, stone size heterogeneity explained most variation in the functional traits of the megabenthos in one fjord. The results of this case study show a significant relationship between bottom water temperature and the functioning of north Svalbard megabenthic communities. Warming temperatures in the Arctic will likely decrease the variety of functional traits represented in Svalbard megabentos, resulting in scavenger-dominated communities. A reduction in megabenthic biomass may also result, reducing energy availability to higher trophic levels.

Impaired short-term functioning of a benthic community from a deep Norwegian fjord following deposition of mine tailings and sediments

The extraction of minerals from land-based mines necessitates the disposal of large amounts of mine tailings. Dumping and storage of tailings into the marine environment, such as fjords, is currently being performed without knowing the potential ecological consequences. This study investigated the effect of short-term exposure to different deposition depths of inert iron ore tailings (0.1, 0.5 and 3 cm) and dead subsurface sediment (0.5 and 3 cm) on a deep water (200 m) fjord benthic assemblage in a microcosm experiment. Biotic and abiotic variables were measured to determine structural and functional changes of the benthic community following an 11 and 16 day exposure with tailings and dead sediment, respectively. Structural changes of macrofauna, meiofauna and bacteria were measured in terms of biomass, density, community composition and mortality while measures of oxygen penetration depth, sediment community oxygen consumption and 13C-uptake and processing by biota revealed changes in the functioning of the system. Burial with mine tailings and natural sediments modified the structure and functioning of the benthic community albeit in a different way. Mine tailings deposition of 0.1 cm and more resulted in a reduced capacity of the benthic community to remineralize fresh 13C-labelled algal material, as evidenced by the reduced sediment community oxygen consumption and uptake rates in all biological compartments. At 3 cm of tailings deposition, it was evident that nematode mortality was higher inside the tailings layer, likely caused by reduced food availability. In contrast, dead sediment addition led to an increase in oxygen consumption and bacterial carbon uptake comparable to control conditions, thereby leaving deeper sediment layers anoxic and in turn causing nematode mortality at 3 cm deposition. This study clearly shows that even small levels (0.1 cm) of instantaneous burial by mine tailings may significantly reduce benthic ecosystem functioning on the short term. Furthermore, it reveals the importance of substrate characteristics and origin when studying the effects of substrate addition on marine benthic fauna. Our findings should alert decision makers when considering approval of new deep-sea tailings placement sites as this technique will have major negative impacts on benthic ecosystem functioning over large areas.

Metabolic rates are significantly lower in abyssal Holothuroidea than in shallow-water Holothuroidea

Recent analyses of metabolic rates in fishes, echinoderms, crustaceans and cephalopods have concluded that bathymetric declines in temperature- and mass-normalized metabolic rate do not result from resource-limitation (e.g. oxygen or food/chemical energy), decreasing temperature or increasing hydrostatic pressure. Instead, based on contrasting bathymetric patterns reported in the metabolic rates of visual and non-visual taxa, declining metabolic rate with depth is proposed to result from relaxation of selection for high locomotory capacity in visual predators as light diminishes. Here, we present metabolic rates of Holothuroidea, a non-visual benthic and benthopelagic echinoderm class, determined in situ at abyssal depths (greater than 4000 m depth). Mean temperature- and mass-normalized metabolic rate did not differ significantly between shallow-water (less than 200 m depth) and bathyal (200–4000 m depth) holothurians, but was significantly lower in abyssal (greater than 4000 m depth) holothurians than in shallow-water holothurians. These results support the dominance of the visual interactions hypothesis at bathyal depths, but indicate that ecological or evolutionary pressures other than biotic visual interactions contribute to bathymetric variation in holothurian metabolic rates. Multiple nonlinear regression assuming power or exponential models indicates that in situ hydrostatic pressure and/or food/chemical energy availability are responsible for variation in holothurian metabolic rates. Consequently, these results have implications for modelling deep-sea energetics and processes.