Craig R. Smith

Man and the Last Great Wilderness: Human Impact on the Deep Sea

The deep sea, the largest ecosystem on Earth and one of the least studied, harbours high biodiversity and provides a wealth of resources. Although humans have used the oceans for millennia, technological developments now allow exploitation of fisheries resources, hydrocarbons and minerals below 2000 m depth. The remoteness of the deep seafloor has promoted the disposal of residues and litter. Ocean acidification and climate change now bring a new dimension of global effects. Thus the challenges facing the deep sea are large and accelerating, providing a new imperative for the science community, industry and national and international organizations to work together to develop successful exploitation management and conservation of the deep-sea ecosystem. This paper provides scientific expert judgement and a semi-quantitative analysis of past, present and future impacts of human-related activities on global deep-sea habitats within three categories: disposal, exploitation and climate change. The analysis is the result of a Census of Marine Life – SYNDEEP workshop (September 2008). A detailed review of known impacts and their effects is provided. The analysis shows how, in recent decades, the most significant anthropogenic activities that affect the deep sea have evolved from mainly disposal (past) to exploitation (present). We predict that from now and into the future, increases in atmospheric CO2 and facets and consequences of climate change will have the most impact on deep-sea habitats and their fauna. Synergies between different anthropogenic pressures and associated effects are discussed, indicating that most synergies are related to increased atmospheric CO2 and climate change effects. We identify deep-sea ecosystems we believe are at higher risk from human impacts in the near future: benthic communities on sedimentary upper slopes, cold-water corals, canyon benthic communities and seamount pelagic and benthic communities. We finalise this review with a short discussion on protection and management methods.

Abyssal food limitation, ecosystem structure and climate change.

The abyssal seafloor covers more than 50% of the Earth and is postulated to be both a reservoir of biodiversity and a source of important ecosystem services. We show that ecosystem structure and function in the abyss are strongly modulated by the quantity and quality of detrital food material sinking from the surface ocean. Climate change and human activities (e.g. successful ocean fertilization) will alter patterns of sinking food flux to the deep ocean, substantially impacting the structure, function and biodiversity of abyssal ecosystems. Abyssal ecosystem response thus must be considered in assessments of the environmental impacts of global warming and ocean fertilization.

Submarine canyons: hotspots of benthic biomass and productivity in the deep sea.

Submarine canyons are dramatic and widespread topographic features crossing continental and island margins in all oceans. Canyons can be sites of enhanced organic-matter flux and deposition through entrainment of coastal detrital export, dense shelf-water cascade, channelling of resuspended particulate material and focusing of sediment deposition. Despite their unusual ecological characteristics and global distribution along oceanic continental margins, only scattered information is available about the influence of submarine canyons on deep-sea ecosystem structure and productivity. Here, we show that deep-sea canyons such as the Kaikoura Canyon on the eastern New Zealand margin (42°01′ S, 173°03′ E) can sustain enormous biomasses of infaunal megabenthic invertebrates over large areas. Our reported biomass values are 100-fold higher than those previously reported for deep-sea (non-chemosynthetic) habitats below 500 m in the ocean. We also present evidence from deep-sea-towed camera images that areas in the canyon that have the extraordinary benthic biomass also harbour high abundances of macrourid (rattail) fishes likely to be feeding on the macro- and megabenthos. Bottom-trawl catch data also indicate that the Kaikoura Canyon has dramatically higher abundances of benthic-feeding fishes than adjacent slopes. Our results demonstrate that the Kaikoura Canyon is one of the most productive habitats described so far in the deep sea. A new global inventory suggests there are at least 660 submarine canyons worldwide, approximately 100 of which could be biomass hotspots similar to the Kaikoura Canyon. The importance of such deep-sea canyons as potential hotspots of production and commercial fisheries yields merits substantial further study.

Phytodetritus at the abyssal seafloor across 10 of latitude in the central equatorial Pacific

Fresh phytoplankton detritus (or phytodetritus) has been reported from numerous deep seafloor sites in the temperate North Atlantic and Pacific Oceans following seasonal phytoplankton blooms. Here we report the first strong evidence for abyssal accumulations of phytodetritus in the tropics, in the central equatorial Pacific. In November–December 1992 we obtained photographs and/or sediment-core samples from 61 abyssal stations (water depths of 4280–5012 m) between 12°S and 9°N along ∼ 140°W. Greenish flocculent material was recovered from the top of multiple-core samples from 5°S to 5°N; this material was most abundant from 2°S to 2°N, in some areas forming continuous layers at least 5 mm thick, and individual aggregates > 1 cm in diameter. The greenish material was clearly visible in bottom photographs as a green veneer that covered >95% of the seafloor near the equator, and as individual cm-scale aggregates covering <1% of the seafloor. Occasionally, thick accumulations of cm-scale aggregates occurred in biogenic pits. Cleared trails and feeding traces suggest that surface-deposit-feeding holothurians and echiurans grazed the greenish material. Microscopic examination of greenish material recovered from core tops and a burrow lumen revealed relatively intact diatoms (including Rhizosolenia sp.) and other microalgae with chloroplasts containing chlorophyll. The greenish material was 1–12.5% organic carbon by weight, i.e. 5–39 times richer than associated seafloor sediments. It also contained high excess activities of 234Th, suggesting arrival from the water column in the previous 100 days. Samples of the greenish flocculent material from 0° and 5°N incubated at simulated environmental pressure and temperature with 14C-labeled glutamate exhibited ⩾ 5-fold higher rates of microbial activity than underlying sediments or brown floc from 9°N. Surface-sediment samples (which included the greenish flocculent material) from 5°S to 5°N also contained significant concentrations of chlorophyll a and other chloropigments; the chloropigment concentrations were roughly comparable to deep-sea phytodetritus collected in the North Atlantic. We conclude that fresh, organic-rich phytodetritus was present on the seafloor from 5°S to 5°N along 140°W in November–December 1992, with highest concentrations within 2–3° of the equator. This material is likely to be a concentrated, high-quality food resource for deep-sea microbes and metazoans. We estimate an upper limit for the standing stock of this phytodetritus to be ∼2.6 mmol Corg/m2; this corresponds to ∼3% of the annual flux of organic carbon to the seafloor at these latitudes in 1992. Because the degradation rate of this material appears to be very high, its presence at the seafloor for several months per year could yield significant phytodetrital contributions to the annual seafloor organic-carbon budget. We also suggest that the phytodetrital aggregates are formed at intense convergence zones resulting from seasonal passage of tropical instability waves within 5° of the equator; if so, phytodetrital accumulations are likely to recur seasonally over broad areas of the abyssal equatorial Pacific.

The deep-sea floor ecosystem: current status and prospects of anthropogenic change by the year 2025

The goal of this paper is to review current impacts of human activities on the deep-sea floor ecosystem, and to predict anthropogenic changes to this ecosystem by the year 2025. The deep-sea floor ecosystem is one of the largest on the planet, covering roughly 60% of the Earths solid surface. Despite this vast size, our knowledge of the deep sea is poor relative to other marine ecosystems, and future human threats are difficult to predict. Low productivity, low physical energy, low biological rates, and the vastness of the soft-sediment deep sea create an unusual suite of conservation challenges relative to shallow water. The numerous, but widely spaced, island habitats of the deep ocean (for example seamounts, hydrothermal vents and submarine canyons) differ from typical deep-sea soft sediments in substrate type (hard) and levels of productivity (often high); these habitats will respond differently to anthropogenic impacts and climate change. The principal human threats to the deep sea are the disposal of wastes (structures, radioactive wastes, munitions and carbon dioxide), deep-sea fishing, oil and gas extraction, marine mineral extraction, and climate change. Current international regulations prohibit deep-sea dumping of structures, radioactive waste and munitions. Future disposal activities that could be significant by 2025 include deep-sea carbon-dioxide sequestration, sewage-sludge emplacement and dredge-spoil disposal. As fish stocks dwindle in the upper ocean, deep-sea fisheries are increasingly targeted. Most (perhaps all) of these deep-sea fisheries are not sustainable in the long term given current management practices; deep-sea fish are long-lived, slow growing and very slow to recruit in the face of sustained fishing pressure. Oil and gas exploitation has begun, and will continue, in deep water, creating significant localized impacts resulting mainly from accumulation of contaminated drill cuttings. Marine mineral extraction, in particular manganese nodule mining, represents one of the most significant conservation challenges in the deep sea. The vast spatial scales planned for nodule mining dwarf other potential direct human impacts. Nodule-mining disturbance will likely affect tens to hundreds of thousands of square kilometres with ecosystem recovery requiring many decades to millions of years (for nodule regrowth). Limited knowledge of the taxonomy, species structure, biogeography and basic natural history of deep-sea animals prevents accurate assessment of the risk of species extinctions from large-scale mining. While there are close linkages between benthic, pelagic and climatic processes, it is difficult to predict the impact of climate change on deep-sea benthic ecosystems; it is certain, however, that changes in primary production in surface waters will alter the standing stocks in the food-limited, deep-sea benthic. Long time-series studies from the abyssal North Pacific and North Atlantic suggest that even seemingly stable deep-sea ecosystems may exhibit change in key ecological parameters on decadal time scales. The causes of these decadal changes remain enigmatic. Compared to the rest of the planet, the bulk of the deep sea will probably remain relatively unimpacted by human activities and climate change in the year 2025. However, increased pressure on terrestrial resources will certainly lead to an expansion of direct human activities in the deep sea, and to direct and indirect environmental impacts. Because so little is known about this remote environment, the deep-sea ecosystem may well be substantially modified before its natural state is fully understood.

Do mussels take wooden steps to deep-sea vents?

Symbiont-containing mussels (Mytilidae) are found at hydrothermal vents and cold seeps on the ocean floor, but it is not known whether these taxa represent an ancient lineage endemic to these surroundings or are more recent invaders. Here we show that several small and poorly known mussels, commonly found on sunken wood and whale bones in the deep sea, are closely related to vent and seep taxa, and that this entire group is divergent from other Mytilidae. Our results indicate that vents and seeps were recently invaded by modern mytilid taxa and suggest that decomposing wood and bone may have served as ‘steps’ for the introduction of mytilid taxa to vents and seeps.

Age-dependent mixing of deep-sea sediments

Rates of bioturbation measured in deep-sea sediments commonly are tracer dependent; in particular, shorter lived radiotracers (such as 234Th) often yield markedly higher diffusive mixing coefficients than their longer-lived counterparts (e.g., 210Pb). At a single station in the 1240-m deep Santa Catalina Basin, we document a strong negative correlation between bioturbation rate and tracer half-life. Sediment profiles of 234Th (half-life = 24 days) yield an average mixing coefficient (60 cm2 y−1) two orders of magnitude greater than that for 210Pb (half-life = 22 y, mean mixing coefficient = 0.4 cm2 y−1). A similar negative relationship between mixing rate and tracer time scale is observed at thirteen other deep-sea sites in which multiple radiotracers have been used to assess diffusive mixing rates. This relationship holds across a variety of radiotracer types and time scales. We hypothesize that this negative relationship results from “age-dependent mixing,” a process in which recently sedimented, food-rich particles are ingested and mixed at higher rates by deposit feeders than are older, food-poor particles. Results from an age-dependent mixing model demonstrate that this process indeed can yield the bioturbation-rate vs. tracer-time-scale correlations observed in deep-sea sediments. Field data on mixing rates of recently sedimented particles, as well the radiotracer activity of deep-sea deposit feeders, provide strong support for the age-dependent mixing model. The presence of age-dependent mixing in deep-sea sediments may have major implications for diagenetic modeling, requiring a match between the characteristic time scales of mixing tracers and modeled reactants.

Latitudinal variations in benthic processes in the abyssal equatorial Pacific : control by biogenic particle flux

Abstract The equatorial Pacific forms a band of high, globally significant primary production. This productivity drops off steeply with distance from equatorial upwelling, yielding large latitudinal gradients in biogenic particle flux to the abyssal seafloor. As part of the US JGOFS Program, we studied the translation of these particle-flux gradients into the benthic ecosystem from 12°S to 9°N along 135–140°W to evaluate their control of key benthic processes, and to evaluate sediment proxies of export production from overlying waters. In October–December 1992 the remineralization rates of organic carbon, calcium carbonate and biogenic opal roughly matched the rain rates of these materials into deep sediment traps, exhibiting peak values within 3° of the equator. Rates of bioturbation near the equator were about ten-fold greater than at 9°N, and appeared to exhibit substantial dependence on particulate-organic-carbon flux, tracer time scale (i.e. age-dependent mixing), and pulsed mixing from burrowing urchins. Organic-carbon degradation within sediments near the equator was dominated by a very labile component (reaction rate constant, k approximately 15 per year) that appeared to be derived from greenish phytodetritus accumulated on the seafloor. Organic-carbon degradation at the highest latitudes was controlled by a less reactive component, with a mean k of approximately 0.075 per year. Where measured, megafaunal and macrofaunal abundances were strongly correlated with annual particulate-organic carbon flux; macrofaunal abundance in particular might potentially serve as a proxy for export production in low-energy abyssal habitats. Sedimentary microbial biomass also was correlated with the rain rate of organic carbon, but less strongly than larger biota and on shorter time scales (i.e. approximately 100 days). We conclude that the vertical flux of biogenic particlues exerts tight control on the nature and rates of benthic biological and chemical processes in the abyssal equatorial Pacific, and suggest that global changes in productivity on decadal or greater time scales could yield profound changes in deep-sea benthic ecoystems.

World-wide whale worms? A new species of Osedax from the shallow north Atlantic

We describe a new species of the remarkable whalebone-eating siboglinid worm genus, Osedax, from a whale carcass in the shallow north Atlantic, west of Sweden. Previously only recorded from deep-sea (1500–3000 m) whale-falls in the northeast Pacific, this is the first species of Osedax known from a shelf-depth whale-fall, and the first from the Atlantic Ocean. The new species, Osedax mucofloris sp. n., is abundant on the bones of an experimentally implanted Minke whale carcass (Balaenoptera acutorostrata) at 125 m depth in the shallow North Sea. O. mucofloris can be cultured on bones maintained in aquaria. The presence of O. mucofloris in the shallow North Sea and northeast Pacific suggests global distribution on whale-falls for the Osedax clade. Molecular evidence from mitochondrial cytochrome oxidase 1 (CO1) and 18S rRNA sequences suggests that O. mucofloris has high dispersal rates, and provides support for the idea of whale-falls acting as ‘stepping-stones’ for the global dispersal of siboglinid annelids over ecological and evolutionary time.

Deep-water taphonomy of vertebrate carcasses: a whale skeleton in the bathyal Santa Catalina Basin

Taphonomic processes in deep-water environments differ markedly from those in shallow waters. These differences are illustrated by the preservational style of a large cetacean skeleton lying at the bottom of the Santa Catalina Basin in 1,240 m of water. The degree of skeletal articulation contrasts with that documented in the shallow North Sea where gas-filled, buoyant carcasses dis- articulated during flotation. Increased hydrostatic pressure at greater depth is presumed to have prevented the whale carcass from floating and promoted increased levels of preservation. We present a model that relates gas evolution during decay to carcass buoyancy with depth. Application of this model may ultimately allow the degree of skeletal articulation to be used as a rough index of paleobathymetry.