Benthic Living: Sublittoral and Deep Seabed PDF

CHAPTER 7 Benthic living: sublittoral and deep seabed Benthic organisms are those that live on or in the seabed, anywhere from the seashore down to abyssal depths. Benthic organisms living on the seashore have already been covered in Chapter 6 and the current chapter covers the equivalent ecology...

CHAPTER 7 Benthic living: sublittoral and deep seabed Benthic organisms are those that live on or in the seabed, anywhere from the seashore down to abyssal depths. Benthic organisms living on the seashore have already been covered in Chapter 6 and the current chapter covers the equivalent ecology and habi- tats of organisms living below the lowest tide level, that is permanently submerged. The sea floor is an area of great contrasts, and this is obviously a huge subject, covering as it does, everything from deep ocean ‘deserts’ of soft sediment to rich coral reefs. Benthic communities on the continental shelf from 0 to 200 m depth are generally described as sublittoral. Beyond this sublittoral zone, animal communities in the bathy- benthic zone extend down the continental slope to around 4000 m. Abyssobenthic communities are found from the bottom of the continental slope at around 3000 4000 m to the deepest depths. The major depth zones and divisions for the sea floor are shown in Fig. 1.9 and described in Sections 1.1.2 1.1.5. As well as depth limitations, exactly what lives on and within the seabed depends pri- marily on the substratum, which is the type of seabed, modified by other conditions. Light and wave action have profound effects on sublittoral communities. Given the right conditions, light can be detected down to 1000 m but by 200 m depth there is only about 1% of surface sunlight, too little for photosynthetic activities. The effects of wind- generated waves are only felt on the seabed at depths down to about half the wavelength (the distance between wave crests). In practice this generally means down to about 50 m and exceptionally 150 m because the maximum wavelength of normal waves is about 300 m. Current speed has an influence far beyond the sublittoral and availability of food is an important aspect at any depth. Except in very shallow depths, the temperature, salinity, illumination and movements of the water at the bottom are less variable than in the sur- face layers. Below 500 m seasonal changes in these variables are negligible and the deeper the water the more constant are the conditions. Food supply is an obvious influencing factor in the development of benthic com- munities, especially for sessile (fixed) animals. Since primary production is limited to shallow depths, deep benthic communities rely for food on organic matter sinking from the overlying water and on dissolved organic matter (DOM) in the water. In some areas this food supply may be sufficient to support a relatively high biomass and complex communities (see Section 7.3.4 Deep-sea food supply). Benthic communities Elements of Marine Ecology r 2022 Elsevier Ltd. DOI: https://doi.org/10.1016/B978-0-08-102826-1.00007-7 All rights reserved. 319 320 Elements of Marine Ecology beneath shallow water have direct access to primary production from benthic algae and phytoplankton to depths of 50 200 m depending on water clarity. Many bottom-dwelling animals are able to live and grow to large size with relatively little expenditure of energy in hunting and collecting food, because they can obtain ade- quate nourishment simply by gathering the particles that fall within their reach or are carried to them by the currents. Others simply digest the organic matter and associated bacteria contained within the sediment. Compared with the pelagic (open water) division of the marine environment (see Chapters 4 and 5) the seabed provides a far wider variety of habitats for marine organ- isms and in very general terms, the benthic population of the sea is correspondingly more diverse than the pelagic population. The seabed can provide hard surfaces for the attachment of sessile forms and plenty of hiding places for mobile animals. Sediment deposits give concealment and protection to burrowing creatures. In terms of area, by far the greater part of the ocean floor is covered in soft sediments and the major deposits are described in Section 1.3 (Seabed composition). Our knowledge of the distribution of deep-sea benthos is increasing rapidly through the use of remote cameras, baited traps and manned and unmanned submersi- bles, now capable of reaching and sampling extreme depths. The early concept that the deep ocean seabed lacked biodiversity has been disproved particularly taking bacte- ria and other microorganisms into account. However in general terms, biomass does decrease with depth as would be expected and the deeper the water and the further from land, the smaller the weight of animals on the sea bottom. There are certain exceptions to this, namely, hydrothermal vent communities (see Section 7.4.6). 7.1 Benthic communities Using the term ‘community’ to refer to populations of different species consistently occur- ring together and free to interact, it is obvious that different parts of the sea floor are pop- ulated by characteristic communities. The differences in environment accountable for the association of particular communities with particular parts of the sea bottom can be related to features of both the water and the substratum. The physical and biotic factors described in this section result in significant patchiness within benthic communities. 7.1.1 Physical factors affecting distribution of benthic communities The major hydrographic parameters which control the distribution of marine organ- isms and communities are the temperature of the water, its composition, movements, pressure and illumination and are outlined in Chapter 2. These physical parameters tend to be more constant in the deep ocean than in shallow sublittoral and seashore environments, but are nonetheless important in relation to the distribution of benthic populations, restricting certain species to particular localities.  Benthic living: sublittoral and deep seabed 321 Substratum The seabed substratum material exerts a dominant influence over the distribution of organisms on the sea floor. Where the seabed is hard and rocky and not overlain by soft deposits, the community consists chiefly of species that live on the surface of the substratum, that is, an epifauna and epiflora. Where the bottom is covered with sedi- ment, most of the inhabitants live within the deposit (infauna). Within any one area, where local conditions are relatively uniform, sediment communities will generally be less diverse than those on rock. Rocky seabeds in the upper, well-lit water levels of the sublittoral zone, are usually dominated by seaweeds and other algae which grow attached to rock, or to stones heavy enough to give secure anchorage. Large kelps (e.g. Laminaria, Macrocystis) form dense forests (see Section 7.4.1), with a variety of foliose algae growing on the rock between their holdfasts, as well as attached epiphytically to their stipes. Many foliose algae have a lower light requirement than kelp and so can form communities on rock surfaces deeper than kelp, as do encrusting calcareous red algae (e.g. Lithophyllum, Lithothamnion). This dominance of photosynthetic organisms is similar to the familiar situation on land, where rooted and attached plants dominate most communities. In contrast, rocky seabed below the photic zone is usually dominated by sessile animals, that is animals that are attached to the seabed and generally unable to move about. This is not something that occurs on land. Predominant sessile marine animal groups include cnidarians, such as hydroids, cor- als and anemones, sponges, bryozoans, barnacles, tube-living polychaete worms, brachio- pods, sea squirts and various bivalve molluscs such as mussels. Crawling and living amongst this cover of sessile animals or amongst seaweeds in shallow water is a variety of mobile animals particularly errant polychaetes, echino- derms, gastropod molluscs, crustaceans and small benthic fish such as blennies (Blenniidae). There is usually a wide diversity of species inhabiting a rocky bottom, because the irregularities of the rock surface provide a great variety of microhabitats, with innumerable differences in living space, water movement, food supply, illumina- tion and even temperature. Rocky seabeds rarely support a numerous infauna, that is animals that live within the substratum, but burrowing animals will occupy any accu- mulations of silt and sediment between rocks and in crevices. There are also a few organisms capable of boring into rock, mainly bivalve molluscs (e.g. Hiatella, Pholas, Lithophaga), a few polychaete worms (e.g. Polydora, Dodecaceria), the sponge Cliona and some barnacles and sea urchins. In some areas there are also species of red algae which bore superficially in calcareous rock. Where shell fragments and stones are available for attachment, a few seaweeds can grow in shallow sediment areas and a varied microflora of benthic diatoms and other photosynthetic microalgae occur on the surface of sand or mud, often visible to the naked eye as a thin brownish biofilm (see Section 7.3.2). However, with the excep- tion of seagrass and maerl beds (see Section 7.4.2) marine sediments are dominated by 322 Elements of Marine Ecology animal communities even in shallow well-lit water, with the animals living buried beneath and sometimes protruding from the sediment surface. Often the only clues to their existence are burrow entrances or the tops of tubes or projecting feeding appara- tus. Some such as seapens, burrowing anemones and crinoids are more obvious and communities of such animals can be spectacular. A few species, such as Horse Mussels (Modiolus), serpulid tubeworms and calcareous maerl algae live on the sediment surface and build biogenic reefs (see Section 7.4.7), their shells or skeletons providing a rock- substitute substratum for attachment of sessile animals and algae. Infaunal sediment communities commonly include burrowing sea anemones and sea- pens (Pennatulacea), polychaete worms, bivalve molluscs, sea cucumbers (Holothuroidea) and crustaceans. Some decapod crabs such as the Angular Crab (Goniplax rhomboides) live in complex, permanent burrows with various entrances and chambers. These burrows may also interconnect with those of other species and some small fish, particularly gobies, live in commensal relationships with burrowing prawns. Many species of fish, particularly flatfish and rays, live on the sediment surface but only a few burrow into it. Red band fish (Cepola) in temperate areas and Garden Eels (e.g. Gorgasia) in tropical areas live in deep burrows and form large colonies. The particle size of sediment is an important factor regulating the distribution of the infauna because the mode of burrowing of many creatures is specialized and suitable only for a certain grade of substratum (Trueman and Ansell, 1969). Particle size itself is determined by many factors including its origins, current speed and wave exposure. Deep-sea sediments are often extremely fine (see Section 1.3.2 Pelagic deposits). Burrowing can be done by forcing or digging through the sediment, push- ing the particles aside, or eating through it, or often by a combination of methods. Large particles are more difficult to displace or ingest than small ones and the mechan- ical difficulty of burrowing in coarse deposits may be one reason why these are usually less populated than finer ones. On the other hand, very fine sediment can compact into a dense, unyielding mass in which it is not easy to burrow and which requires adaptations for dealing with silt. Certain combinations of particles form thixotropic deposits which are readily reduced to a semifluid consistency by repeated, intermittent pressures and yield easily to burrowing. Where the deposit is exceptionally soft, such as occurs beneath some areas of very deep water, mobile animals would simply sink into it or be smothered by it if it were not for adaptations such as long stalks or extremely long appendages to lift the main body clear of the bottom, for example the long fins of tripod fishes (Bathypterois spp.) and the modified tube feet of Scotoplanes and other holothurians (see Section 7.4.5 Abyssal plains). Although differences between communities can often be correlated with differences of particle size of sediments, other factors are also involved. For example, many sediment- dwelling animals do not actively burrow and yet may be quite particular in their choice of sediments. The rather similar common British sea cucumbers Neopentadactyla mixta and  Benthic living: sublittoral and deep seabed 323 Thyone fuscus live in quite different sediments, Neopentadactyla in coarse gravels and Thyone in mud. Here the size of sediment particles is unlikely to be the only factor controlling their distribution. The grade of a deposit depends upon the speed of bottom current and this also controls several other features of the substratum. Slow-moving water allows organic matter to settle, resulting in a sediment that may not only be fine in texture but also rich in organic content. Poor or absent circulation of the water contained in the sedi- ment leads to deficient oxygenation of the subsurface layers and high concentrations of sulphide. Beneath shallow water these conditions often support a large biomass, because there is a good food supply for animals that feed on the surface or digest organic matter from the sediment, but the infauna must be able to cope with silt and a deoxygenated medium. Where the bottom water moves more swiftly, there is likely to be less settlement of food and a lower organic content in coarser sediments, but better oxygenation of the interstitial water. The poorer food supply supports a smaller biomass, but these conditions favour animals which can burrow in coarse material and capture floating food suspended in the water. Therefore several interrelated factors operate to limit certain species to particular substrata. Turbidity and light The intensity of sunlight reaching the seabed has a profound effect on rocky sublittoral communities, particularly in temperate and cold, nutrient-rich waters, where seaweeds and other algae flourish. Sunlight penetrating the ocean is not only absorbed by the seawater and so reduced with increasing depth, but the spectral composition also changes (see Section 2.6 Light and illumination). Thus other factors being equal, algal- dominated communities give way to animal-dominated communities at depths that vary with the clarity of the water (Table 7.1). In turbid water, light penetration can be reduced significantly because particles of suspended matter also absorb light. Turbidity is related to wave exposure, water currents and run-off from land and rivers. Water movement carries settling silt away and prevents it from accumulating and smothering the benthos. Shallow sheltered sea lochs or bays are likely to have poorer water clarity than similar, but more open areas. Around the British Isles, algal-dominated communities can extend to at least 25 m depth in the clear Atlantic waters off the west coast. At otherwise similar rocky sites, but in turbid waters such as in the Bristol Channel, algae may not extend more than a few metres down or may be totally absent. There is a record of seaweeds growing at 268 m depth on a seamount near the Bahamas (Littler et al., 1985), but most grow above 100 m or so. Within the latitudes at which they grow, tropical coral reefs are similarly restricted in distribution by turbid water, due to their requirement for sunlight (see Section 7.4.3). High turbidity may also have adverse effects on benthic animals by clogging the feeding apparatus or smothering the respiratory surfaces. Sessile benthic animals are of 324 Elements of Marine Ecology Table 7.1 Depth distribution of algal and sessile animal communities in the sublittoral zone of a typical, moderately wave exposed, rocky coastline in the British Isles. Depth below Sub-zone Community description chart datum (m) 0 8 Upper infralittoral Dense kelp forest (Laminaria hyperborea) with understorey foliose algae 8 13 Lower infralittoral Scattered kelp. With little shading from kelp, foliose and calcareous algae predominate and out-compete animal growths 13 20 Upper circalittoral Animal growths predominate; low light levels restrict foliose algae to scattered patches 20+ Lower circalittoral Animal growths; no foliose algae but calcareous encrusting algae often present to at least 50 m necessity either filter-feeders or must catch or ensnare passing prey. For example bivalve molluscs, which form a major part of many sediment communities, obtain food by drawing in a current of water, from which they filter suspended food particles and special adaptations are required to cope with the problem of separating food from large quantities of silt. Water currents and waves Benthic organisms are also influenced by the speed of the bottom current, because this controls the particle size of the substratum, its oxygenation and organic content and also affects the dispersal of pelagic larvae and the ease with which they can settle on the bot- tom. The bottom current is also vitally important in the transport of food particles, sweep- ing them away from some areas and concentrating them in others, especially in depressions in the seabed. The richest benthic communities within the sublittoral zone are often found in areas with moderate tidal water flow, such that plenty of food is carried within reach, but the current is not so strong that it damages or rips animal growths away. Moderate wave action can have a similar effect, carrying food and oxygen and resulting in rich benthic communities. However, strong wave action can be extremely destructive. Within the depths to which wave action can have an effect, both water currents and wave movements will affect benthic communities. Pressure At abyssal depths, where temperature and salinity are uniform over great areas, hydro- static pressure may well be the chief factor which accounts for differences between communities within the ocean trenches and those of other parts of the deep-sea bot- tom. There is evidence from sampling of amphipod populations in widely separated ocean trenches, that whilst abyssal zone communities were similar, deeper hadal zone  Benthic living: sublittoral and deep seabed 325 (trench) communities were completely different. Pressure, geographical isolation and overlying surface productivities may all play a part (Jamieson, 2015, section on Community structure). Sampling in the hadal zone is difficult and data, therefore, more limited than in shallower areas. 7.1.2 Biological factors affecting distribution of benthic communities Although physical factors exert a major control, as described in the preceding Section 7.1.1 there are also biological factors which influence the distribution and compo- sition of benthic communities. With the exception of bottom-living fishes, the majority of adult benthic animals are either slow-moving mobile animals, are sedentary and remain more or less immobile within or on sediment (e.g. bivalve molluscs), or are sessile and attached to hard substrata. The majority (though not all) benthic animals start life as pelagic larvae dispersed by water movements. This imposes difficulties and restrictions in finding a suitable habitat in which to settle. Once larvae settle and undergo metamorphosis, there is no going back and they die if conditions are unsuitable. Undoubtedly there are great losses, but the larvae of many species exhibit behaviour which influences dispersal and favours their chances of reaching situations where survival is possible. Many species of lar- vae have some control over the depth at which they float. Within the photic zone this is often by virtue of their response to light. Larvae of shallow-water species are usually pho- topositive for a time, collecting near the surface, while those of deeper-dwelling forms mostly prefer dim illumination or darkness and therefore occupy deeper levels. The depth at which the larvae float must obviously influence the depth at which they settle. Selective settlement of larvae The settlement of pelagic larvae of benthic species is by no means an entirely random pro- cess. Whilst larvae may initially be carried along by water movements in the same passive manner as inorganic particles on large spatial scales, it is an obvious selective advantage that once near the seabed, larvae be able to select where to settle. Considerable experimental work has been done since at least the 1950s, to find which biotic and abiotic parameters influence larval settlement and provide the necessary cues for settlement in various groups and species. Work on larval settlement in polychaetes is reviewed in depth by Qian (1999). Since benthic animals live on, attached to, or in the seabed, selection of a suitable substratum is vitally important. Selective examination of the substratum, with metamorphosis delayed as long as possible until a suitable substratum is discovered, is known from a fairly wide range of marine animals including annelids, barnacles, molluscs, bryozoans and echinoderms. Larvae usually become less discriminating with age, but although the chance of successful metamorphosis reduces as they get older, some are able to continue normal development even after extended periods of pelagic life, once they eventually find a satisfactory surface for attachment. Many different properties of the sub- stratum influence choice, including, roughness, slope, contour, chemical nature, texture 326 Elements of Marine Ecology and even colour, or at least light versus dark surfaces. The majority of rock-settling larvae so far tested from around the British Isles seem to prefer rough surfaces to smooth. Biofilms are also important and may either induce larval settlement or may actively inhibit it, both on hard substrata and in sediment. For aggregative species, such as the Honeycomb Worm Sabellaria alveolata, choosing the right substratum is particularly impor- tant, as these animals settle individually, but live as a colony. Individuals build a tube of cemented sand grains, closely joined to others and use chemosensory means to recognize conspecific tube material. Most sabellariid worms (Sabellariidae) have specific substratum requirements, whether colonial or not (Crisp, 1974; Meadows and Campbell, 1972; refer- ences in Qian, 1999). For sediment-living animals, particle size is particularly important and particle size selection has been demonstrated clearly in various burrowing polychaete worms, for example Ophelia (see Box 7.1), Protodrilus and Pygospio. In many cases the attractiveness of sediments is also associated with the presence of biofilms, which may be important as food. This is most evident in burrowers which actually swallow the substratum. Settling larvae use various senses to detect settlement cues, including sensitivity to light, touch and chemical sensitivity to aqueous diffusing substances. The latter is most typical of species which settle on organic substrata or on sediments containing a high con- tent of organic matter, for instance, the attraction of shipworm (Teredo) larvae to wood, BOX 7.1 Ophelia bicornis. A large number of studies on substratum selection have focused on rock-living animals. An early classic study of sediment type selection is that of Wilson (1956) on the larvae of the small polychaete Ophelia bicornis. This worm has a patchy distribution in various bays and estuaries around the British Isles, living in a particular type of clean, loose sand. Pelagic lar- vae are produced which are ready to metamorphose when about 5 days old. At this stage, they begin to enter the deposit. Wilson discovered that the larvae were able to distinguish between sands from different areas, preferring to complete their metamorphosis in contact with certain ‘attractive’ sand samples and avoiding contact with other sands which had a ‘repellent’ effect. When the larvae settle, they appear to explore the deposit. If the sand is of the ‘repellent’ type, they leave it and swim away, shortly settling again and repeating their exploration. This behaviour continues over a period of several days, with metamorphosis delayed until a suitable substratum is found. If the larvae find nothing suitable, they eventu- ally attempt to metamorphose none the less, but then usually die. During an early series of his experiments, the particle size of the sand seemed to be the main factor to which the lar- vae were sensitive, but further experiments with artificially constituted sands showed the importance of other factors, notably the coating of organic materials and bacteria (biofilm) on the surface of the sand grains. If sand samples were washed in hot concentrated sulphu- ric acid they became neutral, losing their attractive or repellent qualities.  Benthic living: sublittoral and deep seabed 327 spiral tube worm (Spirorbis spirorbis) larvae to the seaweed Fucus serratus and the gastropod Tritia obsoleta to mud. Animals that live as obligate associates with other animals use cues emanating from their host. For example the Christmas Tree Worm Spirobranchus giganteus lives in tubes within live coral colonies, extending its colourful feeding crown of tentacles out into the water. Larvae settle preferentially on particular coral species in response to substances emanating from the coral (Marsden et al., 1990). In rock settling acorn barna- cles, spirorbid tubeworms and S. alveolata, it has been shown that the larvae must usually first make actual contact with the shell, cuticle or cementing substance of their own or a closely related species before settlement is attempted, the stimulus for settlement being dependent on a ‘tactile chemical sense’. In some rocky shore animals, for example Semibalanus balanoides, water turbulence encourages settlement. Barnacle cyprids settle most readily from flowing water, differ- ent species preferring different water velocities; for instance, the velocity of maximum settlement for Semibalanus balanoides is higher than for Austrominius modestus. S. alveolata larvae settle best from swirling water in which sand grains are present, especially after contact is made with the cementing substance of adult tubes or recently metamor- phosed individuals (Wilson, 1968, 1970). The sponge Ophlitaspongia papilla settles pref- erentially on overhanging surfaces, where water movement is likely to be greatest. Selective settlement offers several advantages. It reduces larval losses by hindering meta- morphosis in unsuitable locations. By encouraging gregariousness it facilitates fertilization, especially cross-fertilization between hermaphrodite forms requiring internal fertilization, such as acorn barnacles. Settlement in areas where others of the species have already sur- vived ensures that conditions are likely to be congenial. It is also a form of behaviour that favours close adaptation to particular habitats, with the advantages of specialization. Conversely, although this may confer great efficiency in specific conditions, it increases the risks of extermination if the environment changes and suitable sites are lost. Competition and predation Within a particular community of organisms there will be many interactions between the individuals. For benthic communities, competition for living space is one of the determining factors influencing the local makeup of the community. The larvae of a particular species may be present in water above a particular spot, but unable to settle and grow through lack of space. Some larvae may actually avoid settling if too many of their own species are already present. Larvae can also be prevented from settling by the activities of already established adult benthic animals. Some tube-dwelling poly- chaete worms such as Hydroides elegans are known to prevent settlement of any larvae within reach of their tentacles. However, once settled, larvae can and do make the most of the space around them. After settlement many larvae exhibit some exploratory behaviour, moving about over the surface and often spacing themselves to some extent to avoid crowding. Delayed settlement is usually followed by reduced spacing 328 Elements of Marine Ecology movements. Some larvae tend to space themselves from their own species but not from others, on which they may actually settle and attach. Such behaviour reduces intraspecific, but increases interspecific competition. The relative success of different species in competing for space is also influenced by differences of breeding periods, reproductive capacities and growth rates. One species may gain advantage by early set- tlement, following a seasonal decline in numbers of the community, or a fast-growing species may oust a slower-growing competitor by overgrowing it, or by claiming an increasing proportion of a shared food source (Box 7.2). BOX 7.2 Coral competition. Competition for space can be particularly fierce on coral reefs where the stony corals them- selves, as well as other sessile organisms such as sponges, all jostle for space. Fixed firmly in place, it would seem that corals have little chance to influence the growth around them. This, however, is far from the truth. Intra and inter-competition between corals have been shown to exert a major impact on reef biodiversity and community composition (Chadwick and Morrow, 2011). Interference competition is common, whereby the settlement, growth and health of one coral can be affected by an adjacent colony. Some corals (and sponges) can produce chemicals that have a detrimental physiological effect on neighbouring coral (or other) species. Such substances are known as allelochemicals. Perhaps more dramatically, slow motion filming demonstrates the defensive capabilities of some coral colonies, particu- larly brain corals. These slow-growing and long-lived species can maintain a buffer zone around them by use of sweeper tentacles and sweeper polyps. These extra-long extensions are well-armed with stinging nematocysts and can reach out and destroy newly settled cor- als or prevent further expansion of established neighbouring colonies (Chadwick and Morrow, 2011). Human activities can disturb this natural competitive environment and lead to phase shifts in dominance of particular groups. For example ‘fish bombing’ where explo- sives are used to stun and kill fish damages stony corals and encourages regrowth of non- reef building soft corals (Wood and Dipper, 2008). Having settled close together, this brain and plate coral are competing for limited stable substra- tum. Courtesy Elizabeth Wood.  Benthic living: sublittoral and deep seabed 329 Predator prey interactions can have a significant effect on the make-up and spe- cies balance of communities. Encrusting and sessile animals are grazed by a variety of mobile invertebrates such as gastropod molluscs. For example, sea slugs (Nudibranchia) feed on hydroids, bryozoans and sponges and are often very specific in the species they will eat. Predation is a constant modifier of sessile communities, but in general, mortality is usually highest during the period following settlement while the indivi- duals are still small. Survival may depend upon the time of settlement. Thorson (1960) observed that some benthic carnivores have phases when feeding diminishes or ceases, usually in association with breeding. This passive period may last several weeks and some species which settle during this time may be able to reach a sufficient size to become relatively safe from predation before their predators start active feeding again. The composition of a community may therefore reflect coincidences between passive periods of predators and settlement periods of other species. Interrelationships The individuals of a community are, in various ways, interdependent and some organ- isms thrive only in the presence of particular associated forms. Each type of animal is dependent upon other organisms for food and the quantity and quality of food sources obviously exert a profound control over numbers and composition of communities, as already described in this section under ‘Competition and predation’. Certain organisms depend upon others to provide the substratum or habitat for them to grow on or in and these relationships may be obligate or almost so (Box 7.3). The advantages may be mutual or one-sided. For example, the barnacle Adna anglica grows only on cup corals, mainly Caryophyllia (Caryophyllia) smithii, but confers no advantage to its host. The Cloak Anemone Adamsia palliata lives only on the hermit crab Pagurus prideaux and the crab is not found without this anemone. Both partners benefit: the crab from the growing envelope of the anemone base, which means it does not need a bigger shell and the anemone from food scraps. Some animals share the burrows formed by others; for example the polychaete Lepidasthenia argus shares with another polychaete, Neoamphitrite edwardsii. The polychaete Malmgrenia lunulata may be free-living, but often shares the burrows of the polychaetes Arenicola marina, Neoamphitrite figulus and N. edwardsii, or the echinoderms Acrocnida brachiata, Leptosynapta inhaerens, Oestergrenia digitata and others. One species may even live inside another; for example, the shrimp Typton spongicola within sponges, including Desmacidon fruticosum and the barnacle Acasta spongites embeds itself in the sponge Dysidea fragilis. 7.1.3 Stability of benthic communities: spatial and temporal variability Shallow-water benthic communities show seasonal and annual fluctuations (see Section 3.4.4), but over the long term, basic community composition is usually very 330 Elements of Marine Ecology BOX 7.3 Whelk shell community. The Common Whelk Buccinum undatum is widely distributed on gravelly deposits in shallow water around the British Isles. When an individual dies, its empty shell often forms the basis for an extended mini-community. Whelk shells are the preferred choice of home for the her- mit crab Pagurus bernhardus. Shells inhabited by the crab are often colonized by one or more individuals of the anemone Calliactis parasitica, a commensal relationship by which the crab gains protection and the anemone access to food scraps and mobility. For the hydroid Hydractinia echinata, this is also its normal habitat, though both anemone and hydroid can live on rock. The barnacle Trypetesa lampas burrows exclusively into Buccinum (and Neptunea) shells inhabited by hermit crabs, just inside the shell aperture. Other normally rock-dwelling animals simply use the shell as a hard substratum, something in short supply in the sediment areas often inhabited by whelks. These include saddle oysters Anomia ephip- pium, various tubeworms such as Spirobranchus triqueter and Hydroides norvegica, the barna- cle Balanus crenatus and the sponge Suberites domuncula. The shell is also sometimes bored by the worm Polydora ciliata, which is happy in any calcium carbonate substratum. Living within the shell alongside the hermit crab there is frequently a large worm, Neanthes fucata, which feeds on fragments of food dropped by the crab and is an obligate commensal. In contrast the tiny crab Porcellana platycheles, also sometimes found in the shell, is using the shell as a substitute for its normal rock crevice or under boulder habitat. The hermit crab itself may carry parasites, for example, the isopods Pseudione spp. in the branchial chamber, Athelges paguri attached to the abdomen or occasionally in the branchial chamber and the parasitic barnacle Peltogaster paguri extruding from the abdomen. On board this whelk shell, inhabited by the hermit crab P. bernhardus and the polychaete worm N. fucata is a large C. parasitica anemone and a ‘fuzz’ of hydroid H. echinata. Courtesy Paul Naylor.  Benthic living: sublittoral and deep seabed 331 stable, so long as the environmental conditions that mould the community (such as wave action and turbidity) remain unchanging. Because every community includes a range of species each having slightly different tolerances, there is consequently an inherent capacity to adapt to minor changes of environmental conditions, by corresponding adjustments of community structure. Changes in any parameter, for example temperature and severe weather events, are likely to influence recruitment and mortality of one species differently from another, with the result that the proportion of one species increases while another declines, but does not necessarily disappear. If conditions return to normal, the balance of species responds accordingly and the overall pattern of the community remains (Buchanan et al., 1978). Any tendency for one species to increase is eventually counteracted by increasing competition and predation, so that a dynamic equilibrium is maintained and the natural balance of the community is preserved. Often short-lived and annual species show the most variation over time, whilst long-lived and slow-growing species persist long-term. Hiscock (2018) describes how rocky reef habitats he surveyed in the late 1960s at particular locations still had broadly the same assemblages of species when visited 40 years later, although some species had declined whilst others had increased. Relatively local warm and cool climate shifts over several decades can affect benthic communities through changes in the type and abundance of the plankton on which they feed. Decadal scale oscillations in climate, such as the cold and warm phases of the Atlantic Multidecadal Oscillation (AMO), may be linked to changes in species and abundance within benthic communities, but demonstrating this conclusively is difficult with the time-series of observations cur- rently available (Hiscock, 2018). Rapid, permanent or semipermanent changes of population are associated with major anthropogenic alterations of the environment. This is particularly apparent in sediment communities, where the seabed is altered significantly by trawling, dredging or waste dumping (e.g. Howell and Shelton, 1970). Changes of water circulation or temperature connected with industrial installations can also have sig- nificant effects. Changes may also follow the introduction of a new species to an area, particularly non-native species. Over very long periods, climatic or geological changes may slowly alter the environment and there are also gradual and perma- nent modifications brought about by the activities of the organisms themselves. For example, the substratum may alter through accumulations of shells or skeletons (e.g. maerl on sediment) or through the erosion of rocks and stones by the boring activities of various organisms. The composition of the water is influenced by bio- logical processes of extraction, precipitation and secretion. The continual interac- tions between habitat and community lead very gradually to changes in both and the ecosystem, which comprises both environment and population, is thus a com- posite evolving unit. 332 Elements of Marine Ecology There are numerous examples where anthropogenic changes to the environment result in a community reaching a permanent tipping point, from which it is unlikely to recover back to its previous state. This can be seen on coral reefs where destructive practices such as over-fishing or blast fishing favour the regrowth of algae rather than coral. The algae have always been there, but now have a competitive advantage and the reef enters an algal phase, which is rarely reversible. 7.2 Classification systems for marine communities Classifying and mapping seabed habitats and their associated communities are impor- tant for purposes of managing resources and for conservation and environmental man- agement. The standard, land-based classification in the UK is the National Vegetation Classification, developed in the 1970s for the statutory nature conservation agencies. Since the 1990s a similarly detailed classification for marine communities has been developed the Marine Habitat Classification for Britain and Ireland (Section 7.2.1). This was developed to provide a meaningful structure on which to base a conservation strategy for the marine environment. However, the understanding that different asso- ciations or communities of marine organisms are found in different areas subject to dif- ferent physical conditions, began as far back as the 1920s and some of this early work is described in Section 7.2.3. These early classification systems provided a useful working framework for a number of years. However, the systems concentrated on soft- bottom communities and the northeast Atlantic region. What was needed was a compre- hensive classification of benthic marine biotopes (i.e. habitats and their associated species) encompassing intertidal and sublittoral, rocky and sedimentary ecosystems. The littoral zone in Great Britain has been well studied over the years. However, it is only since the 1980s or so that we have seen a rapid increase in our knowledge of shallow rocky sublittoral ecosystems through the use of divers and standard recording formats. Hiscock (2018) provides a summary of the development and functioning of the system. 7.2.1 Marine habitat classification for Britain and Ireland The national classification of sea floor marine habitats for Britain and Ireland was developed over many years and started in 1987 with data collection for the Marine Nature Conservation Review of Great Britain (MNCR). This involved undertaking and collating a wide variety of underwater surveys and using the data to develop a standard classification. Whilst early versions, first published in 1996, were in book form, it is now maintained as an accessible website (JNCC, 2015) and has become one of the most comprehensive such systems in the world. The classification was exten- sively updated in 2004 and various sections have and are being revised to date  Benthic living: sublittoral and deep seabed 333 (Johnston et al., 2019). Central to this hierarchical system is the concept of a biotope a seabed habitat together with the community of species that lives on or in it, that is it encompasses both biotic and abiotic elements. In rocky habitats, abundant or char- acteristic sessile organisms such as sponges or algae often define the biotope clearly and can be recorded by divers or from remote photography. In sediment habitats, it may often be necessary to take samples to reveal the infauna. The system of MNCR biotopes is hierarchical with up to six levels, from the very general, for example ‘Circalittoral rock and other hard substrata’ down to very specific, for example ‘Phakellia ventilabrum and axinellid sponges on deep, wave- exposed circalittoral rock’. The system covers all known benthic habitats in the waters around the UK including littoral, sublittoral and deep-sea habitats. The sys- tem is intended to be practical and to be of use to anyone involved in descriptive surveys (Box 7.4). BOX 7.4 The marine habitat classification for a Honeycomb Worm (Sabellaria alveolata) reef. LEVEL 1. Marine LEVEL 2. Littoral sediment LEVEL 3. Littoral biogenic reefs (see Section 7.4.7) LEVEL 4. Littoral Sabellaria honeycomb worm reefs LEVEL 5. Sabellaria alveolata reefs on sand-abraded littoral rock A description of the biotope is associated with each level (except Level 1 which is obvi- ous) with the final level defining the specific biotope in detail. 334 Elements of Marine Ecology 7.2.2 European EUNIS habitat classification system The European Nature Information System (Eunis) habitat classification covers terres- trial, freshwater, artificial and marine habitats. As well as benthic habitats, the marine section also covers pelagic and marine ice-associated habitats. The marine section is fully compatible with the UK marine habitat classification described in Section 7.2.1, but due to its pan-European coverage, it is regional and includes many additional habitats not found in Great Britain. The marine habitat classification for Britain and Ireland is integrated with the EUNIS system. 7.2.3 Older classifications Pioneering studies of marine benthic communities began in the first two decades of the 20th century. In the 1920s Petersen (see references in Stephenson et al., 1971) car- ried out detailed investigations by grab samples of the larger animals (the macrofauna) of soft deposits in shallow water off the Danish coast. He found that different areas supported characteristic associations of animals and he distinguished nine communities, naming each after the most conspicuous components of the population, for example ‘Venus communities, widespread on shallow sandy bottoms on open coasts (V. striatula, Tellina fabula, Montacuta ferruginosa, often with Echinocardium cordatum)’. Note that V. striatula is now accepted as Chamelea striatula, T. fabula is Fabulina fabula, M. ferrugino- sa is Tellimya ferruginosa. Thorson (1957) observed that in middle latitudes there are certain conspicuous genera of bivalves, echinoderms, polychaetes, and so on, which occur in communities of generally similar appearance in widely separated places but represented by different species in different parts of the range. He therefore classified communities in terms of their most obvious genus rather than species, for example Macoma communities, Tellina communities, the species varying with differences in local conditions, mainly temperature and salinity. One drawback of their methods of classifying communities by identifying their most prominent genera and species, is that certain eye-catching organisms are so widely distributed as to occur in association with rather different assemblages of other species in different parts of their range. For example, C. striatula is frequently the most obvious species in sand at shallow depths in a community that includes F. fabula, Ensis ensis and Echinocardium cordatum as other conspicuous components. Chamelea striatula also occurs in deeper water with a different group of associated organisms, notably Spisula spp., Echinocardium flavescens and Spatangus purpureus. An alternative basis for classifying benthic communities is to do so in terms of physical and chemical parameters, since the distribution of species is determined closely by such parameters. Jones (1950) defined the shelf communities of the northeast  Benthic living: sublittoral and deep seabed 335 Atlantic primarily with respect to depth, substratum, temperature and salinity. His sys- tem incorporated both sediment and rock bottom communities and details can be found in Jones (1950) and summarized in previous editions of this book. Some of Thorson’s communities can be equated with these divisions. Glemarec (1973) discusses the ideas underlying such classifications, with reference to the European North Atlantic benthos. The modern system described in Section 7.2.1 drew material from these early studies as well as accumulations of survey data undertaken specifically for the project and data from a wide range of other sources. Computer technology has allowed the development of a system that can include habitats and associated communities, from the shore to the deep sea, described in terms of well-defined biotopes, combining both of these early approaches and utilizing both the physical habitat and species approaches. 7.2.4 Limitations to classifications Whatever classification system is devised and used, it will never be perfect. Although some parts of the sea floor present sharp discontinuities, for instance, an abrupt change from rock to sand, alterations of substratum from one place to another are mostly gradual. Furthermore, every species has its own particular distribution which is never identical with that of any other. Consequently, boundaries between communities are usually indefinite with intergrading along transitional zones. On almost every part of the seabed the inhabitants comprise a climax community for that particular area, stable in composition within natural, short-term fluctuations. Wherever environment changes with locality, there are corresponding adjustments in the make-up of the assemblage of species. The concept of a community is essentially an abstraction from studies of overlap- ping distributions of many species along various ecological gradients. The ease with which communities may be characterized by particular conspicuous species (some- times rather misleadingly described as ‘dominants’) is evident in marine benthos around the British Isles, but is less apparent at low latitudes where the composition of communities generally shows a greater diversity. This diversification may be a fea- ture of more mature communities, which have evolved in stable conditions over a long period, permitting the survival of species specialized for narrow ecological niches. The communities of the north-east Atlantic may be regarded as relatively immature, having evolved in fluctuating conditions since the extremes of the Pleistocene period. This favours the evolution of polymorphic populations which survive by virtue of their wide variability, with ‘dominant’ species occupying broad ecological niches. 336 Elements of Marine Ecology 7.3 Benthic food supplies As discussed in Section 3.1, the majority of primary production in the ocean is car- ried out by phytoplankton living in the epipelagic, sunlit zone. Macroalgae and sea- grasses may be very productive, but they are limited to shallow seabed where there is sufficient light for them to grow, generally no deeper than about 40 60 m. In deeper areas, the food supply for the benthic macrofauna derives, directly or indi- rectly, almost entirely from living and dead particulate matter sinking from the over- lying water. Particulate organic matter (POM) sinking through the water and reaching the sea- bed is derived from a variety of sources. In some areas there is an appreciable input of terrestrial plant material and even in very deep water, dredging has disclosed a surpris- ing quantity of this in the form of fragments of wood and leaf. Much of this may be carried into the deep ocean basins by turbidity currents (see Section 2.7.8) flowing down the continental slope. However, the nutritional value of this material to marine organisms may be less than that of marine-derived material. Over the majority of the ocean away from the coast, the greater part of the benthic food supply consists of the remains of plankton and other pelagic organisms. The movement of food particles from the surface to deeper levels is not solely a matter of passive sinking. Active transport downwards is affected by vertically migrating organ- isms, which ascend to feed at the surface and then move downwards, where they may become prey for deeper-living predators. Their faecal pellets may also be used as food by other organisms. Faecal pellets are often rich in organic matter, some of which may be material that was not digested during passage through the gut and some is bacterial proto- plasm rapidly multiplying on this organic substrate (Harding, 1974). Depending on the availability of food, the biomass (weight of living material per unit area) of the sea-bed varies from place to place. Biomass may be expressed as ‘rough weight’ of fresh material, with or without shells, or more accurately as a ‘dry weight’ of organic material obtained after the removal of shells and drying of the remaining tissue to constant weight, allowance being made for any inorganic material present in the residue, that is ash-free dry weight. Early studies such as those of Holme (1953, 1961) working in the English Channel found dry weights of between 1 g and 35 g m22. In areas of exceptional productivity, biomass dry weights as high as 100 200 g m22 occur. Bar-On et al. (2018) compiled and analysed published studies to give a global estimate of biomass distribution on Earth, using carbon mass as the unit (total dry mass is about half of carbon mass). 7.3.1 Feeding strategies There are broadly four ways in which benthic animals gather food: they filter sus- pended particles from the water, they collect food particles which settle on the surface  Benthic living: sublittoral and deep seabed 337 of the sediment, they extract organic material which has become incorporated in the deposit, or they prey upon other animals. Some can also absorb DOM directly from the surrounding water (see Section 7.3.5). These methods are not mutually exclusive and many of course take food from several sources. For example, the shrimp Crangon feeds largely on surface debris, but also preys on small animals; many crabs such as Cancer, are omnivorous, taking a wide variety of dead and live algal and animal mate- rial; the squat lobster Galathea takes large pieces of animal and algal matter and also uses the setae on its maxillipeds to filter microorganisms and debris from the bottom deposit. Particular groups of animals often use the same type of feeding mechanism, adapted to deal with a particular source of food. The majority of sessile and sedentary benthic animals, including sponges, ascidians, bryozoans and hydroids are all suspension fee- ders, collecting or drawing in and filtering out suspended organic particles. Barnacles, many bivalve molluscs, polychaete tubeworms and some holothurians (e.g. Cucumaria) also feed in this manner (Box 7.5). Accumulated food particles that have drifted down and settled on sediments are exploited by surface deposit feeders. Sedentary polychaetes such as Terebella and Amphitrite collect these with long sticky tentacles, whilst some bivalve molluscs such as Scrobicularia and Abra have long siphons that stretch out and vacuum the seabed. Some shallow-water bivalves can swap between suspension feeding and deposit feeding depending on tidal conditions. Extracting and feeding on organic matter within the sediment in the NE Atlantic are polychaetes (Arenicola), heart urchins (Spatangus, Echinocardium) and holothurians (Leptosynapta). Benthic predators include errant polychaetes (Nephtys, Glycera), many BOX 7.5 Carnivorous sponges and ascidians. Sponges and ascidians are well-known for their capacity to filter food particles from the water. This can be visibly demonstrated in a small aquarium tank. However, there are some fascinating exceptions where sessile animals, whilst unable to move around, have neverthe- less become predatory by developing the means to capture and eat live prey. This particu- larly applies in deep ocean habitats where food is in short supply. The sponge family Cladorhizidae contains a number of carnivorous species capable of feeding on small crusta- ceans such as copepods. These are trapped on large, protruding spicules and mobile cells congregate to engulf small fragments. Some sea squirts such as Octacnemus and Megalodicopia have large, lobed siphons that act as traps to ensnare small animals. In Megalodicopia two lobes can close over anything that drifts within reach, in a way reminis- cent of a Venus Flytrap, an insect-eating terrestrial plant. 338 Elements of Marine Ecology crabs, some gastropods (Natica, Scaphander, Buccinum), starfish and ophiuroids (Asterias, Amphiura) and many fish, including most of the commercially fished species. 7.3.2 Shallow sublittoral food supply Sessile benthic animals living on and within the seabed, below shallow euphotic zone waters, including most of the continental shelf, have access to regular supplies of phy- toplankton and zooplankton. The abundance of this food depends upon the rate of surface production. Seasonal changes in the quantity of phytoplankton produce fluc- tuations in the supply of food to the benthos (see Section 3.4.3). In temperate latitudes the numbers of planktonic diatoms reaching the bottom may be over a hundred times greater during the summer months than in winter and there are associated changes in the weight of benthic populations. Seaweeds grow well on rocky shores and on shal- low, sublittoral hard substrata, especially in middle latitudes and form a primary food source that supports many omnivores and herbivores and contributes quantities of organic debris to the local sediments. Rock, sediment, the surfaces of large seaweeds and in fact almost any surface in shallow, well-lit water is likely to be covered with a thin biofilm, a food resource that can be exploited by mobile grazers such as limpets, topshells and other grazing gastropod molluscs. Biofilms consist of a variable mixture of microorganisms, initially bacteria, which produce a variety of organic materials that build up into layers. This not only provides a habitat for the bacteria themselves but also a foothold for benthic diatoms and cyanobacteria. These add to the bulk of the biofilm, as do particles of organic material derived from macroalgae. This nutritious mix attracts microscopic animals such as rotifers (Rotifera) and protozoans. Spores from seaweeds settle and stick to the biofilm which gives them a better foothold than bare rock. The young stages provide additional grazing material. Biofilms are continually renewed and their composition changes as conditions change making them a really important food source. 7.3.3 Deep-sea food supply Benthic animals living in the darkness below the euphotic zone ultimately rely for food on material produced in sunlit surface waters. Some of this descends directly all the way down to within reach of the deep ocean benthos. However, in very deep water surface plankton is unlikely to reach the bottom intact, because most of it is consumed by pelagic organisms on the way down. Between the productive surface layers and the deeper parts of the ocean there is a food pyramid, with many links in the food chain and the quantity of food available to support the population at deep levels can be only a very small fraction of the surface production. The quantity of easily assimilated food reaching the sea bottom depends partly on the numbers of  Benthic living: sublittoral and deep seabed 339 mid-water organisms devouring it on the way down. Nevertheless, a considerable quantity of organic material does eventually get there. Whilst some of it can be directly ingested and digested by benthic animals, much of it consists of more indi- gestible remains such as cell walls, shells and skeletons. Further decomposition of these tough materials, including chitin, keratin, cellulose and lignin, depends upon the activities of bacteria. Bacterial communities thrive in mid-water and within the superficial layers of bottom sediment, even in the deepest water and constitute an essential link in the organic cycle. In this way, organic materials that animals cannot make use of directly, are transformed into bacterial protoplasm and in this form become assimilable by numerous animals which feed on bacteria. There is also some addition to the biomass of deep water from larval and juvenile stages, which develop nearer the surface, drawing on the more abundant food available there, before des- cending to deeper levels. DOM (see Dissolved organic matter in this section) is also important as a food source and in some places chemosynthetic bacteria provide a further source of energy. Estimates suggest that about 1% of ocean total production of carbon reaches the ocean-wide sea floor. Phytoplankton that rely entirely on photosynthesis for their energy requirements can obviously only live in the epipelagic sunlit zone. However, there are other plank- tonic organisms that have photosynthetic ability but can be found at depths well below the photosynthetic zone. Cyanobacteria and prymnesiophytes (coccolitho- phores) are examples that can surprisingly be found in quite large numbers living as deep as 4000 m. Those species living in shallow water can photosynthesize but deep- living species cannot make use of their photosynthetic capabilities. They and protozo- ans such as amoebae live saprophytically feeding on or absorbing dead material in the water column. They in turn provide a food source for the benthos, that has not had to drift all the way down from surface waters. The chemosynthetic activities (see Section 3.1.4) of bacteria at hydrothermal vent and cold seep sites are well-established, but certain abyssal sediments may also support such bacteria, provided that reduced compounds are available. Chemosynthetic bacteria are primary producers that use chemical reactions, instead of sunlight, to produce the energy needed to fix carbon and so produce biomass. Experimental work on samples of abyssal sediments that have polymetal- lic nodules suggests that the reduced inorganic metal compounds of manganese, nickel, cobalt and iron present in the nodules could provide the basis for carbon fixation via such bacteria (Das et al., 2010). Marine snow Material from surface layers such as the shed exoskeletons of zooplankton, can reach the seabed much faster than might be expected from their size and weight. This is 340 Elements of Marine Ecology because of the tendency for dead planktonic microorganisms, fragments of organic debris (e.g. discarded ‘houses’ of larvaceans) and inorganic particles to become aggre- gated, by both physical and biological processes, into larger clumps. These not only sink faster but also become microhabitats on the way down, harbouring diverse com- munities of bacteria and other microorganisms (Fowler and Knauer, 1986). These exude sticky polysaccharides which helps clump material together. Such clumps, sink- ing through the water as particles greater than 0.5 mm in size, are referred to as ‘marine snow’ (Lampitt, 1996) and this is sometimes observed to carpet the sea bottom as a layer of ‘marine fluff’. This is probably one of the main ways in which biogenic material reaches the sea-bed and such aggregated material can sink at a rate of up to 200 m per day. The protoplasmic content of this snow undoubtedly contributes signif- icantly to the food web of deeper levels, especially by enabling animals to obtain food from microorganisms which, though too small to be directly consumed individually, can be readily ingested in this aggregated state. Time-lapse photography and the use of sediment traps have shown clearly that there is seasonal deposition of marine snow linked to surface phytoplankton blooms (Lampitt, 1996). Marine snow is also an important route whereby atmospheric CO2, after solution in the sea surface and fixa- tion by photosynthesis, is rapidly transferred to deep levels and so ‘locked up’. This has obvious implications for our understanding of the interactions between atmosphere and ocean with respect to climate change and global warming (Section 9.2). Whale falls Occasionally large pieces of meat in the form of the remains of dead marine mammals and very large fish reach the deep seabed, even the great depths found on ocean abys- sal plains. Such bonanzas attract and support a population of relatively large scavengers, particularly hagfish (Myxini), grenadiers (Macrouridae), sleeper sharks (Somniosidae) and amphipod and isopod crustaceans. Normally widely dispersed, these animals home in on a carcass from quite large distances. When a whale carcass reaches the deep-sea floor below about 1000 m it is often referred to as a ‘whale fall’. Such a large, localized food resource creates its own distinctive, but temporary community (Box 7.6). The scavengers spread detritus from the carcass and this organic material is incorporated into surrounding sediments, where it provides food for smaller organisms for many months. As the bones undergo bacterial decay, sulphides are released, which can in turn be used as an energy source by chemosynthetic bacteria. Like the bacteria at hydrothermal vents, chemosynthesis then becomes the basis for a community of worms, bivalve clams and crustaceans. A large whale fall can sustain a community for many years. These communities have been filmed from submersibles that have made serendipitous finds of dead whales. Their development has also been followed by tow- ing whale carcasses, retrieved from shallow water, out into deep water, sinking them and using time-lapse photography.  Benthic living: sublittoral and deep seabed 341 BOX 7.6 Bone eaters. Osedax is a genus of polychaete worms that live and feed on bones. These small animals are the reason that even the huge bones from baleen whales can disappear, sometimes within as little as a decade. The worms have a tangled root-like lower body which penetrates the bone and dis- solves it via an acid secretion, releasing fats and proteins. Symbiotic bacteria living within the worms take up these nutrients and appear to be essential for nutrient transference, in some man- ner, to the worms. The worms themselves do not have a mouth or gut. Feathery appendages at the anterior end absorb oxygen from the water. Since the original description of the genus (Rouse et al., 2004), many more species have been discovered, feeding on a variety of marine animal bones including turtles and fish. There are currently (2020) 26 described species. Dissolved organic matter (DOM) An important source of food available to deep-sea benthic animals is DOM and the ori- gins and composition of this material are described in Section 2.2.2. The ways in which DOM can be utilized by planktonic bacteria and their role in the ‘microbial loop’ as part of the ocean food web are described in Section 3.1.2. However, it is also clear that some benthic animals can utilize DOM directly, rather than via bacteria and other microorgan- isms. Whilst some shallow-water invertebrates are known to utilize dissolved amino acids, it is in deep-sea benthic animals that uptake of DOM is best developed. Giant tubeworms such as Riftia (Siboglinidae) found around hydrothermal vents (Section 7.4.6) do not have an internal alimentary system and part of their energy requirements are thought to be met by uptake of DOM. They also utilize symbiotic chemosynthetic bacteria (see Section 3.1.4). Experimental evidence from the 1970s and 1980s suggested early on that many other marine invertebrates, though possessing feeding mechanisms which ingest solid food, are also capable of taking in amino acids, glucose and fatty acids from dilute solution by direct absorption through the epidermis (Sorokin and Wyshkwarzev, 1973; Southward and Southward, 1970, 1972; Southward et al., 1979). Southward and Southward (1982) estimated that dissolved organic carbon provides 30% of the energy required by the deep water starfish Plutonaster and the polychaete Tharyx. The invertebrates best placed to absorb DOM are those with soft bodies and a large surface area to body volume ratio, such as suspension-feeding sponges and cnidarians. Considerable quantities of DOM are also held in the interstitial water of deep-sea sediments where it is available to microorganisms, but could also be utilized by buried invertebrates. The food relationships of benthic communities, especially those in the deep sea, are complex as can be seen from Fig. 7.1, where some interconnections of the marine food web are illustrated. However, enough has been said to emphasize that bacteria and saprophytes are an extremely important source of food for the benthic animal population at all depths. The same holds true for the microbenthos, including flagel- lates, amoebae and ciliates, many of which also ingest minute particles of POM and  Erosion, drainage and Sewage Man Land organic materials from land Zooplankton Euphotic levels Plant nutrients in surface Phytoplankton layers e.g., forming grazing Small Larger absorption NO3, PO4, organic Herbivores by plants predators predators Fe, Mn, materials by Co etc photosynthesis Diurnal vertical migrations Fisheries Small Larger Sinking Leaching Herbivores predators predators Replacement of nutrients in surface by vertical mixing Direct regeneration Excretion Predation Egestion Death Sinking Sinking dead dead plants animals Deeper; levels Suspended organic fragments Plant nutrients Indirect Bacteria DOM at deep levels regeneration Pelagic saprophytes Losses by precipitation Pelagic animals of Regeneration deeper levels Sinking Sinking Insoluble Organic Suspension Predatory Digestible Protozoa and inorganic debris benthos organic and some deposit Scavengers remains of not and debris other feeding biological digestible demersal microbenthos benthos origin by animals fish Death Sea floor Bacteria Nodules etc. Permanent deposit Figure 7.1 Diagram illustrating some of the connections of the ocean food web, from surface to deep ocean. This is highly simplified and does not reflect the importance of dissolved organic mat- ter at all levels (see Fig. 3.3).  Benthic living: sublittoral and deep seabed 343 for the meiobenthos (Section 7.4.3) living between sediment grains. Bacteria comprise an appreciable part of the food of many macrobenthic suspension and surface deposit feeders. Polychaete worms and sediment-eating invertebrates digest dead and live organic material including the bacteria and protozoa it contains. 7.3.4 Meiobenthos Classical and early studies of benthic communities were mostly confined to examina- tion of the larger animals or macrobenthos. Communities are still mostly defined on this basis for the obvious reason that they are visible to the naked eye. However, ben- thic communities also contain many smaller organisms, the meiobenthos and the importance of these in terms of food supply near the base of food chains is now well understood. Numerically prominent amongst the meiofauna are nematodes and har- pacticoid copepods, but there are representatives from the large majority of marine animal phyla (Schmidt-Rhaesa, 2020). In some phyla, such as tardigrades (Tardigrada) or water-bears, all species are meiofauna. In terms of size, meiofauna are small enough to live mainly in the interstices between sand grains and such organisms are described as interstitial. Size definitions vary, but most are smaller than 0.5 mm ranging down to about 0.063 mm (500 63 µm). Smaller organisms, the microbenthos, are also present in the same habitats and include bacteria, flagellates, ciliates and amoebae and often other small organisms such as rotifers. Many meiofaunal species are permanent resi- dents whilst others are temporary, in the form of the larvae and early stages of macro- scopic burrowing or sediment-surface living animals. Most are found in sediment from the intertidal to the deep ocean and provide a vital early trophic link in the food web, between bacteria and larger organisms. Meiofauna can also be found in other habitats including on and amongst algae and sessile animals. In shallow water there is often a microflora of diatoms and coloured flagellates on the sediment surface. 7.3.5 Measuring the supply In the deep sea, the amount of particulate organic material reaching the deeper layers and the sea-bed affects the composition and biomass of animal communities. The amount and nature of the biogenic particles that rain down throughout the year can be measured using sediment traps. The traps can be moored at various depths above the sea-bed and there are various designs for use in shallow and deep water, including neutrally buoyant drifting traps. Traps deployed in deep water are moored and use a large funnel around 90 cm in diameter, to collect sufficient material. Modern traps work automatically using a rotary collector (Fig. 7.2) with up to 20 or so sampling bottles. Each bottle opens for a set time, then closes and the traps can be left in place for a year or so. The technique was first tried in deep water in 1978 and such traps, 344 Elements of Marine Ecology Wire Baffle to keep large objects out Funnel Rotating carousel Collecting tubes Acoustically operated release mechanism Weight on seabed Figure 7.2 A moored, time series deep water sediment trap. Falling material enters the cone and drops down into a collecting bottle. After a set time, the motor seals the bottle and moves the next one into position.  Benthic living: sublittoral and deep seabed 345 along with time-lapse photographic techniques were widely used in the Joint Global Ocean Flux Study carried out in the 1990s (Ducklow and Harris, 1993). 7.4 Examples of benthic communities and ecosystems 7.4.1 Temperate kelp forests In a natural and undamaged state, kelp forests are highly productive and biodiverse and are an example of an ecosystem in which the physical framework is provided by one predominant group of organisms, that is, the habitat is biologically generated. In this case, the framework is the kelp, a general name for a group of large brown sea- weeds belonging to the order Laminariales. Kelp can grow to a very large size and includes the largest of all macroalgae, Giant Kelp (Macrocystis pyrifera), which can attain heights of 30 40 m. This is the same height reached by many tropical rainfor- est trees. There are distinct similarities between the two ecosystems; kelp forms a canopy shading the seabed in the same way forest trees shade the ground and whilst trees have trunks, kelp has robust stipes (stems) providing attachment for epiphytes. Both have an understory of foliage exploited by grazing animals, but in addition the seabed beneath a kelp forest may have extensive growths of sessile animals, including colourful arrays of anemones and other cnidarians. It has been estimated that kelp forests of one sort or another are present around 25% of the world’s coastline and predominate in various temperate and boreal coastal ecosystems. The key requirements for a true kelp forest to grow are cool, nutrient- rich water and a stable rocky substratum in shallow, sunlit areas. This restricts their growth to temperate and cold water, ranging from about 5 C to 20 C, in coastal areas of both hemispheres (Fig. 7.3). Although kelp is found around some parts of the Figure 7.3 Approximate native distribution of the main forest-forming kelp genera. From Dipper, F.A., 2016. The Marine World: A Natural History of Ocean Life. Princeton University Press (Wild Nature Press), 544pp. Courtesy Marc Dando and Wild Nature Press. 346 Elements of Marine Ecology Antarctic continent, the most southerly forests fringe sub-Antarctic islands such as South Georgia. The most northerly forests occur in the Norwegian archipelago of Svalbard. Smaller areas of kelp, often called kelp beds, also occur outside the normal geographical range in warmer regions such as southern Oman. Here cold and nutrient-rich upwelling currents provide suitable conditions. Primary production within a kelp forest can be high and given ideal conditions, Giant Kelp can grow up to 60 cm a day, though most species have a much slower growth rate. The kelp itself provides a direct food source for herbivores including sea urchins and herbivorous molluscs such as limpets and chitons. However, by far the larger proportion of kelp production is consumed as detritus or utilized in the form of DOM, produced as the material breaks down. Waves and strong currents lash the fronds and the resultant debris that reaches the seabed is exploited by a wide range of small invertebrates, including amphipods, crabs and polychaete worms. In temperate areas with well-defined winter and summer seasons, some kelps are deciduous and shed their fronds yearly (see Section 3.4.4). Some of this material is inevitably washed up onto the shoreline, providing a food source for intertidal detritivores. Many nek- tonic species are drawn to kelp forests, which provide rich feeding grounds and shelter for fish, seals and cetaceans. In terms of physical habitat, the stipes of some (but not all) species have a rough texture that allows attachment of epiphytic algae, particularly red seaweeds and sessile animals such as hydroids and bryozoans. The latter two groups also grow well on the kelp fronds, which provide an elevated platform and better access to waterborne plankton. By the end of the growing season some species have such as heavy epiphytic load that their photosynthetic ability is significantly reduced. Under these conditions, deciduous species are at an advantage as they start the growing season with clean fronds. Many species of kelp have large, complex holdfasts with cracks and crevices which provide a safe home for small mobile invertebrates, such as annelid worms, molluscs and brittle stars and can even be home to small, cryptic fish. Depending on the size and structure of the holdfast, some kelp species support a higher biomass and biodiversity than others. Typical Laminaria hyperborea holdfasts in the UK support any- thing up to 70 different species of animals and many hundred individuals. Walls et al. (2016) demonstrated differences in holdfast fauna and flora between Laminaria digitata growing in the wild and suspended in kelp farms in Ireland. Kelp forests also act as spawning areas and nurseries for fish, squid and cuttlefish, including those of commer- cial species (Fig. 7.4). Although kelp forests form stable and long-term communities, they are neverthe- less vulnerable to destruction as a result of climatic change, pollution, removal of key- stone species (see Box 7.7 and Section 9.2.5) and fishery practices. As an example, kelp forests of L. hyperborea, L. digitata and Saccharina latissima used to cover large areas of rocky seabed along the coastline of the county of Sussex in the UK, but have  Benthic living: sublittoral and deep seabed 347 BOX 7.7 Keystone species. The concept of keystone species within an ecosystem was first introduced by Robert Paine, an American ecologist in the late 1960s (see Paine, 1995). He realised that certain species (or groups) can exert an influence on the ecosystem within which they live, that is out of pro- portion to their abundance or biomass. If the species is removed, for example through over- exploitation, then the ecosystem will change, sometimes dramatically and usually for the worse. The keystone species influence is often as a predator, which if removed, can have far- reaching consequences down the food chain. One of the best-known examples is the effect of over-exploitation of Sea Otters (Enhydra lutris), which were hunted nearly to extinction by the early 1900s, along the Pacific coast of North America. Sea Otters eat large numbers of Purple Sea urchins (Strongylocentrotus pur- puratus), which graze directly on the kelp and can eat right through holdfasts and stipes. Without the sea otters to keep them in check, the urchins proliferated and destroyed the kelp forests over large areas. This is undoubtedly an over-simplification, but there is little doubt as to the importance of Sea Otters to the kelp ecosystem. In the 2010s kelp forests in this region were again being destroyed by sea urchins, this time with a different cause (see Section 9.2.5). The sea urchins themselves can therefore also be considered a keystone spe- cies, one that has an effect when predatory controls on them are no longer exerted. Figure 7.4 A typical Laminaria hyperborea forest in southern England, with an undergrowth of filter-feeding soft corals Alcyonium digitatum. Ballan Wrasse (Labrus bergylta) and other fish hunt and shelter in the forest, whilst sea urchins (Echinus esculentus) graze on the kelp itself, algae and epiphytic growths. Courtesy Paul Naylor. disappeared since the 1980s. Whilst it is difficult to pinpoint any one cause, changes in fishery practise, storm damage and deterioration in water quality from sediment dump- ing are all implicated. In 2019 efforts to improve the habitat and allow the kelp to regenerate were begun, using measures such as restricting certain fishing practices. On 348 Elements of Marine Ecology a worldwide basis the Kelp Ecosystem Ecology Network is a group of marine scientists working together to assess the impacts of global change on kelp forests. 7.4.2 Seagrass beds Like kelp forests (Section 7.4.1) the seagrass ecosystem has a physical framework pro- vided by one predominant group of organisms in this case seagrasses. Dense beds or meadows of seagrass grow in sediment areas in calm, shallow water along coastlines throughout the world, with the exception of Antarctica. They are also rare within the Arctic circle. Whilst a few species form beds on the lower seashore, the majority are sublittoral and normally only extend down to 5 10 m depth. In really clear water, sparse patches can be found down to about 50 m. Seagrasses can tolerate a wide range of temperatures but are most abundant in warm tropical waters. However, seagrasses have a relatively high light requirement and water clarity is key to their success. A suitable sediment substratum is also important, but they cannot grow if there is a high sediment or nutrient load in the water, because this reduces water clarity. Seagrasses are not directly related to grasses on land, but like them, they are flow- ering plants and monocotyledons. In structural terms, the latter group have seedlings with one, rather than two initial seed leaves (called cotyledons). They are the only group of flowering plants to have adapted to the marine environment. There are around 60 species most of which are relatively small with strap-like blades up to about half a metre long. The largest species Zostera caulescens is found in the Sea of Japan and has blades up to 4 m long (Green and Short, 2003), but there are also many species with small, oval or elliptical blades of only a few centimetres. Seagrasses are extremely good at binding and stabilizing sediment because they have extensive root systems and spread horizontally by means of creeping rhizomes (Fig. 7.5). Seagrasses produce flowers and waterborne pollen and the fruits and seeds are dispersed by currents. Given the right conditions seagrasses can spread via their rhizomes and recover from physical damage from storms or human activities, but cannot persist where there is continual disturbance. New areas and gaps can also be colonised by new plants growing from seeds and fruits. Old and well-established beds such as some of the extensive Posidonia beds found in the Mediterranean are hard to replace. Destruction of such beds is reminiscent of the destruction of ancient forests on land. Some of the Mediterranean beds are calculated to have been there for hundreds if not thousands of years. During this time, a thick layer of dead material has accumulated forming a tan- gled structure called a ‘matte’ which persists and builds up below the sediment surface, where conditions are anoxic. In spite of the fact that many seagrass beds are effectively monocultures of one, or at the most a handful of species, they form a richly biodiverse ecosystem supporting  Benthic living: sublittoral and deep seabed 349 Leaf blades Longitudinal leaf veins Ligule Leaf sheath Branching roots Nodes Rhizomes Figure 7.5 Cymodocea is a typical strap-like seagrass with stems and leaves arising at intervals from a creeping rhizome. From Dipper, F.A., 2016. The Marine World: A Natural History of Ocean Life. Princeton University Press (Wild Nature Press), 544pp. Courtesy Marc Dando and Wild Nature Press. thousands of other species. The plants are highly productive and nutrients are recycled relatively efficiently, just as they are in tropical rain forests. In these terms and given their wide distribution, seagrass beds are one of the most valuable of all coastal marine habitats. Estimates of their productivity at about 1000 g dry weight m22 year21 is more than twice that of macroalgae and puts them on a par with terrestrial ecosystems such as savannah and boreal forests (Kaiser et al., 2011 who uses values from various references). The fragments and detritus produced as the leaves fray at the ends and as older leaves die is as vital a part of the food web, as are the live plants (Table 7.2). Dugongs (Dugong dugon) and to a lesser extent manatees are notable large grazers, the former almost entirely dependent on seagrass. The plants are also eaten directly by Green Turtles (Chelonia mydas), various herbivorous fish and particularly sea urchins. All these large herbivores influence the density, abundance and species composition of seagrass beds. Most invertebrate grazers feed primarily on the epiphytic algae, hydroids, bryozoans and colonial sea squirts that grow on the leaves. Seagrass detritus is con- sumed by a wide variety of sediment-dwelling invertebrates, such as polychaete 350 Elements of Marine Ecology Table 7.2 Major species and taxa dependent on seagrass for food. Live seagrass Epiphytic material Detritus Dugong Gastropod molluscs Sea cucumbers (Holothuroidea) (including sea slugs) Coastal manatees Bivalve molluscs (Trichechus spp.) Turtles especially Chelonia Amphipods Amphipods, decapod crustaceans mydas (crabs, shrimp, etc.) Rabbitfishes (Siganidae) Rabbitfishes (Siganidae) Polychaete and other worms Sea urchins, for example Lytechinus variegatus Figure 7.6 Zostera marina is the predominant sublittoral seagrass in the British Isles. In the 1930s the coverage of this species in western Europe was drastically reduced by a wasting disease, proba- bly resulting from poor coastal quality water prevailing at that time. The beds have never attained their former extent. worms, amphipods and other small crustaceans and holothurians (sea cucumbers). Particles and DOM derived from detritus provides nutrients and is eaten or absorbed by phytoplankton, algae and epizoan suspension feeders. A well-developed seagrass bed (Fig. 7.6) provides stability to sediment habitats by holding and binding the material with roots and rhizomes. Vegetation on coastal sand dunes plays a similar role. This in turn provides a stable habitat for infauna, burrowing and surface sediment-living invertebrate