Abstract

The surprisingly high species diversity found among the mostly smallbodied invertebrates inhabiting the deep-sea sediment is thought to be maintained by biologically generated habitat heterogeneity and patchy food resources acting in concert with biological disturbance at the metre to centimetre scale or less (Grassle & Maciolek, 1992). Disturbance is thought to thin existing populations, and is followed by recolonisation of the disturbed patch, to that the populations never develop to a full competitive equilibrium before the next disturbance event.

This review focuses on the possible importance of larger, >kilometre scale disturbance, generated by currents at the deep-sea floor. Data on species richness and abundance from quantitative benthic samples from five areas presenting varying space–time scales in hydrodynamic disturbance are reviewed, in order to show that such diffuse disturbance of the sediment community resulting from episodes of high bed flow in the supposedly tranquil physical conditions at the deep-sea bed may be an important structuring agent for the deep-sea benthic community. The first area is located at the High Energy Benthic Boundary Layer (HEBBLE) study site on the Nova Scotian continental rise in the North West Atlantic, where the sediment floor periodically experiences strong flow and massive re-suspension during vorticity-driven ‘benthic storms’ and hence where eddy kinetic energy, KE, is very high in the benthic mixed layer.

THE SHAPE OF THE SEA FLOOR

The topography of the floor of the deep ocean (Fig. 2.1) is a balance between the parameters of seafloor spreading and sedimentation of inorganic and organic particles. Around the periphery of the ocean basins lies a continental shelf of varying width ending at the shelf break, usually at a depth of c. 200 m, below which plant life is supposed to be absent. In the Antarctic, owing to the weight of the ice cap, the shelf edge is at c. 500 m. If we accept topographic criteria, the deep sea may be said to begin at the shelf break. This is a safer distinction than one based on photosynthetic depth since attached seaweeds have been found as deep as 268 m off the Bahamas (Littler et al., 1985).

Seaward of the shelf edge there is a marked increase in the downward gradient of the seabed indicating the continental slope (Fig. 2.2). The slope may be a simple structure where the isobaths are parallel to each other and evenly spaced or it may contain a series of irregularities to give a very uneven gradient. The slope marks the underlying boundary between oceanic and continental crust. The theory of plate tectonics tells us that these areas of crust consist of a dynamic system of plates where crust is both being formed at mid-ocean ridge spreading centres and consumed by subduction at ‘active’, or seismic margins typical in the Pacific (Fig. 2.3).

In the short history of the subject, the rapidly expanding knowledge of the physical nature and processes of the deep oceans has very much determined the approach and methodology adopted in the biological study of this, the most remote and seemingly ‘difficult’ of environments for life on Earth. At the time of the pioneering voyage of the ‘Challenger’, knowledge of deep-ocean bathymetry barely existed, vast areas of ocean basins had never been sounded, and a certain sameness in the catch of larger animals trawled from the depths, as the ship worked wide-spaced stations across the ocean basins, encouraged a view of an almost endless, though impoverished, uniformity in the animal life existing on the deep-sea ooze. Such a view encouraged workers to think that it is perfectly feasible to make generalizations of deep-sea biology from single and widely spaced hauls made with the relatively crude technical gear available. As graphically illustrated by Sparck (1956a), the idea of assessing the ocean's fauna by means of a few trawl and dredge hauls is absurd in relation to its vast area and volume: fishing up a postman and a policeman from a net cast randomly from a balloon floating above land might similarly lead to a distorted picture of a human population below made up entirely of postmen and policemen!

This concept of uniformity remains valid today only in a restricted way.

There are two major variables that are clearly related to resource availability in the deep-sea environment. First, the density (standing crop), expressed either as biomass, organic or carbon content, or numbers of individuals; and second the body size of individuals. With both, a large literature has demonstrated, or qualified, an inverse relationship to bathymetry along the depth gradient from the continental shelf to the abyss.

DENSITY

In this chapter we shall concentrate on quantitative investigations of the abundance of benthic life on and within the deep-sea bottom. This is because quantitative data on the purely benthopelagic fauna are very sparse. However, there are indications that biomass of gelatinous organisms, such as sea cucumbers, found swimming just off the bottom may, in places, be high (Childress et al., 1989). We shall consider biomass of other benthopelagic organisms, such as large, swimming scavenging organisms, along with other megafauna later in the chapter.

Quantitative studies of the deep-sea benthos date from the 1950s with the cruise of the ‘Galathea’. On this voyage a 0.2 m2 Petersen grab was first used in the deep sea (Spärck, 1956b) and this followed upon many Russian deep-sea expeditions using the 0.25 m2 ‘Okean’ grab (Filatova, 1982). The Russian studies have underlined the positive relationship between pelagic and benthic productivity, and their results (Fig. 7.1) largely reinforce the general prediction that density of benthic life decreases with depth and distance from shore, as well as from polar and temperate to tropical latitudes (Filatova, 1982).

These animals are usually subdivided into size-based categories (that are also reflected by peaks in size-class spectra (see Chapter 7); the meioben-thos, being defined as those animals that are retained by the finest screens down to a mesh opening of 62 microns or smaller, and the macrobenthos as that part retained by sieves with meshes of about 1 mm (Mare, 1942; Mclntyre, 1969). Those mostly single-celled organisms, such as Pro-karyotes (lacking the outer cell membranes of Eukaryotic unicells), yeastlike cells, certain sorts of Protozoans (single-celled animals, some with a quite complex organization such as ciliates) and some early stages of meiobenthic Metazoans (multicelled animals) in the size range from about 40 to 2 microns, make up an additional category, the nanobenthos (Thiel, 1983) which falls between meiofauna and bacteria.

However, the division of the benthos above nanobenthos level into size-based groupings has little ecological and even less taxonomic justification in the deep sea. This is because of a trend towards miniaturization (see Chapter 7) which has occurred to the extent that the deep sea has been termed a ‘small-organism habitat’ (Thiel, 1975). Clearly, this trend has not affected the megafauna described earlier where in some groups, such as scavenging amphipods, a reverse trend towards gigantism has occurred. However, the trend to miniaturization is well marked amongst the macrofauna (Sanders, Hessler & Hampson, 1965; Rowe & Menzel, 1971; Rowe, 1971a). Furthermore, Hessler (1974) found that he had to use a 0.3 mm screen to catch the sparse macrofauna in box-cores from the central N. Pacific, noting that individuals here are so small as to be of meiofaunal size.

MICROBIAL ECOLOGY: APPROACH AND PROBLEMS

The first observations of bacterial populations in the deep sea were made in 1882 and 1883 during the cruises of the ‘Travailleur’ and ‘Talisman’ (Certes, 1884). Although observations continued to be made, no data became available on rates of deep-sea bacterial metabolism until the early 1950s. Morita & Zobell (1955) and Zobell and Morita (1957) demonstrated that bacterial activity in deep-sea sediments was very low. This was not thought surprising as the low temperature, high pressure and low nutrient levels known to occur in the deep sea did not present a particularly favourable milieu for bacterial growth. All bacterial activity in the deep sea (with the exception of chemosynthesis which is limited to hydrothermal vents and sulphide-rich cold seeps – see Chapter 15) is heterotrophic, requiring an energy source in the form of organic matter ultimately derived from surface production.

In the last 20 years there has been a great effort in understanding the bacterial ecology of the deep sea. This effort was stimulated by two unrelated events. The first was the accidental sinking of the submersible ‘Alvin’. The submersible was swamped by a wave on launching. The crew escaped but left behind their lunch which consisted of bouillon, bologna sandwiches and apples. When ‘Alvin’ was recovered one year later, the scientists were amazed to find the food was still in good condition (see photograph in Jannasch, 1978) within the flooded pressure sphere, but it soon rotted even in a refrigerator at atmospheric pressure (Jannasch et al., 1970).

HORIZONTAL DISTRIBUTIONS IN THE DEEP SEA

Deriving from the monotony of the fauna from abyssal basins in trawlings undertaken world-wide during the pioneering voyage of the ‘Challenger’, the first conception of the zoogeography of the deep sea was of a single province, sharing many species with cosmopolitan distributions. Although this view was supported by Bruun (1957), other workers have perceived some differentiation of the abyssal into four zoogeographic zones, the Atlantic, Indo-Pacific, Arctic and Antarctic (Ekman, 1953). The extensive global sampling investigations of Russian workers has been summarized in English by Vinogradova (1959, 1962a,b, 1979). She found only 15% of species occurring in more than one ocean and only 4% being found in all of them. These conclusions follow the philosophy of an essentially unified fauna for the abyssal and hadal zones; whilst recognizing substantial differentiation has occurred in different oceanic regions, particularly those corresponding to topographic boundaries such as trenches (Fig. 10.1).

For the N. Atlantic, these conclusions were essentially similar to those of Mortensen (1907), and are more or less supported by zoogeographic analyses of collections from the ‘Galathea’ expedition (Kirkegaard, 1954; Wolff, 1962; Levi, 1964; Millar, 1970). Other schemes developed from the ‘Galathea’ sampling differ only with respect to the major faunistic connections (Madsen, 1961b; Hansen, 1967,1975; Knudsen, 1979). Other, more complex, schemes have been developed subdividing Ekman's zones into further subareas and provinces with species having quite narrow ranges separated by topographic barriers (Clark, 1962) or mainly related to the origin and temperature structure of deep-water masses (Menzies et al., 1973).

In this book we focus on the sorts of animal life inhabiting the benthic boundary. Deep-sea sampling world-wide has demonstrated that the evolutionary radiation of life has penetrated to all parts of the world ocean. Animal life has been recovered from the depths of the Arctic Ocean under the polar ice cap to the greatest depths of the deepest ocean trench. Only in anoxic basins where sulphide bacteria flourish are animals virtually excluded.

CATEGORIES OF FAUNA

The fauna of the benthic boundary is comprised of those animals living either on the ocean floor, the benthos, or those associated with the immediately overlying water, the benthopelagic fauna, which comprises swimming or drifting forms, some of which may spend varying amounts of time on, or even buried in, the seabed.

This is not to deny the importance of the other major categories of life which impinge on the seafloor, but normally spend their entire lives swimming (the nekton) or drifting (the plankton) in the overlying water. Biomass of these pelagic communities is highest near the surface, and decreases exponentially with increasing depth until at 4 km depth it is about 1% of that at the surface (Angel & Baker, 1982). However, Wishner (1980a) found, from a net attached to the deeply towed instrument package ‘Deep Tow’ (see Chapter 3), that abundance starts to increase 100 m above the bottom and doubles at 10 m above.

From the days of the ‘Challenger’ expedition, biological oceanographers had relied on intuition that the extreme physical conditions and impoverished nutritional input could be tolerated only by a small number of specialized forms of life. This concept was overturned in the 1960s after examination of bottom samples obtained by Howard Sanders and Robert Hessler at the Woods Hole Oceanographic Institution using the fine-meshed epibenthic sled (see Chapter 5) uncovered an astonishing richness in species of the smaller animals dwelling in the deep-sea sediments (Hessler & Sanders, 1967; Sanders & Hessler, 1969). These workers showed that the trend of decreasing diversity with increasing depth in species caught in relatively coarse meshed deep-sea trawls was an artefact resulting from the decreased density of individual animals and the small number of samples taken at great depths.

Also, such high species richness had not been predicted by theoretical ecologists. Environments that are seemingly spatial and temporally uniform, with few and low-grade nutritional sources, were thought to tend towards an equilibrium with just a few competing species (Hutchin-son, 1953). We shall examine the literature that has attempted to explain this apparent anomaly. But first we must define the concept so that its measurement becomes tractable.

MEASUREMENT OF DIVERSITY

The term diversity is commonly used as a synonym for species richness, the number of species present in the community.