3 Life on the ocean bottom.
1.1 Life at the bottom of the sea
For human beings, the bottom of the sea is one of the least accessible parts of the biosphere. It is enormous, occupying approximately 70% of the Earth's crust. Although humans cannot colonize this huge space, they exploit a large part of it, whether by fishing or by exploiting its mineral resources. This exploitation is undertaken without our having a level of knowledge comparable to what is known about terrestrial ecosystems. There are, in effect, still large gaps in our knowledge about the functioning of underwater ecosystems and even of the organisms that live there.
The diversity of the sea floor is extraordinary, as it includes well-lit zones and zones in total darkness, temperatures that range from more than 86-32[degrees]F (30-0[degrees]C), pressures that may exceed 1,000 atmospheres, totally different nutrient supplies and water movements, and hard or soft ocean bottoms. This wide range of ecological conditions is reflected in a diversity of landscapes equal to, or greater than, that of the terrestrial ecosystems on a global scale, and a diversity of phyla that is unequalled. All the organisms that live on the ocean bottom, and thus occupy the water-sediment or water-rock interface, are called benthic organisms. They and their physical medium are known as the benthos.
Primary producers: bacteria, algae, and sea grasses
The primary producers in the benthic world are mainly photosynthetic organisms, whose distribution is limited to the illuminated area near the surface. Chemoautotrophic bacteria, such as those that live associated with the vents of the ocean ridges, are the only benthic primary producers that are not photosynthetic. Although their production is of great interest as a source of food for one of the most peculiar and interesting ecosystems in the biosphere, it is irrelevant to the marine environment as a whole. Other chemoautotrophic bacteria that live in the bottom sediments obtain their reducing power from the reduced inorganic molecules present in the sediment as a result of bacterial decomposition of organic material, and as such their production is not strictly "new." Phanerogams, algae, and some photosynthetic sulfur bacteria are the typical benthic primary producers.
Marine phanerogams originated as land plants and then adapted to marine life and have had great success on ocean bottoms with sediments and also near the surface, where they have competed successfully with algae for space, because their roots fix them to the substrate and extract nutrients from it.
The highly diversified algae are the main producers in most benthic ecosystems. Green algae (chlorophytes), brown algae (phaeophytes), and red algae (rhodophytes) cover submerged rocks all over the world, wherever there is a little light for photosynthesis. Diatoms (chrysophytes) are very important in the sedimentary seafloor, while zooxanthellae (dinophytes) are of great importance to coral reefs, where they live as endosymbionts of the coral.
Cyanobacteria (formerly cyanophytes, Cyanophy-caceae, or blue-green algae) occur almost everywhere, but they are especially abundant in extreme ecological conditions, such as those in estuaries, tropical lagoons, hypersaline areas, and sites rich in nutrients.
Lastly there are the photosynthetic sulfur bacteria that are found only in sedimentary bottoms and are concentrated at the level where conditions are almost anoxic, because they use sulfuric acid as an electron donor and transform it into sulfur or into sulfate ions.
Consumers and decomposers: animals, fungi, and bacteria
Most areas of the ocean bottom are considerably deeper than the point where there is sufficient light to allow photosynthetic organisms to live. In fact, the average depth of the oceans is about 13,123 ft (4,000 m), while the photic layer penetrated by light normally does not exceed 328 ft (100 m). The remainder is in complete darkness, broken only by the bioluminescent flashes of some abyssal organisms.
This means that life below the illuminated zone depends on energy sources that are external to the system. The entry of food is always conditioned by the productive capacity of the photic zone and arrives transported by water. This material in suspension may be directly consumed by some organisms especially adapted to capturing it (suspensivores), or it may sink to the seafloor where it is used by sedimentivorous organisms or directly degraded by decomposers.
The suspensivorous trophic strategy is extremely important in the aquatic medium, although it is practically non-existent on the land environment, where the only remotely similar strategy is found in the spiders that spin webs to catch flying insects. Suspensivorous organisms form a conceptually very broad category, because it includes both filter feeders and predators. Typical filter feeders separate small particles (bacteria, particulate organic matter, phytoplankton) from the medium by filtration: characteristic examples of these feeders are sponges, sea squirts and many bivalve molluscs. Others concentrate particles in suspension by using their branchiae (polychaetes), their cirri (cirripedes) or their arms (crinoids). Others, like the beard worms (Pogonophora) have sticky tentacles that collect planktonic organisms, which are then externally digested. Predatory suspensivores, however, are colonial organisms with polyps, or zooids that capture their prey (mainly zooplankton) by tentacles or tentacular structures. Several groups of cnidarians (hydrozoans, alcyonarians, antipatharian (black) corals, corallimorpharians, zooantharians, madreporarians), and bryozoans fit into this category. One can also divide suspensivorous feeders into two categories, depending on whether the energy necessary for movement is provided by the animals themselves (active filter feeders) or by marine currents (passive ones).
Detritivorous organisms eat organic remains and are especially relevant in the benthos, as they eat the remains of benthic production, for instance, the corpses of pelagic organisms deposited on the sea bottom. Many benthic detritivorous organisms are sedimentivorous, as they ingest the sediment, assimilate the organic part, and expel the rest. This means that they make use of both the organic remains and the small animals and microorganisms living in the sediment. Most sedimentivorous organisms are polychaetes, bivalve molluscs, holothurians, echinoids, tanaidaceans, or isopods.
Benthic communities also include herbivores and carnivores. Herbivores are abundant in rocky areas nearer the surface, in the photic zone, where algae live. Algae and marine phanerogams are eaten by sea urchins, some species of fish, some gastropod and polyplacophoran molluscs, and some crustaceans. Carnivores are also abundant and prey on both the sessile and mobile fauna: They include actiniarians (sea anemones), some polychaetes, many crustaceans, gastropod and cephalopod molluscs, starfish and brittle stars, and many fish.
Finally, the decomposer organisms degrade dead organic material into inorganic compounds again (mineralization). As in terrestrial ecosystems, the decomposer organisms of the seafloor consist basically of bacteria, together with a few fungi.
1.2 Environmental factors
The characteristics of the benthic communities installed on an area of seafloor depend to a large extent on the environmental conditions. The amount of structure in a community and its complexity and functioning are imposed by a series of abiotic factors, both as regards their average values and their variation in time and space. However, the resulting community depends on the biotic interactions between different organisms that are, a priori, adapted to the environmental conditions imposed by these abiotic factors, with the modifications imposed by biogeographical restrictions.
It should be noted that in some cases the variations in environmental parameters are more important than their average values. Very often it is the variations and maximum and minimum values of temperature, light, hydrodynamism, salinity, or some other environmental factor that limit the growth of the organisms or determine the dynamics of benthic communities. Thus, for example, the average environmental conditions of temperature, light, and nutrients found in the waters off the island of Cabrera, in the western Mediterranean, and in many other areas of the central and western Mediterranean, would allow the development of coral reefs. However, the minimum winter temperatures of 57-59[degrees]F (14-15[degrees]C) lasting for at least three months prevent the growth of hermatypic corals in this area. The absence of populations of giant kelp in the Pacific to the south of the California Peninsula appears to be determined mainly by the length of the period with relatively warm and nutrient-poor waters.
The physical substrate
The physical nature of the substrate distinguishes soft or sedimentary ocean bottoms from hard or rocky ones. In general terms, soft ones are much less stable than hard ones, and this greatly conditions the type of organisms that can live there, the trophic structure, and the occupation of space. Hard seafloors are dominated by sessile organisms that grow on the substrate, covering it or using it as a support. Thus, the occupation of space extends from the substrate to the water. On soft seafloors, however, the generally mobile organisms are concentrated inside or on the upper part of the sediment; thus the sediment's physical (particle size, nature) and chemical (oxygenation, redox potential, content of organic material) characteristics have an overriding impact on the populations of organisms that establish themselves in it.
In rocky seafloors near the surface, seaweeds play an important role in compartmentalizing space and as a source of food, permitting the existence of a series of herbivores and detritivores that incorporate these nutrients into other trophic levels. In sandy seafloors not colonized by marine phanerogams nor by green (chlorophycean) algae, unicellular algae develop that play no structural role and are consumed by sediment-eaters. Rocks in deep water, however, with little or no light, are dominated by suspensivores that incorporate organic material suspended in the water into the benthos.
On the other hand, the most abundant organisms on soft seafloors with fine sediment and relatively rich in organic material are sediment feeders, while in areas with thick, relatively nutrient-poor sediments, suspensivory is the dominant trophic strategy. A soft seafloor may be converted into a hard seafloor, or one with the biotic characteristics of one, through the building activities of its organisms. This might occur by the fixation of sediment by meadows of marine phanerogams, the building of organogenic structures by the accumulation of carbonated algae that live free in sedimentary seafloor, or (at least partially) by the creation of a hard substrate by the hermatypic corals and carbonated algae of coral reefs. The opposite change may also occur, and although it may be linked to the action of organisms (for, example, the erosion caused by certain herbivorous fish in coral reefs), it is often caused by physical erosion and infilling processes.
Light is of fundamental importance in the marine benthos. The diffusion of light in water depends on its transparency, which is determined by the particles in suspension. Regardless of whether the water is clear or turbid, the reduction of light with depth is exponential, and the distribution of plants is limited to seafloor that is illuminated. In accordance with their distribution and response to light, they are divided into light loving (photophilic) or shade loving (sciaphilic) plants.
Recently, some species of seaweed have been found that are adapted to life at very low light intensity. Despite this, the possibility of autotrophic photosynthesizing life is generally limited to the surface waters, and does not usually exceed 656 ft (200 m) in tropical and subtropical seas, and 197 ft (60 m) in cold seas. The range where seaweeds dominate other benthic organisms is even more limited. So, if we bear in mind the area of the oceans and their large average depth, we can see that the area of seafloor where primary production is important is very small.
There are several implications of great importance in the trophic structure of benthic ecosystems, because the main source of energy changes from light, as in surface ecosystems, to particles, either captured by the suspensivores or deposited on the seafloor, then consumed by sedimentivores in ecosystems at great depth. Clearly, this change is gradual, so that the importance of autochthonous primary production is greatest in the first few meters and diminishes progressively with depth.
In addition to this distinction between "illuminated seafloor" and "dark seafloor," the difference in light intensity in the photic zone from one place to another is also of great importance. It is the main factor responsible for the differences observed in the species composition (especially those of seaweeds and animals with plant cell symbionts, but also those of other organisms), spatial structure, productive capacity, dynamics, and biotic relations of communities. This is shown by the different strips, or horizons, found in communities developed on rocky areas at increasing depths, or the gradient of benthic populations found on the walls of caves, mainly caused by differences in the availability of light.
Hydrodynamism is also an important factor in the marine benthos. Water movement renews the layer of water immediately adjacent to an organism and favors the uptake of carbon dioxide and nutrients by the plants and of suspended particles by sedimentivores. Excessive agitation is counterproductive, because individuals need a morphology adapted to withstand being dislodged by the force of the current. Furthermore, if intense hydrodynamism takes place in the soft seafloor or in a rocky one covered in sand, the movement and resuspension of sediment make life difficult. In fact, one of the most unfavorable locations for life is the sandy bottom just below the surface of rough coastal waters, as the high mobility of the sediment and the lack of food determine low diversity and biomass.
The surface zone is usually the most agitated, but this agitation is turbulent and diminishes exponentially with depth. This is reflected in the distribution of sea urchins or other vagile organisms that cannot withstand intense agitation. Directional tidal currents are very important and are especially intense closer to the surface, mainly in estuaries or shallow areas. Nearer the bottom, but only in certain areas, strong currents may arise due to local phenomena or geostrophic causes. These deep areas affected by currents also have clearly differentiated populations, consisting of species called rheophiles (current-lovers). Thus, for example, the bryozoans--encrusting sponges and madreporians that are generally dominant on walls at 131-295 ft (40-90 m) in depth in the central Mediterranean--are replaced by gorgonians and globulous sponges in areas subjected to strong currents.
Nutrients and organic material
Communities of benthic organisms are also strongly influenced by the availability of nutrients and organic material, which often determine their productive capacity. Thus laminarian seaweeds are restricted to cold or temperate nutrient-rich seas, and are very rare in tropical and subtropical areas, where the lack of nutrients in the water prevents their development or limits them to the richer waters of the seafloor.
The growth of seaweeds and marine phanerogams is often determined by their capacity to assimilate nutrients, and their seasonal cycle often reflects variations in the water's nutrient concentration. In fact, the maximum growth of many light-loving seaweeds in temperate seas coincides with the peak in dissolved nutrients (generally nitrates, but also phosphates) and not the peak in sunlight. The presence or absence of reef-forming corals is generally associated with water temperature, but nutrient levels are also determining factors for their growth, as shown by their absence or very limited presence in nutrient-rich tropical zones. The degree of eutrophy or oligotrophy in an area also determines its algal population, because in eutrophic situations fast-growing opportunistic seaweeds eliminate the more mature populations of larger and usually slower-growing seaweeds.
The quantity of particulate organic material in suspension in the water is a fundamental factor determining the density and types of suspensivorous organisms. Thus, the change in species, groups of organisms, and degree of cover seen when entering a submarine cave is mainly determined by the lower availability of food for the cave-dwelling fauna. We have already commented that on soft seafloors, the zones with sediments rich in organic material favor sedimentivorous organisms, while sediments with little organic material favor suspensivores.
Temperature is another important factor in the marine benthos, because it determines the geographical and vertical distribution of many species.
With respect to geographical distribution, the most classic example is the coincidence between the minimum temperature of 68[degrees]F (20[degrees]C) and the worldwide distribution of coral reefs. There are also very many species whose distribution appears to be limited by annual minimum or maximum temperatures. The geographical limits of algae are often attributed to temperature, but may also be due to nutrient levels in the water, since cold waters are usually nutrient-rich and warm waters tend to be nutrient-poor. Even so, in many species distribution is clearly limited by temperature. Many genera of algae are restricted to warm waters (for example, Halimeda, Caulerpa, Udotea, Dictyosphaeria, Turbinaria), while others are restricted to cold areas (Desmarestia, Iridaea, Laminariales). The same happens with any animal group, especially fish. The abundance and northern limit of certain fish with tropical affinities in the western Mediterranean oscillates annually, as is the case of the wrasse (Thalassoma pavo) or the painted comber (Serranus scriba).
The thermocline that forms during the summer months in all temperate seas conditions the bathymetric range of species, some of which may be prevented from growing above the thermocline, and others below it. A clear example of this is the distribution of several endemic seaweeds in the Mediterranean, such as Laminaria rodriguezii, which never appears above the summer thermocline. Other Mediterranean organisms, such as some brachiopods (Megerlia truncata, Gryphus vitreus), only live in deep water but never in submarine caves, which suggests that temperature is the limiting factor in their distribution.
The incidence of disturbances or catastrophic factors, whether natural in origin or due to human activity, is fundamental for many populations. Communities located on the continental platform are the ones most affected by these events. Conditions are much more regular below 656 ft (200 m), and the probability of these phenomena occurring is much lower. Storms, drying out, unusual periods of great turbulence or clarity of the water, or even events with a periodicity of several years, may have great effects on the benthic medium.
In the Mediterranean the dynamics of the community dominated by the alga Cystoseira mediterranea depend on the incidence of dry periods. Because these populations do not grow at a depth of more than one meter, long periods of becalmed seas and exceptionally low sea level (caused by a high pressure center) during the spring may cause the desiccation and death of its small branches with negative effects on its production, and also on that of the other species in the community.
The incidence of strong storms may greatly modify the structure of some communities, as happened in January 1988 on the coasts of California, in a storm considered the worst in 200 years. The effect on the "forests" of kelp (Macrocystis pyrifera) was dramatic, causing unprecedented mortality (almost 100%) in these perennial species. The alga Desmaresta ligulata then covered the available substrate, but the "forest" of Macrocystis gradually recovered to a comparable state within a year and a half.
Another important cause of disturbance in benthic communities may be climatic episodes such as El Nino, which have an irregular, but pluriannual, periodicity. Although its main effect is on the planktonic communities and it has very negative effects on certain commercially important pelagic fish, El Nino also affects the benthos communities by causing a major reduction in the organic material from the pelagic environment available to the benthic system. It also negatively affects the growth of coastal seaweeds (Macrocystis and other laminariales). The repercussions of this phenomenon in the 1982-1983 winter were very important for the populations of giant kelp on the coast of California, which were seriously damaged and took two years to show signs of recovery.
Salinity and sedimentation
There are other factors that affect benthic communities, such as salinity and the amount of material settling, and these are especially important in coastal environments.
Variations in salinity affect organisms living in estuaries or enclosed areas such as small saltwater lakes or tropical lagoons. Their effects on the other benthic environments are unknown, but they are surely very limited.
Sedimentation may be locally intense and affect any sessile organism by burying it or by blocking its filters in the case of suspensivores. Some organisms, such as many algae of the genera Caulerpa, Dasycladus, Halimeda and Penicillus withstand or are especially adapted to environments with high rates of sedimentation. In other environments, the lack of sedimentation may lead to erosion of the sediment, with important repercussions for both the animals living in it and for those living on its surface.
1.3 Relationships between organisms
Environmental parameters greatly affect the structure and dynamics of a community, but in the end, it is biotic interactions that determine many of the characteristics of the populations established on the seafloor. We must, however, bear in mind the different importance of biotic and abiotic factors. Thus, a sedimentary seafloor at 13,123 ft (4,000 m) with a temperature of 36[degrees]F (2[degrees]C) and in total darkness will have a benthic population totally different from a coral reef or a kelp "forest" and their structure and dynamics will reflect the different environmental characteristics of the two types of seafloor. Furthermore, these communities are not interchangeable: That is to say, neither of them could lead by succession to the other on a human or ecological time scale. A "meadow" of erect seaweed however, can change into a rocky area, with a covering formed only of encrusting corallinaceous algae, as a result of slight modifications in the behavior, predation intensity, or recruitment of sea urchins, the main herbivores in many coastal systems. Communities of erect seaweeds are interchangeable with those of rocks with corallinaceous algae and sea urchins, as it is possible for one to replace the other.
It is now accepted that abiotic factors determine the possible pool of species that can develop in a particular site and also the class of community that may establish itself. In spite of this, biotic factors may be very important in structuring benthic communities. In fact, their relative importance seems to depend on the system, so that in more structured communities biotic factors determine the final composition of the population, while in less mature communities physical factors are more important.
The biological mechanisms determining the complexity of marine ecosystems are much more diverse than the environmental factors mentioned above. In fact, they include morphological characters, growth, reproduction, dispersal ability, feeding, excretion, and the mortality of each of the species present. On the basis of these properties, species interact in different ways and, although some relations are of little or no importance, some are vital in understanding the final composition of the ecosystem.
The entry of energy and its transformation are two basic points of an ecosystem. From what we have said about trophic strategies, it can be seen that photosynthesizing, suspensivorous, and detritivorous organisms are the possible routes for the entry of energy. Suspensivorous and detritivorous organisms feed, at least partially, on material produced in the pelagic zone and incorporate it into the benthic system, while algae and other photosynthesizers produce organic material from carbon dioxide, water, light, and nutrients. Predation within the benthic system is thus centered on the material provided by these three trophic strategies and transmitted by herbivores and carnivores.
There are many references to the importance of these relations in the structure of the marine benthos, but perhaps the most instructive example is that of the kelp populations on the west coast of North America. These consist of kelp (Macrocystis, Nereocystis, Laminaria), sea urchins (genus Strongylocentrotus), and sea otters (Enhydra lutris). The sea urchins are the main consumers of the seaweed, although in normal situations they mainly eat drifting pieces of seaweed. If this source of energy is insufficient, the sea urchins eat the living seaweed and may totally devastate the kelp "forest." Sea otters and some starfish (Pycnopodia helianthoides) feed mainly on sea urchins and limit their population growth. The indiscriminate hunting of the otters in the last century and at the beginning of this one led to important changes in the distribution and structure of the kelp "forests," and the protection of the otters has helped to regenerate the populations of algae.
The importance of sea urchins and their predators as key species in infralittoral benthic communities with rocky substrates is general, and has been noted in Atlantic and Pacific kelp, as well as in coral reefs (where herbivorous fish share with sea urchins the control of algal abundance and distribution) or in Mediterranean algal communities. Thus, in many places in the Canary Islands in the Atlantic, the extraordinary abundance of the sea urchin Diadema antillarum at depths between 7-131 ft (2-40 m) prevents the growth of well-structured algal communities, except in areas with strong hydrodynamism. The reason for this extraordinary density of sea urchins in the Canary Islands is unknown, but it may be linked to overfishing of their main predators.
There are many strategies that allow benthic organisms to escape predation: cryptic coloration; mimicry; hiding in the convolutions and cracks of rocks; making shells, hard skeletons, spines or spicules; nocturnal activity; forming groups; burying themselves; rapid movement; chemical defense, and many others. The diversity of organisms that live in a benthic community is related to the diversity of defensive strategies, so the greatest complexity is found in the most stable, mature ecosystems, and the least complexity is found in communities dominated by a few species that interact strongly among themselves and with the physical environment.
Benthic organisms almost always compete for limiting resources, such as light, nutrients, food, and space. The different morphologies of seaweeds are always a compromise between adaptation to environmental factors and the need to compete successfully with other seaweeds. A tall, erect growth form, as occurs in the trees of tropical forests, is a response to competition for light. There are excellent examples of how natural selection can act this way in the laminarial seaweeds. Most genera in this order of phaeophytes such as Nereocystis, Macrocystis, and Laminaria, and many in the order Fucales (Sargassum, Cystoseira) form dense "forests" that greatly reduce the light reaching the substrate, decisively influencing the recruitment, growth, reproduction, and survival of smaller algae. The natural or experimental elimination of this seaweed cover allows the fixation and growth of a large number of species.
Competition for food is very common among benthic animals, which often exploit the same food resources. Sometimes this competition leads to species that use the same food resource having different distributions, but in other cases, both species may coexist. One of the as yet unresolved questions of marine biology is how to explain the high diversity of species that apparently use the same food resource in the same community. The answer probably lies in the fact that the food resource varies slightly and what is really lacking is more thorough knowledge of the biology of each species. Thus the high diversity of detritivores found in muddy, very deep communities seems to be due to specific differences in their ability to ingest sediment particles of different sizes. Coexistence may also be possible thanks to different responses by competing species to slight changes in environmental parameters or biotic factors.
Benthic communities are often saturated sites where species compete intensely for space. Probably one of the best examples of this saturation of space is the population of suspensivores of dimly lit vertical walls and submarine cave entrances all over the world. Sponges, cnidarians, polychaetes, bryozoans, and tunicates form a continuous multicolored cover in these environments. Their beauty does not reflect the real situation of continuous struggle to occupy and to avoid being occupied, or the harshness of the competition, from the larval stage onwards, to occupy the vacancies that occasionally arise. The weapons used by these organisms are often very subtle, but have been "perfected" by evolution, and are deadly, such as secondary metabolites that inhibit the growth of other species. The chemicals responsible for this type of chemical defense often serve also to avoid predation, which favors even more the permanence and competitiveness of the organisms that possess them. Other communities where competition for space clearly occurs include rocky areas with seaweed, meadows of marine phanerogams, coral reefs, and in general any environment where the availability of food is not limiting.
Parasitism, symbiosis, commensalism, and mutualism
As in terrestrial environments, parasitism is a very broad type of biotic interaction that potentially affects all organisms in an ecosystem. It may be caused by microorganisms or by various types of invertebrate parasites. The activities of some parasites may be of key importance in structuring communities. Returning to the example of sea urchins, it seems that the kelp forests of the western coast of North America recovered from the dominance by sea urchins when an epidemic spread through the sea urchins, after a period of unusually high temperatures.
Another example of the importance of disease in structuring communities are the changes that occurred in Caribbean coral reefs after the death in 1983 of populations of the sea urchin Diadema antillarum. Seaweed cover has decreased significantly, while coral cover has increased.
Symbiosis may also be considered as an important biotic relationship in the determination of a marine ecosystem's structural characteristics. The most relevant cases are the symbiosis between unicellular algae and some heterotrophic organisms. Corals, which have symbiotic zooxanthellae, are the typical and most important example, as this symbiosis has allowed them to colonize biotopes "reserved" for algae. Algal-animal symbiosis is not found only in coral reefs: In temperate waters there are many sponges (Ircinia, Cliona, Chondrilla) and zooantharians (Anemonia, Anthopleura) that take advantage of microscopic endosymbiotic algae to increase their production in illuminated areas and, thus, compete with seaweeds. Even more curious is the survival and productive activity of the chloroplasts of some chlorophycaceous algae (Acetabularia, Udotea, Halimeda) consumed by opisthobranch mollusks (Elysia, Bosellia) within the cells of the animal's digestive gland.
Commensalism and mutualism are very frequent in the benthos. Filter feeders like sponges, tunicates, and some bivalve mollusks always have a large number of internal commensal organisms, including such diverse groups as protoctists, amphipods, copepods, lamellibranchs, crabs, worms, and even fish. In soft seafloors, the galleries constructed by filter feeders are occupied by a large number of commensals. Other examples of mutualism are cleaner organisms, very common among fish, and the well-known association between hermit crabs (Dardanus arrossor) and some anemones (Calliactis parasitica).
Very often, as happens in the terrestrial environment, the existence of some species, generally large in size and dominant, allows the subsistence of other species or even entire communities, thanks to the microhabitats they create. The marine benthos is full of examples of this type of interaction.
The "forests" of upright seaweeds create conditions on the substrate that prevent the growth of other seaweeds that need a lot of light to grow (photophilic), but favor those that prefer low light intensity (sciaphilic). Many suspensivores are also favored, because in the absence of these large seaweeds they would be unable to compete with the small photophilic seaweed that would otherwise cover them.
The coralligen of the Mediterranean is a biogenic structure, consisting mainly of the carbonated skeletons of algae belonging to depths where light is decreasing from 2 to 0.05% of the surface intensity. The structural complexity of this environment, drilled through with holes, allows the coexistence of a very large number of species, often ones more typical of deeper areas.
On the continental edges of the North Atlantic, the fish Lopholatilus chamaeleonticeps digs holes 13 ft (4 m) wide and 10 ft (3 m) deep in the sediment, which attract a large number of crabs, fish, echinoderms, and other benthic organisms that are usually sparsely distributed over the seafloor.
As a last example of control or modification of the seafloor by the organisms that live there, we could mention the now classic explanation of the regulation of benthic populations on soft seafloors by suspensivores or sedimentivores. In general, the fine sediments of the continental platform have a high content of organic material and bacteria, and this favors sedimentivores. Their activity stirs up the sediment and this blocks the filtration mechanisms of the suspensivores and makes the fixation of their larvae difficult. However, suspensivores are abundant in thicker sediments, where there is less organic material and less for sedimentivores to eat. Because the substrate is stable, the suspensivores have no problem establishing themselves, and they prevent the establishment of sedimentivores by their continuous filtration of the water. Thus, we can see that performing certain strategies encourages their own continuity and makes possible change more difficult.
1.4 The benthic landscape
The presence of a species in a specific spot depends not only on environmental and biotic factors and interactions, but also on its geographical distribution. Speciation takes place in a specific geographical site and under more or less defined environmental conditions. This does not mean that the species can only live in these environments.
There are many vicarious species that have become so because of the historical isolation of their populations, but that live in very similar environmental conditions. This is true for many tropical and temperate species of the Atlantic and Pacific, both at the surface and at depth. These species belong to a single genus that has undergone different evolutionary radiation and speciation in the two oceans, and the species now occupy similar habitats and play similar roles in their ecosystems.
However, other species have a wide geographical distribution, and although their ecology often coincides closely, they sometimes occupy a different habitat because of the biotic interactions that are produced in different places.
Occasionally, species that have evolved in one area may adapt well to conditions in another, and if they are introduced into the latter, they may well become dominant there. This has happened with many accidental or deliberate human introductions, such as the brown seaweed Sargassum muticum, whose growth has displaced some populations of seaweed on the coasts of the Atlantic, or the expansion of the Japanese clam (Ruditapes philippinarum) at the expense of the native clams of the sandy bays of the northern Adriatic.
So the presence or absence of certain species may be for biogeographical reasons, and communities are the way they are partly because of their evolutionary history. Although the species found differ from one sea to another and from one ocean to another, the structure of communities and the processes occurring in them are always similar, provided they are affected by similar environmental factors. So a seaweed colony, a community of suspensivores on a rocky substrate, a sandy coastal seabed, or a deep muddy ocean bottom will show a different species composition in the waters off the British Isles, South Africa, the coasts of Japan, or California. Nevertheless, their trophic strategies, their types of organisms, their compartmentalization of space and the processes regulating the community, their energy flows, and population dynamics are consistent enough within each system to allow an overall explanation. On the contrary, the study of a particular case allows the extrapolation of results to similar systems in other geographical areas.
Maximum variation in environmental conditions occurs along the vertical axis. Depth, although it is not strictly an environmental factor, is associated with changes in many factors that decisively affect organisms, such as light, hydrodynamism, temperature, the occurrence of catastrophes and, to a lesser extent, nutrients and organic material. Variations in the values of these parameters cause changes in the relations between organisms, leading to changes in animals and plants with depth. At first glance, this difference appears as a change in the dominant species. The zones with different dominant species form bands, or horizons, at right angles to the bathymetric axis, called zonation. This characteristic pattern of distribution is even clearer in the intertidal zone, and is found in any zone of the biosphere subject to a strong ecological gradient.
Evidently, zonation patterns vary geographically and in accordance with biotic and abiotic parameters. Thus, different zonation is observed on the Mediterranean coast and in the British Isles, and both are different from those of the Pacific coasts of North America and Australia. Zonation also varies depending on whether the seabed is soft or hard, the exposure to the action of waves, nutrient levels, or (as an example of a biotic factor) the level of predation by sea urchins.
Unlike the situation in the well-studied intertidal zone, there are few studies of the infralittoral zone that show the real causes for a particular model of zonation. In the Gulf of Maine, in the north-west Atlantic, the rocky seafloor is dominated by two kelps (Laminaria digitata and L. saccharina) at depths between 13-26 ft (4-8 m), and by a mussel (Modiolus modiolus) at depths between 36-59 ft (11-18 m). The mussels that occasionally grow in surface water are covered by kelp and are dislodged by storms, due to the force the waves exert directly on the kelp and indirectly on the mussels. The empty spaces left by the uprooted mussels are rapidly recolonized by the kelp, not by the slower-growing mussels. The mussels cannot, therefore, dominate near the surface because they are dislodged by the storms and because the kelp are better at competing for space. On the other hand, light diminishes with depth, reducing the growth of the two Laminaria species. Below 36 ft (11 m) the light is so dim that the consumption of these phaeophytes by sea urchins (Strongylocentrotus droebachiensis) cannot be compensated for. The sea urchins are more abundant in the mussel community than among the kelp, because this is where they find more shelter from the strong hydrodynamism and from predators. Experimentally removing the sea urchins in the mussel community provokes high recruitment of kelp, and this leads to high mussel mortality as a result of dislodging. Consequently, the interaction between mussels and sea urchins facilitates their coexistence and prevents colonization by Laminaria.
This case is an excellent example of the interaction of the different factors and shows how light, hydrodynamism, temporary disturbances, herbivory, and protection from predation occur so as to produce a model of zonation. The relative complexity of the model, even though these communities are very simple, and the added complication of performing experiments underwater explains why studies like this are rare. It also shows the importance of integrating environmental factors, biotic interactions, and life and growth cycles into a model in order to understand the reasons for the distribution of species in the benthos.
Zones and levels
Different zones or levels, arranged by depth, are distinguished on the basis of the characteristics of the environments and the organisms that live in them, and are valid for any site. The first main division is between the littoral system and the deep-sea system. The littoral zone includes the floor of the continental platforms, approximately from sea level to 656 ft (200 m) depth. In seas with transparent water, autotrophic life forms are viable on the entire surface of the continental platform, but in seas with turbulent productive waters the distribution of autotrophs is less widespread. The deep-sea zone starts on the continental slope, and no photosynthesis is possible there. Apart from the populations of the hydrothermal vents of oceanic ridges, all its energy comes from material produced in the photic zone. The deep benthos is, thus, a totally heterotrophic system, whose dynamics are governed by processes taking place far above.
The littoral zone begins at the lowest limit of the tides and often finishes with the total disappearance of the seaweed. This is why it is also called the phytal zone. It is typically divided into two zones or levels, the sublittoral and the circumlittoral. Their width is conditioned by the transparency of the water and is related to the quantity of light that arrives there. On rocky seafloor the limit is governed by the dominance of photophilic (sublittoral zone) or sciaphilic seaweeds and suspensivores (circumlittoral zone). The change between infralittoral and circumlittoral is not sharp, but is usually where light has decreased to between 1 and 5% of surface levels.
The deep system is then divided into three major zones or habitats: bathyal, abyssal, and hadal. The bathyal begins where the circumlittoral finishes and basically consists of the communities of the continental slope and the areas down to about 9,843 ft (3,000 m), immediately around it. The abyssal zone occupies the centers of the oceans with depths of 9,843-19,685 ft (3,000-6,000 m). The hadal zone consists of the deepest ocean trenches. The differences between them are mainly trophic in nature, as food diminishes with depth, meaning less biomass and lower density of individuals.
Except for the zonation observed in coral reefs where corals are very important in the illuminated zone, on rocky littoral seafloor the pattern of zonation established is to some extent similar all over the world. As examples of zonation, we may comment on the littoral system on rocky substrate in three very different but well-studied areas. These are the northwest Mediterranean, the coast of French Brittany in the northeast Atlantic, and the coast of California near Monterey, in the northeast Pacific.
In the surface zone, in moderately rough areas immediately below the intertidal bands, there is a community with a limited bathymetric distribution, dominated by one or a few phaeophytes, which are only found at this level (Cystoseira mediterranea or C. stricta in the Mediterranean, Laminaria digitata and Alaraia esculenta off Brittany, and Egregia menziesii on the Monterey coast). Slightly below, the community diversifies, with the displacement of surface species and the appearance of many new plant and animal species. In the Mediterranean there is a zone dominated by other species of Cystoseira, members of the order Dictyotales (another order of phaeophytes) and by Halopteris scoparia (a phaeophyte of the order Sphacelariales). In Brittany, the relief is covered by Saccorhiza polyschides and Laminaria hyperborea, while in Monterey it is covered by spectacular kelp forests, mainly of Macrocystis pyrifera and other laminariales (Laminaria sechelli, L. farlowii, Dictyoneurum californicum, Eiseni arborea).
The lower part of the infralittoral level is very different in composition. In the Mediterranean there are a large number of species, some of which form definite facies (Codium vermilara, Dictyopteris membranacea, Cystoseira). In Brittany, Laminaria hyperborea forms sparse populations in which other smaller seaweeds can grow (Dictyota dichotoma, Dictyopteris membranacea, Cryptopleura ramosa). In Monterey Macrocystis is still present, but Nereocystis luetkeana is often the dominant species. In the lower stratum the laminarians Pterygophora californica and Costaria costata are abundant.
In the circumlittoral zone the light is failing and zonation is not as clear as in the sublittoral. Although there is a pattern of zonation, it is broken up by patches dominated by particular species. The circumlittoral level typically shows progressive displacement of seaweeds by animals. In the northwest Mediterranean, thick layers of encrusting coralline algae give rise to a most peculiar community: coralligen covered by sciaphilic seaweeds (Mesophyllum, Halimeda, Peyssonnelia) in the upper circumlittoral level, while in the lower circumlittoral level it is dominated by populations of suspensivores (gorgonians such as Paramuricia and Eunicella, red coral, and sponges). The circumlittoral level shows great diversity. On the coasts of Brittany and Monterey, the upper circumlittoral consists of mixed populations of corallinaceous algae (Mesophyllum, Lithothamnium, Lithophyllum), laminar rhodophytes (Rhodymenia, Fryeella, Phycodrys), and suspensivorous animals (sponges like Axinella, alcyonarians like Alcyonium, or Paralcyonium), but they do not form communities as complex as those in the Mediterranean. The lower circumlittoral, however, is almost totaly dominated by animals (white corals, such as Dendrophyllia, gorgonians, sponges, antipatharians or spiny corals, etc.).
In the soft seafloor, the reduction in light with depth is of little importance, as seaweeds play no structural role and bathymetric zonation is blurred or absent. The parameters that vary with depth, such as hydrodynamism or the quantity of organic material, may also vary just as much, or more, in the horizontal. Marine currents or geological history may change the characteristics of the sediment more intensely than could depth. Even so, if we suppose there is a horizontal homogeneity, depth is associated with a decrease in the average size of the grains of sediment, so that on the coninental platform there is a gradient from coarse sand to fine silt with increasing depth, often with high levels of organic material because the decrease in hydrodynamism means less is borne away. There are many different types of ocean bottom, with the unusual characteristic that, although the maximum variability of environmental conditions is arranged along the vertical axis, many different communities or zones may be found at a single location. The reasons for this zonation have been attributed to the reduction in organic material at depth, to the change in the types of sediment, and to the currents and the effect of pressure on enzyme systems. This landscape diversity is greater than that of the terrestrial environment, where the variation in environmental parameters occurs on a different scale.
2. Seaweeds that are not seaweeds, and meadows that are not meadows
2.1 Underwater meadows
Algae evolved in the sea and diversified into a relatively large number of groups, one of which, the green algae or chlorophytes, gave rise to organisms better adapted to the terrestrial environment. These in turn they gave rise to the true plants, the spermatophytes that now completely dominate the land surface.
Some terrestrial plants have secondarily adapted to living totally or partially in an aquatic medium. Some people have compared this "return to origins" with the evolution of marine mammals. The fossil record of the entry of terrestrial plants into the sea is scanty. The first fossils date back to the Cretaceous period, 100 million years ago, and indicate that this "return" occurred independently several times in several places, giving rise to a series of five or six separate evolutionary lineages. Their readaptation to aquatic life probably took place in coastal marshes or salt marshes, and there was no intermediate stage in freshwater (except, perhaps, in the case of the genus Enhalus).
This return led to a "technological overhaul" of the underwater vegetation. Colonizing the land led to anatomical and histological complexity much greater than that of the seaweeds, and some use was made of these adaptations when colonizing the sea. Some typical adaptations to terrestrial life make no sense in the marine medium (showy flowers adapted to pollinating insects, stomata to control transpiration, impermeable cuticles) and have not been maintained by marine phanerogams. However, the following adaptations to terrestrial life have acquired new purposes. Stems are transformed into subterranean organs (rhizomes) with roots that fix the plants to the sediment. The roots absorb nutrients from the interstitial waters, much richer in nutrients than the free-flowing water. Their resistant polymers may give some protection against herbivores and ensure greater persistence. Their well-developed conductive systems allow greater functional integration. The air-bearing lacunar system allows gas transport in a medium in which gas diffusion is slow and problematic.
They do not, however, appear to have been one of evolution's success stories. The marine phanerogams have colonized extensive areas, but they have done so mainly on substrates where seaweeds could not prosper: the sedimentary ocean bottoms. Thus, it cannot be considered that they have successfully competed with seaweeds, because seaweeds still dominate rocky ocean bottoms. This evolutionary lineage has diversified very little, with only a dozen genera and about sixty species, while thousands of seaweeds are known. This might be due to adaptation to a certain degree of stress, the change from wind- or insect-pollination to water-pollination or, perhaps, other agents that reduce the success of sexual reproduction.
Anyway, this field may provide important new data in the near future as a result of using new study techniques (studies of the cell nucleus, molecular genetics, etc.) and new data from the fossil record.
The genera of marine phanerogams have usually been divided into two groups: tropical ones (Halodule, Cymodocea, Syringodium, Thalassodendron, Enhalus, Thalassia, and Halophila) and temperate ones (Zostera, Phyllospadix, Heterozostera, Posidonia and Amphibolis). There are many exceptions to this scheme, as in any simplification. It puts the Mediterranean in an odd position, as one of its two main species, Cymodocea nodosa, is a species with subtropical affinities, while the other, Posidonia oceanica, is endemic to the Mediterranean. Two of the three other species found (Zostera marina and Z. nolti) have temperate affinities, while the third (Halophila stipulacea), which was recently introduced through the Suez Canal, has tropical affinities. The reasons for this floristic composition lie in the Mediterranean's biogeographical history and in its thermal characteristics, which are intermediate (in terms of water temperature in the hottest month) between temperate and tropical waters. Partly because of this intermediate biogeographical position and the plant's similarity with other species, ecosystems dominated by P. oceanica are representative examples of all marine ecosystems dominated by phanerogams, as most of the processes and structures are analogous, if not identical, to the "meadows" in other areas.
Organisms of the Posidonia meadows
Posidonia (Posidonia oceanica) is a quite large species, with strap-like leaves 0.23-0.47 in (0.6-1.2 cm) wide and 31.5 in (80 cm) long (sometimes 39.4 in [1 m]). The rhizomes are robust and, like some other species of this genus, the leaf bases (petioles) remain attached to the rhizome after the leaves are shed (abscission). The rhizomes can grow vertically (to compensate for sedimentation) or horizontally (colonizing organs), and bear more or less lignified roots. The species occupies sandy ocean bottoms (and sometimes rocky ones) between the surface and a depth of 66-131 ft (20-40 m), depending on the transparency of the water. They cannot tolerate pollution, excessive sedimentation, lack of renewal of the water, or variations from normal salinity. Their limited colonizing capacity, their rich associated community, and their persistence over time have led some authors to consider them a climax species (or community), the end of the succession beginning with beds of Cymodacea nodosa.
Within the sometimes very imposing mass of waving green leaves, light changes in color and intensity. Looking closely at the leaves, one can see the small epiphytic organisms painting the green leaves with patches of white, brown, and pink. Under the crowded mass of leaves one may see larger sessile organisms on the rhizomes, similar to those of the rocky floor, and on the sediment sea urchins rest while holothurians ceaselessly gobble the sand for its food content. A multitude of small crustaceans, mollusks, and polychaetes walk over the leaves or nibble the small epiphytes. In the interstices of the sandy bottom there
are different polychaetes and mollusks, and a whole gamut of smaller organisms (copepods, cumaceans, nematodes). Large masses of salps (Sarpa [= Boops] salpa) graze, slowly and systematically nibbling the leaves. Sea bass Dicentrarchus labrax, giltheads Sparus auratus, and other fish swim confidently in search of prey hidden in the meadow.
The meadow thus shows great diversity of organisms and habitats, in spite of its apparent uniformity. On the other hand, in addition to the species that live there permanently, there are others that do so occasionally or regularly. They go there to feed and rest, and leave to hunt, although in some cases they use the meadow as a "nursery school" for their vulnerable juvenile phases, since this favorable environment provides both food and protection. These observations are a good example of how the presence of an organism models the characteristics of its environment, allowing other organisms to adapt to the new state (or simply use it), resulting in biodiversity that is both highly complex and beautiful.
Production in Posidonia meadows
It should not be inferred that the meadow is a static entity, consisting of a support (the plant) used by other organisms. On the contrary, it is a complex functioning machine with a constant interchange of energy and materials.
These plants have a more complicated productive system than seaweeds, and one that is characterized by its clearly defined functional specialization. The photosynthetic organs (leaves) have to meet the energetic needs of the plant as a whole, and the rhizomes and roots are energy consumers (and storage organs if necessary) and absorb nutrients from the sediment. For the whole plant to be viable, its parts must show adequate functional integration, supported by an active transport system.
"Mature," fully functional leaves with high levels of chlorophyll generally synthesize more organic carbon than required for their own growth and metabolism, and the surplus can be put to several uses. It may accumulate as carbohydrates in the leaf itself, for reuse if needed to bridge the oscillations in photosynthesis over short periods of time (a few days). It may be exported, normally as sucrose, to other parts of the plant. This can, in turn, be put to multiple uses.
It is essential for the growing leaf primordia at the center of the axis, which are protected by the adult leaves from physical attack (hydrodynamism) or biological attack (herbivores) and, as a result, they do not receive any light for use in photosynthesis. Roots and rhizomes may use this sucrose for growth or respiration, and can store it as starch for long periods. It may be transported to fast-growing horizontal rhizomes to colonize empty spaces, or it may be used in the formation of new shoots that need more organic carbon than they can synthesize.
The plant is able, however, to recover some nutrients from senescent leaves and transport them to younger leaves before abscission occurs. In addition to solutes (sugars and nutrients), plants can transport the gases needed for respiration (such as oxygen to the roots and rhizomes) in a medium that is (temporarily or permanently) anoxic or hypoxic. This complex integrated mechanism allows a very high rate of production, and patterns of leaf growth that are partly independent of photosynthesis. This is shown by the fact that the leaves grow actively in winter (thanks to the starch accumulated at the end of summer), ensuring a large leaf area when optimal conditions for photosynthesis return in spring.
Furthermore, other sources of organic material are allowed or encouraged by the presence of these phanerogams. The leaves support a rich flora of epiphytic algae that, in spite of their small size, have a high rate of turnover and so make a significant contribution to the meadow's synthesis of organic materials.
The same happens to a lesser extent with the epiphytic organisms on the rhizomes. The leaves act as hydrodynamic filters, limiting the speed of the passing water, reducing its carrying capacity, and causing the sedimentation of organic and inorganic particles, thus increasing the input of organic carbon to the sediment.
The obvious destination of this organic material is paradoxically the least important, as herbivores are only represented by sea urchins, salps, leaf-eaters, and some members of the small vagile fauna (polychaetes, mollusks, and a few isopods) that essentially only feed on the epiphytic organisms. Only a small part of the phanerogams are directly consumed (generally less than 10%), although it is not known if this is due to the high concentrations of cellulose in the leaves (or other resistant polymers), chemical defenses (phenolics), or their low content of certain elements (nitrogen). Experiments have shown that herbivores prefer the older parts of the leaves, with a greater density of epiphytic organisms, which are probably easier to assimilate. The efficiency of assimilation is very low, and it is very instructive to observe the behavior of a mass of salps (Sarpa [= Boops] salpa). They nibble the leaves, leaving typical half-moon shaped marks (corresponding to their jaws), and defecate many small pellets that, when broken down, still show recognizable half-moon shaped pieces of leaf.
Unconsumed leaf material passes to the "leaf litter," after natural senescence and abscission, often speeded up by autumn storms. This leaf litter is partly exported by the movement of water; indirect calculations suggest this may account for 50% of total leaf production, although this is a reference value, and there may be very large variations due to local conditions. The part that is not exported just slowly decomposes, either abiotically (leaching, mechanical fragmentation) or biotically (autolysis, bacterial attack, fragmentation by detritivores).
Some products of this decomposition process, together with the remains of epiphytic organisms, pieces of rhizomes and other subterranean organs and root, end up in the sediment's organic substrate.
The surface of the substrate is gobbled by holothurians on a huge scale (it is estimated that every portion of sediment is consumed by a holothurian between 1-5 times a year). After assimilating a small part, they defecate it. Even so, most consumption of the sediment's organic material is by aerobic and anaerobic bacteria (denitrifiers and sulfate-reducers). These form the basis of short food-chains consisting of foraminifers and other protozoa, nematodes, polychaetes, and many other animals that live buried among the plant's subterranean structures.
The higher levels of trophic chains consist of predators (mainly fish and decapod crustaceans) that feed on members of the vagile fauna, and to a lesser extent, on the endofauna of the sediment. Finally, the least degradable part of the plant's production (the rhizomes, the petioles that remain attached after the leaves fall, and the roots) is gradually buried in the sediment, where it remains for an indefinite period (millennia).
Meadows in the littoral ecosystem
Meadows of marine phanerogams cover large areas. Thus, a recent study estimated for the Catalan coast (slightly less than 311 mi [500 km]) an area of 4,000 ha (1 hectare = 2.5 acres), equivalent to just under a third of the ocean bottom between 0-82 ft (0-25 m). Estimates of 2% of the total surface of the Mediterranean take into account the large areas covered by meadows where they are favored by shallow water (Gulf of Gabes, Tunisia). The importance of the processes described increases greatly if we consider the scale on which they occur and the noticeable effects they have on the littoral ecosystem. Some of these effects deserve special attention.
These meadows, as mentioned before, favor the sedimentation of particles that are then trapped in the mass of roots and rhizomes. In meadows closer to the surface, the leaves may act as a natural breakwater, reducing the effects of the waves and protecting beaches from erosion. An identical effect has been suggested for the accumulations of leaf litter deposited on beaches in the autumn. The interaction between the meadows and littoral sedimentological processes is thus very intense.
From the above considerations, it is clear that these meadows are genuine underwater oases. If we surveyed an area of sandy seafloor and an equivalent area of Posidonia, the meadow would show ten times as many species and a hundred times more individuals than the sandy floor. More than 1,000 species of animals and plants have been recorded in Mediterranean phanerogam meadows. The food produced (and the oxygen evolved) does not only nourish the system but also adjacent systems, because of the export mentioned above. Large areas of seabed at more than 328 ft (100 m) have been observed to be covered by these plants, and similar remains have been found at more than 3,281 ft (1,000 m). The meadow buries a lot of carbon, nitrogen, and phosphorus in the rhizomes and associated organs. The epiphytic organisms produce abundant calcium carbonate, which may contain coprecipitated phosphorus. Significant denitrification takes place in the sediment, and in the leaf litter or humus. To sum up, the Posidonia meadow withdraws elements from circulation, that, in excess, are or may be prejudicial to the environment (nutrients: coastal eutrophication) or even for the whole biosphere (carbon dioxide: greenhouse effect).
2.2 Kelp "forests"
All over the world most rocks in the infralittoral habitat are populated by seaweeds. Coral reefs are the only places where this does not occur, but even here there are places where seaweeds dominate corals. Seaweed communities vary greatly in appearance with geographical location, depth, and other environmental factors. The greatest complexity is found in kelp, large brown seaweeds that form "forests" in cold and temperate seas throughout the world.
Kelp consist of a more or less irregular, ramified basal disc (the holdfast) that is strongly fixed to the rock and produces one or more stipes of variable length, with one or many phylloids or "leaves" distributed along the stipe or at its top. Their size varies greatly, from less than 3 ft (1 m) to more than 131 ft (40 m). The most important forest-forming genera are Laminaria (in the Atlantic and north Pacific), Macrocystis (southern hemisphere and eastern Pacific), and Ecklonia (southern hemisphere and western Pacific).
Biomass and production
Macrocystis pyrifera forms the most spectacular forests, as their enormous rhizoidal bases produce a large number of stipes, each up to 164 ft (50 m) long. The 3 ft (1 m) long phylloids (leaves) are distributed along the stipes and have an air bladder, or pneumatophore, that helps them to float. The surface of the water is full of floating phylloids, and below them is a genuine forest formed by their stipes and other smaller seaweeds. The forests of Laminaria and Ecklonia are less spectacular, as the stipes are much shorter. L. hyperborea, the main species forming these forests on the European coastline, has only one stipe per plant. It is 3-7 ft (1-2 m) long and produces a large palmate phylloid, similar in size to the stipe.
The density of these populations is very variable, given that it depends on the size of the plants. The mature forests of Macrocystis pyrifera in coastal California have an average density of 0.5 plants per square meter, while Laminaria forests often have 10-15 plants per square meter. The biomass is much more constant, and is generally between 22-66 lb (10-30 kg) fresh weight per square meter.
The kelps' growth is seasonal: They grow at the time of year when nutrient concentrations in the water are highest. Thus, Laminaria hyperborea, on the European coasts of the Atlantic, only grows between February and June. L. longicruris, on the Atlantic coast of Canada, shows a growth maximum in the spring, but maintains limited growth throughout the year. Finally, Macrocystis pyrifera, on the coasts of California, grows in the spring and summer, using the nutrient-rich waters of the summer upwelling. The importance of nutrients for kelp growth is clearly shown by the fact that maximum development often begins in midwinter, when nutrient concentrations are greatest but the light reaching the plants is insufficient. Winter growth occurs thanks to the translocation of stored reserves in the stipe and old phylloids during the previous summer. The plants also use this period to store nutrients that will be used to continue growth at the end of the spring, when nutrients are lacking but light levels are best.
The increase in length of the phylloids during the maximum growth period is between 0.08-1.2 in (0.2-3 cm) a day in species of Laminaria that grow in the infralittoral, while Macrocystis pyrifera can grow up to 20 in (50 cm) a day in optimal conditions on the coastline of California. Production in kelp forests is 0.9-4 lb (0.4-2 kg) of carbon per square meter per year, making them some of the most productive communities in the biosphere. This is about one order of magnitude greater than phytoplankton production in the same areas and makes kelp forests the main energy source on which coastal trophic webs are based.
Structure and stratification
Apart from their importance as an energy source, kelp forests are fundamental to the littoral system as a habitat for many species of plants and animals. We can make a structural division of the kelp community into various strata. The most complex communities show up to six strata.
By analogy with a terrestrial forest, we can call these six strata: an upper "arboreal" layer consisting of large seaweeds (Macrocystis, Nereocystis) whose "canopy" floats on the water; a lower "arboreal" layer, consisting of smaller species of kelp (Laminaria, Eisenia, Pterygophora); a "shrub" layer, consisting of large phaeophytes (Cystoseira, Desmarestia, Chorda); a "herbaceous" layer consisting or organisms from 4-12 in (10-30 cm) in height, including some small seaweeds (Delesseria, Gigartina), hydroids (Nemertesia), sponges (Axinella), and gorgonians; organisms from 1-4 in (3-10 cm) in height, such as small seaweeds (Corallina, Calliarthon, Rhodymenia) and hydroids (Aglaophenia); a "moss" layer from 0.4-1 in (1-3 cm) in height, including filamentous algae (Ceramiales, Ectocarpales), erect bryozoans, anemones, and scleractinians; and an encrusting stratum consisting of algae, sponges, bryozoans, and sea squirts that grow on the substrate itself. Growing on all of these six strata are epibionts, organisms that live on others, which include representatives of all the main groups of benthic organisms.
Apart from these categories of plants and animals, there are mobile or dispersed organisms that are distributed differently. In a Pacific kelp forest, sea otters (Enhydra lutris) live in the canopy of the Macrocystis and forage in the lower layers, the preferred habitat of minuscule transparent shrimps (Acanthomysis) and a fish (Heterostichus rostratus). The stipes are colonized by different species of small herbivorous snails (Tegula, Calliostoma) escaping from their main predators (sea urchins and crabs). Many fish swim among the stipes, including damsel fish (Chromis punctipinnis), anchovies (Engraulis mordax), rockfish (Sebastes), garibaldis (Hypsypops rubicundus), and saurels (Trachurus symmetricus). Seals (Phoca vitulina) and Californian sea-lions (Zalophus californianus) also make incursions in search of food. On the seafloor there are many crabs (Cancer, Loxorhyncus), starfish (Pisaster, Patiria, Pycnopodia, Solaster), sea urchins (Strongylocentrotus), holothurians (Parastichopus, Cucumaria), and abalones (Haliotis). In other communities of forest-forming kelp, despite different mobile species, the large groups of organisms maintain the same type of distribution.
The seasonality of kelp growth already mentioned is not unique and, as happens in temperate terrestrial forests, is reflected in the entire community. One can distinguish two stages joined by two clearly differentiated phases. Spring growth coincides with the production phase and is when many annual species germinate, including both seaweeds and small epiphytic animals. By the middle of the summer it has attained the state of a developed community characterized by its maximum biomass and cover, and by its complex spatial structure. During the autumn there is a phase of diversification, dominated by the consumption and decomposition of the organic material produced during spring and summer, which ends with the arrival of storms that eliminate or drastically reduce many of the populations. The most diverse community stage occurs at the beginning of winter, with minimum biomass and cover, as well as great structural simplification. This seasonality is obviously determined by seasonal changes in the environmental factors that affect the metabolism of seaweeds and animals: The main factors are light, nutrients, temperature, hydrodynamism, and major disturbances.
Stability and persistence
The stability or persistence of seaweed communities has been the subject of many studies and heated discussions among those studying the subject. We have already commented on the importance of disturbances and some biological interactions as determinants of the persistence of kelp forests and seaweed communities in general. Kelp forests disappear as a result of storms or through the effects of sea urchins feeding on them. In practice, there is coexistence of seafloors dominated by sea urchins or by kelp, and their relative areas vary, depending on the occurrence of storms, predation intensity, disease in sea urchins, and the seaweed's recruitment capacity.
3. Hard and soft seafloors
3.1 Communities of suspensivores on rocky substrates
Except for some mollusk filter feeders, which we shall not discuss, suspensivore communities on rocky substrates live in the depths. Because they are often at (or below) the limit of safe and effective work with a scuba diving suit and cannot be sampled by dredging, these populations have been little studied. The descriptions available are either the result of visual inventories taken underwater or ones performed by submarines or remote-controlled vehicles. There are biomass data for some communities at limited depth (caves) or in seas that favor underwater working (Mediterranean), and the first results are being obtained for the growth of some species. Thus there is a huge difference in knowledge about communities dominated by algae and those dominated by suspensivores.
Structure and stratification
As in algal communities, the structure of communities dominated by suspensivores is variable, but in the most complex cases several strata can be distinguished. The upper stratum consists of upright forms that grow mainly vertically, such as octocorallians (alcyonarians, stoloniferans, and gorgonians), antipatharian corals, some zooantharids and madrepores, and some arborescent sponges. The intermediate stratum includes globular bryozoans, sponges, sea squirts, hydrozoans, and tubiculous polychaetes. The basal stratum contains many sponges, madrepores, bryozoans, sea squirts, polychaetes, and hydrozoans. The encrusting stratum is also important, and consists mainly of sponges and bryozoans, and occasionally some seaweeds. The perforating endolithic stratum is very important in some cases and consists of some sponges, polychaetes, and bivalves. Epibionts grow on any other organism in any stratum, and include members of several animal groups. In fact, the skeletons of dead organisms serve as a new substrate for the juveniles of all the species that make up the community. A rich mobile fauna (polychaetes, mollusks, crustaceans, sea spiders, echinoderms, and fish) find food and shelter in these environments.
The density of organisms and the biomass of the populations is proportional to the availability of food. This depends on the quantity of food and the hydrodynamism. There is therefore a gradient in the abundance of organisms from the communities nearest the coast to those furthest away, from the areas affected by upwellings to more oligotrophic environments, or from the exterior to the interior of a cave. In the richest communities, the space is totally occupied and acts as a limiting factor. In the poorest ones there are empty spaces, but food availability limits biomass.
In these communities the growth of the dominant organisms is very slow, and the greater the depth at which they live, the more slowly they grow. For example, the Mediterranean gorgonian Paramuricea clavata grows about 4-6 in (10-15 cm) a year on walls between 66-197 ft (20-60 m) in depth, but the red coral (Corallium rubrum) present in the Mediterranean at greater depths 164-656 ft (50- 200 m) does not grow more than 0.2 in (5 mm) in height in a year. White corals Madrepora oculata and Lophelia pertusa, on bathyal 656-6,562 ft (200-2,000 m) rocks in the Atlantic and Mediterranean, grow about 0.004 in (0.1 mm) a year.
Cycles and disturbances
Communities dominated by suspensivores are much less seasonal than seaweed communities, and in fact seasonal changes disappear below a certain depth, where these changes in environmental factors are reduced to almost nil. Even so, many short-lived species (some hydrozoans, polychaetes, and bryozoans) may show very notable seasonal changes in their populations, showing greatest development in the period of the year when most food is available. In larger organisms, metabolic activity and reproduction may vary seasonally, as in Paramuricea clavata in the northwest Mediterranean, which reproduces at the first full moon in June.
As physical factors are relatively constant and disturbances are rare or non-existent, it is obvious that in suspensivore communities biotic interactions are very important in structuring the community. Increasing biomass is so difficult in these environments that most organism have mechanisms to avoid depredation, e.g., hard skeletons, spicules, and chemical defenses. Moreover, since in many groups capturing food in suspension depends on the surface of the organism in contact with the water, any morphological or chemical strategy to avoid being covered is important. In general, colonial life-forms (cnidarians, bryozoans, some sea squirts) or modular life-forms (sponges) are more competitive than solitary organisms, since they occupy space more efficiently and have more resources to escape predation and being covered.
There are no studies of the persistence of suspensivorous communities, but the general impression is that they are very stable. The data obtained for the growth of some of these organisms confirm this impression, as adult colonies of Paramuricea clavata and Corallium rubrum of coral-bearing Mediterranean walls must be 25 to 50 years old. The slow recovery of red coral populations in the reserves created in several places in the Mediterranean also strengthens the hypothesis that strong natural disturbances are absent in these populations and that they are very stable.
All over the world there are examples of communities dominated by suspensivores, even in areas with coral reefs where they occupy the zone of the reef called the "twilight zone," in which corals with zooxanthellae symbionts do not obtain enough light to lead an autotrophic life. Nearer the surface they share space with some species of seaweed adapted to life in low light intensities (such as Corallinaceae, other cryptonemialians such as Peyssonnelia, or some Chlorophyceae such as Halimeda), but at deeper levels the communities are exclusively dominated by suspensivores.
Mediterranean coralligen, in its most shady aspects, is a good example of a suspensivore community, especially the facies dominated by the gorgonian Paramuricea clavata. It is probably also the suspensivore community most visited by scuba divers and most studied by scientists. Its biomass reaches 1 lb (500 g) organic material per square meter 11-22 lb (5-10 kg) fresh weight per square meter. The main organisms, both in terms of cover and biomass, are anthozoans (Paramuricea, Parazoanthus, Leptopsammia) and sponges (Chondrosia, Petrosia, Axinella). Bryozoans (Pentapora, Schizomavella, Porella) and corallinaceous algae follow them in importance, and in lesser numbers there are hydrozoans, polychaetes, mollusks, sea squirts, and crustaceans. The groups with the highest diversity of species are, in this order, bryozoans, mollusks, polychaetes, crustaceans, and sponges.
Yellow coral communities are found on the Atlantic coastline, always below 180-197 ft (55-60 m) in depth. On the coasts of Europe coral populations are dominated by yellow coral (Dendrophyllia cornigera), black corals (Antipathes, Parantipathes), the gorgonian Swiftia rosea, several sponges (Axinella, Phakellia, Reniera), and some hydrozoans (Thecocarpus), bryozoans (Porella), and brachiopods (Gryphus, Terebratulina). In the Mediterranean this community is poorer than in the Atlantic Ocean, and is always found in deeper waters 328-820 ft (100-250 m). On the coast of Africa, and especially off the Canary Islands, the community has a bathymetric distribution similar to that in the Mediterranean, although between 197-394 ft (60-120 m) depth there is a similar structural base, in which the dominant upright species are red madrepore Dendropyhyllia ramea, the black coral Antipathes wollastoni, and the zooantharian Gerardia savaglia.
Submerged caves walls all over the world are also dominated by suspensivores. Caves are interesting because within a few meters there is a very marked change in environmental parameters (light, circulation of water, fragmented organic material) that in a way reproduces on a very small scale the changes occurring with increasing depth. The distribution of organisms within a cave reflects this very steep physical gradient, so that from the exterior to the interior there is a change in the colonizing species and a decrease in numbers, cover, and biomass. The animals are structurally simpler than those found in the open sea. Large gorgonians, black corals, and madrepores are absent, and the dominant organisms are sponges, bryozoans, solitary madrepores, and polychaetes.
3.2 Soft-floor platform communities
This name is applied to a great variety of ocean bottoms that have no more in common than their position in the littoral system at between 0-656 ft (0- 200 m) in depth. Although there is usually zonation, it is often blurred by the existence of other factors unrelated to depth, but of great importance in the soft seafloor. The type of sediment is determined by the hydrodynamism and by the characteristics of the mother rock, and thus need not be linked to depth. The sediment's content of organic material varies more with hydrodynamism (exposed areas or protected areas) or the proximity of estuaries, rather than with the distance from the coast. Changes in the characteristics of the sediment modify the vertical profile of different chemical parameters (oxygenation, reduction-oxidation [redox] potential) that are of basic importance to the distribution of organisms. In this sense, it is especially instructive to observe the changes in community structure (sediment space occupied by macrofauna, diversity, strategies) over a pollution gradient.
Structure and organization
Although environmental parameters are important in the distribution of organisms in the sediment, the animals themselves modify the sediment's physical and chemical characteristics, creating heterogeneity on a scale comparable to their size. Their mobility, feeding, constructive activities, and excrement modify sediment in an overall process that is known as biodisturbance. There are several classic examples of the biological alteration of sediments. Some sedimentivorous amphipods (Ampelisca, Haploops) build tubes by agglomerating and cementing the sediment, and so if they are abundant they stabilize the substrate and facilitate the establishment of suspensivores because their feeding increases the proportion of fine particles on the surface of the sediment. Excavating organisms, such as the bivalve (Scrobicularia plana) or the holothurian (Molpadia oolitica) are very important as oxygenators of the sediment, as they encourage the remineralization of organic material by aerobic bacteria.
Surface sediments contain microalgae, cyanobacteria, and photosynthetic sulfur bacteria, whose distribution is concentrated in the uppermost millimeters of sediment. The concentration of chlorophyll in this fraction of microbiota does not exceed 100 mg m-2 and is often lower, but this still represents a significant oxygen input to the surface layers.
Apart from the modification of the characteristics of the sediment provoked by the life of its organisms, other biotic relations greatly affect community structure. We have already seen the importance of suspensivores in preventing the fixation of the larval forms of sedimentivores, and how sedimentivores modify the texture of the sediment and make life difficult for suspensivores. Predation may also be very important. Ophiuridea (brittle-stars) of the genus Amphiura, either carnivores or facultative sedimentivores, can reach densities of 400-500 per square meter and this exercises brutal predation pressure on the recently attached larvae of bivalves and polychaetes. Recruitment to these populations would be practically impossible if the brittle stars did not become practically inactive during the reproductive period. On the other hand, sedimentivorous organisms may be very important as predators of juvenile forms. Thus, sand-dollars (Echinocardium) "swallow" sediment continuously, so that if on average there are 20 individuals per square meter which process 13 lb (6 kg) of sediment per month, this represents the ingestion of 600-700 larvae of bivalves per month.
Ecological strategies and seasonal cycles
The non-productive fraction of the microbiota ("microfauna") consists of bacteria, diatoms, flagellates, and ciliates (3-328 ft [1-100 m]); the meiofauna (328-3,281 ft [100-1,000 m]) is rich in foraminifers, nematodes, turbellarians, gastrotrichans, cumaceans, copepods, and the juvenile phases of macro-invertebrates. The macrofauna (greater than 3,281 ft [1,000 m]) consists mainly of mollusks, polychaetes, crustaceans, and echinoderms. All the trophic strategies, from suspensivory and detritivory to carnivory, are present in each size category. All systems for classifying platform communities only take the macrofauna into account, but it should be remembered that the other two categories usually have a similar or greater number of species on muddy ocean bottoms, and that their biomass may be greater than that of the macrofauna.
The biomass of the macrofauna is very variable and mainly depends on the quantity of food. The available data give ranges from 0.4-18 oz (10-500 g) fresh weight per square meter. Growth is also very variable, as it depends on the life cycle of each species and its efficiency. Furthermore, organisms often modify their growth according to the availability of food.
Seasonality can be very important, mainly in populations in surface waters. At high latitudes, population density and biomass vary over the year, increasing in the summer and decreasing in the winter. Generally, the reason for these cycles is larval recruitment, which normally occurs during the summer. In cold seas most species reproduce and recruit once a year, with a high production of larvae. In temperate and subtropical seas there are often two recruitments a year. In any case, the mortality of juvenile individuals is caused by environmental changes (whether catastrophic or not), predation, and competition. The recruitment of different species of a community is displaced in time and its success depends on many factors and varies greatly from one species to another.
This is why the relative abundance of individuals of different species varies from year to year, and there may even be changes in the dominance of species over periods of 6-7 years, or periods of 20-30 years, reminiscent of the cycles of dominance of seaweeds and sea urchins discussed in the section on biotic interactions. These fluctuations seem to be related to variable recruitment, and the factors causing this variability form one of the main obstacles to understanding these fluctuations. Sometimes they are due to strong disturbances and unusually high or low temperatures.
Some case studies
It is difficult to make a general classification of the sediment communities of the platform, due to the many factors causing heterogeneity in sedimentary ocean bottoms and due to differences in fauna caused by the geographical distribution of organisms. Even so, there are approximations that reflect reality quite well, such as the one for the straits separating the Baltic Sea from the North Sea.
Six main communities have been distinguished: the community of the surface estuarine waters, with cockles (Cardium), other bivalves (Macoma, Mya), and the polychaetes commonly known as sandworms (Arenicola marina), although shrimp (Leander) and common shrimp (Crangon) may also be common; the coarse sands community, with tellins and wedge shells (Tellina, Donax) between 0-33 ft (0-10 m) near beaches; the fine sand community, with venus (Venus), starfish (Astropecten), and heart urchins (Echinocardium, Spatangus) between 23-131 ft (7-40 m); the muddy sand community, with several bivalves (Abra, Cultellus, Corbula, Nucula), sand-dollars (Echinocardium), and polychaetes (Pectinaria, Nephthys) between 16-98 ft (5-30 m); the mud community with brittle-stars (Amphiura), gastropods of the genus Turritella, bivalves of the genera Thyasira and Nucula, polychaetes of the genera Nephthys, Terebellides and Lumbrinereis, tusk shells (scaphopods of the genus Dentalium), and several sand-dollars between 49-328 ft (15-100 m); the mud and silt community, between 328-984 ft (100-300 m), with many polychaetes (Maldane and Terebellides are the most characteristic), the brittle-stars Ophiura sarsi, the sea urchins Echinocardium, and Brissopsis, and several mollusks; the community of the estuarine waters with tube-building amphipods (Haploops), brittle-stars (Ophiura), polychaetes (Aphrodite, Eumania), and scallops of the genus Chlamys.
It should be noted that structurally and trophically similar communities, consisting of different species and genera, have been found in arctic and boreal seas.
3.3 The communities of the deep soft seafloor
The bathyal level, the abyssal plains, and the great oceanic trenches represent more than 80% of the ocean bottom, and thus more than half of the surface of planet Earth. The communities that develop there are the most extensive in the biosphere (if we exclude those of the pelagic medium), and those that have been least affected by human beings. The great distance separating them from the surface, the enormous hydrostatic pressure, and the lack of light have made study extremely difficult, and it is only since the 1960s that references to ocean bottoms have begun to appear regularly. Russian and American research submarines, such as the celebrated Alvin--owned by the renowned North American Woods Hole Oceanographic Institution--have considerably increased knowledge of these ocean bottoms, although we can affirm that almost everything is yet to be discovered.
Environmental conditions at depth
Deep ocean bottoms are mostly made of mud and silt, except some rocky outcrops that stand out from the continental slope and the oceanic ridges. The newest areas of the seafloor are, in fact, closest to these ocean ridges, while the oldest ones are located on the slope and next to the edge of the continent. This is why the archaic fauna (living fossils) live at intermediate depths, while the fauna of the great depths is relatively recent, certainly later than the Tertiary period. Even so, the level of endemism in the deep basins is very high, as the genetic flow between the populations in separate basins is very low or completely nonexistent.
Ocean bottoms, except for the vent communities of ocean ridges, are totally heterotrophic and depend entirely on the supply of organic material from the surface layers. However, the organic content of the sediments is low, except in areas of upwelling with high biological production in the surface layer. The cause of this poverty in organic material is that most of the production in the photic zone is remineralized in the top 1,640 ft (500 m), and only a very small part reaches the great depths. Generally, 2-4 g per square meter per year reach depths of 10,000 ft (3,000 m), while not more than 0.5 g reaches the abyssal plains.
The environmental characteristics of this seafloor are very special. Below 3,281 ft (1,000 m) darkness is total, even in the most transparent waters. The water is cold, about 36[degrees]F (2[degrees]C) and the content of oxygen and particulate organic matter is very constant, due to the low metabolic expenditure. The currents are usually very gentle, but can reach speeds of 10 in (25 cm) per second, affecting sediment distribution and creating heterogeneity in the ocean bottom. The only factor varying appreciably at this depth is hydrostatic pressure, which increases 1 atmosphere with every 33 ft (10 m) increase in depth. This means that in the deepest trenches reach pressures of 1,000 kg/cm2, which has biochemical and taxonomic consequences that are as yet little studied. In fact, the reduced metabolism of the bacteria that live on the abyssal plains is attributed to the high pressure, which would inhibit protein synthesis. The remineralization of organic material is thus very slow.
The fauna of the deep seafloor are surprisingly small, miniaturized in comparison with the animals of the surface water. The reason for this is not clear, as species that are widely distributed both at the surface and at depth do not show any significant decrease in size, and it is the taxa that live exclusively in the depths that are small. The high pressure and limited availability of food must be at least partially responsible for their small size.
The density of individuals and the total biomass decreases with depth, the level of oligotrophy of the surface layers, and distance from the coast. While the abundance of the macrofauna decreases 10-fold for every 0.6-1 mi (1-2 km) increase in depth, the meiofauna decreases at a lower rate (10 times for every 2.5 mi [4 km]). Thus with increasing depth the meiofauna increases in importance with respect to the macrofauna, attributed to the lower availability of food. Their reduced size is also associated with a change in the dominant taxonomic groups. Polychaetes are the dominant group at all depths, but their relative abundance decreases towards the bottom, both in number of individuals and species diversity. At the bathyal level, the other dominant organisms are in the following order: amphipods, isopods, and tanaidacian crustaceans; in the abyssal plains, tanaidacians, bivalves, and isopods; in the oceanic trenches, bivalves, solenogastres (Aplacophora), acorn worms (Enteropneusta), bryozoans, tanaidacians, and spoon worms (Echiurida). Holothiurians are very abundant in some oceanic trenches.
The distribution of organisms by trophic strategies shows absolute dominance by the sedimentivores (80% or more of the total number of individuals), both on the surface and in the fauna. Carnivores account for less than 10% of the individuals, and suspensivores do not usually exceed 7%. In the deep benthos, even representatives of typically filter feeder groups like the sea squirts have adopted sedimentivorous strategies. Detritus-eaters are mainly represented by amphipods (lissianassids), polychaetes, brittle-stars, and fish, but only amphipods go down to the hadal zone.
The normal biomass values found on the abyssal plains range from 0.1-5 g fresh weight per square meter, while at the greatest depths of the hadal zone they are often less than 0.03 g. At the bathyal level the values are much more variable, ranging from 0.5-300 g fresh weight per square meter per year, so that biomass below 6,562 ft (2,000 m) rarely exceeds 5 g.
These low biomass values are linked to extraordinarily slow growth, such as that shown by the bivalve Tindaria calistiformis, which takes 100 years to attain its maximum size of just a few millimeters. Other organisms grow more rapidly, such as certain brachiopods or the macrurid fish Nezumia, which grows at the rate of 1 in (2.5 cm) per year. As a result of the year-round constancy of environmental parameters, there are no signs of seasonality in these deep communities and growth is regular throughout the year.
The exaltation of biodiversity
Maybe the most remarkable fact about the communities of the deep seafloor is their extraordinary biodiversity. The few inventories available for the bathyal depths give a very high number of species, but this diminishes on the abyssal plains and especially at the hadal level. In a study published in 1992 on the bathyal macrofauna (6,890 ft [2,100 m]) of the eastern coast of the United States, the researchers Grassle and Maciolek list 798 species (58% new to science) belonging to 171 families and 14 phyla, collected in an area of 226 sq ft (21 sq m). The Shannon-Wiener index of diversity was extraordinarily high (5.8-6.6), but the most surprising thing was that there was no diminution in the appearance of new species when the sample area was increased, at least within the size limits sampled by these researchers, which confirmed data obtained before in other experiments. Together with the high levels of endemism in the different basins, this makes it possible to affirm that the number of marine species is much greater than previously estimated, and maybe greater than 10 million! There is no agreement on which characteristics of the deep seafloor allow the coexistence of so many species. Several possible causes have been suggested that doubtless operate to a greater or lesser extent. Many of them coincide in that, of necessity, organisms that live in the bathyal seafloor are distributed in "patches," as a response to environmental heterogeneity caused by the unequal arrival of food to the ocean bottom, by the activity of the organisms themselves, small topographical irregularities, the activity of predators, or the preferential fixation of larvae. Another reason might be the existence of great specialization in food consumption, which would minimize competition for a single resource. Nevertheless, it is clear that the deep seafloor houses a number of species that is equal to or greater than the richest ecosystems of the biosphere, and that the study of the mechanisms making this possible is one of the main challenges facing contemporary oceanography.
4. Coral Reefs
4.1 Jungles in the ocean
Coral reefs are a special case of bioherms, or wave-resistant calcium carbonate structures of biological origin. Such marine formations consist of the cemented skeletons of living organisms, known as hermatypes (reef-forming) and their dead remains. Reefs are constructed by various kinds of organisms including, among others, oysters, vermetid gastropods, serpulid polychaetes, calcifying algae (in particular red algae or Rhodophytes), hydrozoans, and corals. The latter are by far the most extensive and form probably the most diverse and colorful of all marine ecosystems, the marine equivalent of tropical rain forest.
Coral reefs surely represent the peak of life on our planet in the marine domain. All other organic reefs are rather limited in distribution, whereas coral reefs dominate benthic biota in virtually all coastal regions in tropical waters. In coral reefs, the hermatypic corals form both the physical framework and the trophic foundation for the entire ecosystem. In many instances they do this in conjunction with the related fire corals, (Millepora, Stylaster), which are not corals at all, but hydrozoans.
The different types of coral reef
Coral reefs have been roughly grouped into three major types: fringing reefs, barrier reefs, and atolls, although in certain studies they have been further subdivided into many more sub-types according to their morphology and genesis.
Fringing reefs are found in close proximity to land, occasionally as close as a few meters from the shoreline, leaving only a narrow lagoon between the reef and the shore. Fringing reefs are common and appear wherever coral reefs begin developing.
Barrier reefs are found much further from land, as in the case of the Australian Great Barrier Reef, which is not only the largest coral reef on Earth, but arguably, also the largest biological structure on it. The Great Barrier Reef spans over 600 mi (1,000 km), skirting the eastern shores of Australia. This reef is often found at more than 60 mi (100 km) from the shore with no true lagoon between land and reef.
The last group, the atolls, are the most peculiar of all reefs. They are subcircular in shape and enclose a shallow lagoon. Diameters of atolls vary between a few meters to over 45 mi (70 km). There are about one hundred atolls in existence, most of them in the Indian Ocean and in the Pacific, while the remaining are spread around the Atlantic Ocean and the Caribbean. The unusual and regular shape of atolls attracted Darwin's attention during his voyage on the Beagle and led him to develop a theory of the origin of their shape that was based on their formation. He suggested that all atolls originated as volcanic islands emerging from the ocean floor, devoid of all life due to their fiery birth. Upon reaching the surface or very near to it, they became a suitable substrate for various benthic organisms to settle upon, mostly, but not exclusively, those with planktonic propagules. Corals indeed do have such free living, planktonic larvae, called planulae. Moreover, they are capable of additional ways of propagation, which will be discussed below. These corals and their associated fauna and flora develop into fringing reefs, surrounding the conical volcanic island. Subsequent changes in the relative height of the island and the sea level, resulting either from a rise in sea level or from the subsidence of the island, lead to the disappearance of the island itself, while the coral reef grows upwards, keeping pace with the rising sea level. If the rate of upward growth of the coral reef cannot keep up with the sinking of the island, the reef is doomed and dies. In existing atolls, obviously this was not the case and once the island sunk, the surrounding reef encircled the lagoon where the volcano once stood. Darwin's theory, proposed in 1842, was finally proven true a century later, when experimental drilling in the lagoon of Eniwetok atoll, specifically designed to test this theory, hit basaltic rock of volcanic origin at a depth of 4,593 ft (1,400 m) below a cover of fossil coral reef.
Fossil coral reefs are found in numerous locations, many of which are at the present time far removed from any sea. The earliest reefs in the fossil record date back to the Ordovician period, 450 million years ago. However, these reefs were built by different hermatypes from those we are familiar with in present-day coral reefs. Since in almost all cases soft tissues are not preserved in the fossils we find, we cannot be certain of the taxonomic affinities of these early reef builders. However, based only on the remains of their skeletons, they are thought to belong to now extinct groups of corals, the rugose and the tabulate. Beginning in the Jurassic period we are able to find coral reefs in which existing groups of corals, and even extant genera and species, play an increasingly dominant role. The main group of hermatypic corals in reefs today are the scleractinias, also known as the madreporarians, which appear in increasing abundance from the Cenozoic period onwards. Of the 7,500 known coral species, some 5,000 are extinct and 2,500 have survived and are found in contemporary reefs.
Living coral reefs are found mainly between the latitudes of 30[degrees]N and 30[degrees]S, or between the tropics of Cancer and Capricorn. However, fossil reefs are found way outside these present limits. Since it is well known that the position of the poles as well as that of the equator have shifted over geological times during which corals and coral reefs already exited, we believe that these major shifts in coral reef distribution result primarily from concomitant changes in the distribution of global climatic patterns over the same period. Today, although some coral species are found outside the described boundaries, they are not hermatypes since they survive and grow as isolated colonies that never develop into continuous, stable reef structures.
The main questions concerning the global distribution of coral reefs are: What are the environmental factors that set the boundaries on coral reef development and survival? How can the present patterns of coral diversity be explained?
Environmental conditions and the availability of nutrients
The obvious absence of coral reefs from the benthos of coastal waters immediately north and south of the tropics indicates a likely relationship with temperature. Unfortunately, the direct experimental evidence to prove this is the causal agent is not conclusive. It has been suggested that temperatures below 59[degrees]F (15[degrees]C) prevent corals from either efficiently capturing prey or from reproducing. Nevertheless, a number of corals have survived exposures of a few hours to temperatures below 59[degrees]F (15[degrees]C). It seems that based on present knowledge we may state that the critical thermal limit to coral reef distribution is set by the 59[degrees]F (15[degrees]C) winter minimum isotherm. So far no oceanic waters too warm for reef formation have been found. However, recently there has been an accumulation of evidence relating extensive damage and subsequent mortality of reefs following changes in oceanic circulation that led to elevated temperatures in the damaged region. These events, in the course of which sea temperatures exceeded by 34-37[degrees]F (1-3[degrees]C) the average values for that area and season, lasted from a few weeks to a couple of months. Based on this correlation and on some laboratory studies, it has been suggested that coral reefs may be potential long-term recorders of sea water warming.
However, temperature may have indirect effects on corals. In tropical waters there is only a minimal difference, if any, between summer and winter temperatures. High insolation keeps the upper part of the water column warm, and due to thermal expansion, also maintains it lighter than the underlying, deep cold water. This situation is called thermal stratification and is a permanent feature of tropical seas. Thermal stratification prevents vertical mixing of the warm upper water and the underlying water. While growing and proliferating, phytoplankton, the microscopic algae which are the primary producers in the oceans, have to extract nutrients, the compounds and elements needed for their multiplication, from the surrounding water. Since phytoplankton require light for their photosynthesis in addition to CO2, which in most marine situations is plentiful, the upper, illuminated water is depleted of these nutrients.
Such nutrient-poor waters are called oligotrophic and cannot support plentiful growth of phytoplankton. This sparseness of plant life is visible to the naked eye, since such waters are strikingly transparent and characteristically blue, the color of clean sea water, rather than the greenish, turbid color typical of "fertile," phytoplankton-rich water. These oligotrophic tropical waters are known as "blue deserts," and due to the paucity of life, deserve this name. Like any other ecosystem, the oceans also depend on photosynthesis of plants as their only energy source. Therefore, lacking phytoplankton, tropical seas cannot support plentiful life of any other group which depends directly or indirectly on these plants. This is especially the case of zooplankton, the free-living animals that graze upon microscopic phytoplankton, and all larger animals which feed upon them, like fish fry, and their predators, as well as all of the larger marine carnivores, including humans, even if they are terrestrial animals.
As we shall see, it is precisely this lack of nutrients and of zooplankton that led to the evolution of the zooxanthellae-coral symbiosis and to the eventual domination of corals in shallow tropical waters. Only under these special conditions of warm, oligotrophic, transparent, phytoplankton- and zooplankton-poor waters do corals and coral reefs have a competitive advantage over other benthic marine communities and, in particular, over seaweeds. In marine environments within the "coral belt" where upwelling takes place, coral reefs are absent. In such regions ocean currents bring nutrient-rich waters from the depths up to the illuminated surface. In these waters massive growth of phytoplankton (water bloom) occurs and the water is turbid and only allows little light to reach the benthos. Moreover, in such waters seaweeds have a clear competitive edge over the slowly growing corals, and the upwelling of water and the abundant nutrients enables seaweeds to overgrow and smother the reef. By controlling vertical mixing, or the lack thereof, and nutrient supply to the upper part of the water column, temperature exerts an additional but indirect effect on coral distribution.
It may be in part due to such upwelling that in general coral reefs are absent from the western shores of continents in latitudes where they abound on the eastern shores of the same continents. This is the case in Australia, Africa, and most of the Americas. Major river systems also cause gaps or interruptions in otherwise continuous reef systems. This may be the result of any of the following or their synergistic effects: lowered salinity, silting, and increased nutrient loading from terrestrial runoff.
However, even within the region where water temperature and low nutrient levels favor the dominance of the shallow benthos by coral reefs, additional factors interact in determining the eventual outcome of the race for the substrate. The relative abundance of herbivores may tip the scales between corals and various algal communities.
Specific diversity and coral behavior
Another major question in coral zoogeography is that of the uneven distribution of the species and genera. There are marked differences between the Atlantic and the Indo-Pacific domains. This has led to a controversy over the question of whether the Indo-Pacific region of high diversity is a center of evolution from where coral species spread out, many of them simply vanishing on the way, or whether this region of high diversity is a "refuge" where species that evolved elsewhere accumulated due to the favorable conditions found there. This question remains unresolved.
Another related question concerns the settlement of corals on newly formed suitable substrates, such as emerging volcanic islands, far from existing reefs. It has been known for a long time that coral planulae become part of the plankton and as such are carried by ocean currents. However, little is known about the ability of these planulae to survive such voyages. Laboratory studies have shown that planulae of some coral species may survive for periods as long as three months before settling. If during this time they reach suitable and unoccupied substrates, they may become the beginning of a nascent reef. Given the velocities of oceanic currents, transportation of planulae over distances beyond 621 mi (1,000 km) is highly unlikely. Nevertheless, recent studies have demonstrated that coral planulae may settle on floating pumice stone and start developing into a coral colony. This colony, occasionally even a few colonies of different species, may then be transported in the oceanic circulation over many months and years and cover thousands of kilometers. Once they hit land or sink due to the increasing weight of the growing coral colony, they may become the beginning of a reef, or just add species to an existing one. Given that the pumice originates in eruptions of submarine or terrestrial volcanoes and that each volcano and eruption has a characteristic "fingerprint," or chemical composition, it is possible to date each piece of pumice. Based on such evidence and on the collection of "rafting" corals on beaches of Pacific islands, a model of colonization of islands by corals and reefs has been proposed.
Distribution by depth
On a local scale, the single factor determining the distribution of corals and of any individual reef is depth. Reefs begin virtually at the surface of the sea and reach maximal development in the upper few meters. Both growth rates and abundance of species slowly decrease with depth. Although some coral species such as the deep water Red Sea coral, Leptoseris fragilis, may live at depths over 325 ft (100 m), they are not hermatypes, since they do not form reefs. Furthermore, common hermatype species such as the common Red Sea coral, Stylophora pistillata, which in shallow waters may be an important element in the reef structure, do not form reefs towards the lower limit of their distribution.
The only single environmental parameter that follows a similar bathymetric pattern is underwater light. In all aquatic environments light is attenuated rapidly, at a rate that depends on water transparency. Other parameters known to affect reef growth and distribution--such as temperature, nutrients, and zooplankton--or which have been suggested, do not show a depth relationship that would explain observations in reefs throughout the world. The basis of this dependence of coral reefs on light will be discussed in detail in later sections. In any case, the depth boundary for coral reef development depends on water transparency, the parameter that determines how far light can penetrate to a given depth. This close correlation between underwater light and reef development is determined by the photosynthetic capabilities of the coral's algal symbionts, the zooxanthellae.
4.2 The coral reef ecosystem
The coral reef ecosystem shows all the parameters of a mature ecosystem, according to the now classic definitions of Margalef and Odum. It has a high and constant biomass, and respiration nearly equals productivity. In other words, coral reefs are in an almost steady state, with respiration consuming all the biomass produced and utilizing all of the photosynthetically stored energy. Biodiversity on coral reefs is high (among the highest found anywhere on our planet), a feature also thought to be a corollary of maturity in ecosystems.
Complexity and relationships
If, as a result of volcanic action, a land mass emerges at suitable latitudes, a never-ending process of colonization by coral planulae and propagules of various other benthic organisms begins. These sessile organisms are followed by others, and by motile organisms that depend on the sessile organisms for shelter and food. As time passes more species settle and competition for available substratum and energy reduces the resources available for each species. Opportunistic species following an r strategy (many easily dispersed, quick-growing, short-lived offspring) are replaced by highly specialized K strategists. Specialization narrows the niche needed for each species, reduces overlap among these narrowing niches, and results in an increase in the number of species with small populations. This minimizes interspecific competition while reducing the population of each individual species.
Since nutrients in surrounding waters are scarce and most are locked away as part of the living reef biomass, the production of new biomass on reefs is limited and regulated by the rate of their release from the reef. The release and mineralization of these nutrients, in particular nitrogen and to a lesser degree phosphorus, is accomplished by the death of reef organisms and the action of many bioeroding animals that drill into and dissolve the reef framework. These are mainly drilling algae and sponges, as well as coral-dwelling barnacles and clams.
In most developed coral-reef ecosystems, the energetic foundation of the reef ecosystem is provided by the zooxanthellae, the endosymbiotic algae living within the coral cells. In addition to these primary producers, coral reefs are home to many other types of algae: lowly inconspicuous caespitose algae, endolithic algae hidden within the coral skeleton, calcareous hermatypic red algae, calcifying green algae, as well as many seaweeds attached to bare rock or dead coral on the reef. Nearby sandy bottoms and shallows are covered with sea grasses.
These photosynthetic organisms, as well as the relatively sparse zooplankton, all contribute to the overall high primary productivity of the reef. The photosynthesizers, or producers, eventually support all of the many reef consumers, including plant-eating herbivores, carnivores, detritivores, and decomposers. The herbivores grazing and browsing on plants include filter-feeders such as clams and mussels, zooplankton, and the grazing sea urchins, gastropods, fish, turtles, and dugong.
All the predators depend on these herbivores, or on other, lower order carnivores for food. These predators include corals, sea lilies, polychaetes, manta rays, and planktivorous fish. The reefs are inhabited by many predatory fish such as groupers, moray eels, lionfish, scorpionfish, stone fish, parrotfish, sharks, and stingrays (Trigon), all carnivores and part of the reef's second trophic level, after primary producers and herbivores. These are joined by many invertebrate carnivores such as starfish, sea snails and slugs, and many crabs and shrimps.
Detritus, or dead particulate organic matter, satisfies the needs of many additional reef dwellers. Prominent detritivores are sea cucumbers and bottom-burrowing sea urchins.
Since corals and coral reef ecosystems have evolved under long periods of stable conditions, they are ill-adapted to deal with catastrophic perturbations of these conditions. Being marine organisms living in a medium with extremely constant salinity, corals are very sensitive to any exposure to fresh water. A massive downpour over the Hawaiian island of Oahu resulted in the formation of a 3 ft (1 m) deep layer of fresh water over the Kaneohe Bay coral reefs. This layer persisted for a few days and resulted in the death of virtually all shallow water corals, particularly affecting the reef table. Cases of coral death due to rainfall during low tide have also been described in the Great Barrier Reef.
In the Red Sea corals are normally never exposed, even during low tide. However, in 1970 a combination of low tides with northerly winds resulted in a week-long exposure of the reef table to the air and to the scorching noon-day heat. This led to the massive die off of all of the upper part of the reef in the Gulf of Aqaba and the stench of decomposing coral permeated the air of the entire region.
Hurricanes have likewise wreaked havoc on reefs. Many reefs such as Discovery Bay, Jamaica and the Mexican reefs in Yucatan in the Caribbean were hit very hard in 1988 by hurricane Gilbert. Branching species such as the stag-horn coral (Acropora cervicornis), which prior to the hurricane dominated the reefscapes, were the hardest hit. This was not only due to their abundance, but also to the arrangement of the branches, which have a narrow, fragile base that presents a long lever to the high energies of the wave and currents.
It is worth mentioning that the effects of these catastrophes on the respective reef systems, and the subsequent courses of recovery, are quite different. The Red Sea system had, prior to the low tide, a very high species diversity, with around one hundred species of hermatypic corals, all affected to the same extent by the catastrophe. However, once the area was denuded, colonization by the opportunist species Stylophora pistillata (an "r" strategist), began and it has now become dominant. As time passes since the 1970 low tides, this species is declining, and species diversity is gradually increasing. In the Caribbean the reef was almost a monospecific stand of the stag-horn coral (Acropora cervicornis). Once this was wiped out the smaller, more compact species that were smothered in the shade of the branches of the A. cervicornis thicket, began to grow. The result of the hurricane was thus an increase in species diversity, rather than a reduction as occurred in the Red Sea. As time passes, A. cervicornis populations are recovering and will probably become dominant again.
The recent widespread reef mortalities following "bleaching" events (loss of the zooxanthellae of the corals) are also thought to have been triggered by natural phenomena. However, there is convincing evidence that bleaching events are triggered by a regional increase in water temperatures. Ocean warming by 36-37[degrees]F (2-3[degrees]C) was in turn linked to an El Nino Southern Oscillation event. This is a change in the oceanic current patterns in the southern Pacific ocean, which some researchers suggest is a result (or proof) of global warming.
An interesting case of natural damage to a coral reef was seen in the winter of 1992-1993 in the Red Sea. That year the winter was the longest and coldest on record, and as a result the mixing of waters was deeper and lasted longer than normal. This resulted in the injection of a much larger quantity of nutrients from the deep waters below the thermocline into the illuminated surface waters. This "natural eutrophication" event had two consequences. In the normally nutrient-poor, crystal-clear waters of the northern Red Sea, a phytoplankton bloom developed, severely curtailing the light reaching the corals. This problem was further exacerbated by the development of a massive cover of seaweeds, mainly the green algae Enteromorpha and Ulva, which overgrew and eventually smothered many of the reef corals. Hardest hit were small colonies of branched species such as Stylophora pistillata, which suffered a 40% loss.
In general it seems that in most cases reef systems are capable of recovering following a natural perturbation, even a major one. It is the chronic exposure to sub-lethal, anthropogenic stress agents that reduces the ability of reefs to overcome natural disasters. This was clearly the case in the Red Sea, where following the 1970 low-tide die-off, corals in polluted and heavily visited reefs never recovered their original splendor. However, twenty years after the event remote reefs in pristine locations are as diverse and robust as they were before.
4.3 The organisms of the coral reefs
It is evident that coral reefs contain more than just corals. To the contrary, as has already been mentioned, the biodiversity around coral reefs is enormous, although the corals, or perhaps the very striking coral fish, are the most typical group. Invertebrates are also abundant and highly diverse.
The coral reef ecosystem consists of corals, which are of course invertebrates, and is also inhabited by myriads of animals from almost all the other marine groups. They can be classified by their degree of association with the reef, the trophic level they occupy, whether they are builders (hermatypes) or not, whether they contribute to the workings of the system, or whether they are bioeroders that attack it. The invertebrates of the coral reefs can be classified according to their taxonomic affinities. A detailed consideration of any of these classifications, given the immense numbers of organisms that are involved, goes far beyond the scope of this work. Furthermore, owing to the remote situation of many coral reefs, many species have not yet been discovered and described. Even in the cases of the relatively few organisms that have been described, little is known of their biology, life cycles, trophic levels, and niches within the coral reef ecosystem. We will confine ourselves to some of the most visible and important invertebrates of the coral reefs, and use them to illustrate certain key groups and their functions within the ecosystem.
Bacteria are, however, a special case worthy of comment. They are present in relatively low concentrations in the oligotrophic waters around the coral reefs. They undoubtedly help the ecosystem to extract certain nutrients from the water that, given their low concentrations, are unavailable to phytoplankton, corals, seaweeds, and marine phanerogams. There are undoubtedly populations of bacteria associated with the copious mucous secretion produced by the corals, as well as with the regenerative functions of nutrients that occur in the internal spaces of the coral reefs and colonies. The important role of this group is only just beginning to be studied.
Corals or anthozoans
Corals, although they are sessile for most of their lives, are animals. Not only are they incapable, with very few exceptions, of locomotion, but their shapes and colors bring to mind plants and flowers. This is probably the reason for the name that was given to the whole group when it was first described: Anthozoa, which in Greek means flower-shaped animals. Corals belong to the Coelenterata, multicellular animals with a simple body plan based on radial symmetry. Their body develops from two cell layers, an outer one, the ectoderm, and an internal one, the endoderm. These layers are invaginated into each other, forming a double-walled tube open at one end. This opening, the mouth, serves for food ingestion and for excretion, and is surrounded by tentacles used for food capture. In most coelenterate groups (including the corals), the tentacles are armed with numerous stinging cells for prey capture and immobilization.
The Cnidaria consists of three groups of predominantly marine aquatic organisms. These three groups are the Scyphozoans, the medusas or jellyfish; the Hydrozoans, which include the Hydras and the fire corals; and the Anthozoans whose most familiar members are the sea anemones and the corals. In the coelenterates there is an alternation of generations between a sexual, motile, medusa stage and a sessile, asexual, polyp stage. The distinction between the three groups is based primarily on the relative importance of the medusa and polyp stages. In the jellyfish the medusa predominates, both in terms of size and duration of life cycle, whereas in the hydrozoans it is the polyp, with the medusae being minute and short-lived, and in the Anthozoans the medusa stage is totally absent.
Most corals are colonial, starting from a fertilized egg, that develops into a free-living and free-swimming planula. Once it finds a suitable substrate it loses motility, settles, and develops into a polyp. This subsequently grows by budding into a colony with a typical shape for each species, but that also modified by environmental conditions.
The corals themselves are further divided into the Octocorallia and the Hexacorallia. Members of the first group have eight feathered tentacles, whereas the second have six simple tentacles or multiples thereof.
The octocorallians or soft corals
The Octocorallians as a group, unlike the Hexacorallians, do not have calcium carbonate skeletons and, with few exceptions, are not hermatypes. Their skeletal elements may either be characteristic, flexible individual spicules, or hard, horn-like skeletons used in some cases as jewellery, especially the red coral, Corallium rubrum and the black corals (Antipathes). Members of this group, also known as soft corals, are important members of every reef although they do not contribute to reef architecture.
All of these probably feed on zooplankton, and many of them, like the Hexacorallians, have symbiotic zooxanthellae. Some members of this group have striking shapes and colors, and the species that do not harbor symbiotic zooxanthellae may be found at great depths where they feed by filtering zooplankton from the water, like nets growing at right angles to the predominant currents. Some members of this group produce potent anti-predator substances that are being carefully screened by pharmaceutical companies as possible sources of antibiotics. The various soft corals compete with Hexacorallians and other hermatypes for suitable substrates for settling. Members of this group generally reproduce sexually in a number of ways. The sexes may or may not be separate, and in the simplest cases, the female eggs and male sperm may be released into the water, where fertilization takes place. In many species the egg is retained in special brooding pouches where fertilization takes place. The fertilized egg develops into a planula that is released into the water when mature.
The hexacorallians or madrepores
The hexacorallians (particularly the scleractinians) are by far the most important reef builders. This group contains some 2,500 living members that vary in shape, color, size, longevity, and biology. The basic building unit of these corals is the same as that found in the soft corals, the polyp. This polyp originates from a sexually produced planula which, once settled, begins building a skeleton attached to the substrate. The preferred substrates are rocks scraped clean of previous inhabitants by fish or sea urchins, or the skeletons of dead corals. These skeletons, although they eventually become surrounded by living animal tissue, are nevertheless cemented to the rock and are thus topologically external, unlike the internal skeletons of vertebrates. As the skeleton grows, a cup-like depression is formed where the polyp resides. This depression, the calyx, has radially arranged partitions, or septa, corresponding to animal tissue structures anchored to these septa, the mesenteries. These, and the mesenteric filaments attached to them, create a body cavity, extending to the mouth, whose main function is digestive. Zooplankton touching the tentacles cause a discharge of the stinging cells that inject poison, immobilizing or killing the prey. The tentacles bring the prey to the mouth and it is digested by the action of the endoderm. Undigested remains of the prey are evacuated through the mouth. In some species the mesenterial filaments can be extended through the mouth, to a considerable distance and are used against competing coral colonies. In such encounters the less "aggressive" species is digested by these mesenterial filaments or damaged by the action of special "sweeper tentacles." Such interaction, as well as "overtopping," determine the hierarchy of dominance among competing coral species in reef communities.
Individual polyps divide upon reaching a characteristic size, typical for each species. These polyps usually remain in contact by means of continuity of tissue among the individual polyps in the growing colony, which grows into a shape and size unique to the species--although it may be modified to some extent in response to environmental factors, especially wave energy, and the intensity and directionality of underwater light. The shape, size, and arrangement of septa in the calyx, as well as the distances and pattern of calyces in the colony, are the most important features upon which coral taxonomy and identification of of species is based.
In other species there are no discrete individual polyps, a situation that leads to the familiar "brain coral" colony morphology (e.g., Platygira meandrina). Some corals consist of single polyps, which nevertheless may reach sizes of 20 in (50 cm), like some "mushroom corals" of the genus Fungia. Coral species differ not only in colony morphology, but in growth rate, ranging from a few millimeters per year in some of the massive, slow-growing species, to over 4 in (10 cm) a year in branching, rapidly growing ones.
Hexacorallian corals reproduce sexually in similar ways to those described for the related Octocorallians. Whenever fertilization is external, the timing of egg and sperm release is critical. In the Great Barrier Reef all species spawn during a few nights, presumably synchronized by the phase of the moon. In other localities no such mass spawnings are known, and in some localities coral reproduction is spread over many months even, in some cases, in species that in the Great Barrier Reef participate in mass spawning "orgies." Of course the protein-rich eggs and sperm are relished by all planktivores, which make sure they are around at spawning time.
The planula resulting from fertilization is barely visible to the naked eye and is exposed to the same dangers as all marine plankton. This planula is capable of swimming by ciliary motion, although it is transported over significant distances by ocean currents. It has a mouth, and is usually capable of feeding during its planktonic phase. Once it settles it undergoes metamorphosis into a polyp and begins depositing a calcareous skeleton on the substrate which, if it survives, will develop into a characteristic colony.
Many hermatypic corals, and in particular branching ones, frequently suffer breakage due to their calcium carbonate skeletons. This may happen as a result of storms or, as is increasingly likely, of human action. Such broken branches, if they fall upon suitable substrate at suitable depth, may develop into new colonies. In certain species and localities such fragmentation is an important means of reproduction. All daughter colonies in a stand originating by fragmentation from a single colony are, of course, genetically identical. Such reproduction contributes to the formation of extensive monospecific stands, whereas sexual reproduction provides opportunities for increasing gene pools within populations, as well as allowing for long-range transportation of species and their eventual establishment in new regions.
The coral reef is unique because the main primary producers, the algae, whose photosynthesis supports the life of the entire ecosystem, live within the cells of animals, or to be more precise, within the cells of the corals themselves. These plants are unicellular organisms belonging to a group of algae called the dinophytes or dinoflagellates, which are important components of many phytoplankton assemblages. However, while the free-living dinoflagellates have two flagella each that endow them with motility, the endozoic symbionts of corals, the zooxanthellae, are normally sessile.
These microscopic algae are about 10 microna in diameter and may reach densities of over a million cells per square centimeter of coral. The zooxanthellae live in a very tight symbiotic association with the corals, from which both partners benefit in a way that allows both of them--or more accurately their association, the zooxanthellate coral colony--to colonize and dominate habitats in which each partner alone could not succeed. In their association, it is the zooxanthellae that put their photosynthetic capability at the service of the association, providing the host animal with energy-rich organic molecules produced by means of photosynthesis. These compounds are not retained by the algae, they leak from their cells and thus become available to the host animal.
It is thought that this process, called translocation, results from a combination of two factors. The zoo-xanthellae, due to the low level of available nitrogen and phosphorus, cannot utilize the abundant carbon acquired through photosynthesis and so excrete these high-energy, low-nitrogen compounds into their environment (the cytoplasm of the coral cells). In addition, the coral, by means of the so-called "host factor," induces increased excretion in the zooxanthellae. The translocated compounds, especially in shallow water under conditions of high light, satisfy all the metabolic needs of both symbiont and host, and their needs for growth and reproduction. In return, the zooxanthellae gain access to the coral's nutrient-rich metabolic waste products.
These waste-products are harmful to the coral, but they are efficiently taken up by the zooxanthellae, thus preventing their loss into the nutrient-poor water and allowing them to be recycled and utilized within the coral colony and the reef as a whole. However, although the symbiosis between coral and zooxanthellae assures the coral a source of energy in zooplankton-poor waters and minimizes nutrient losses from the system, this relationship cannot provide the nutrients, other than carbon, needed for growth. These still have to be acquired either from the dissolved, mostly inorganic nutrients in the water, or from the digestion of prey captured by the polyps. Since both of these are usually in poor supply in the tropics, whenever they are available they are avidly taken up and stored for prolonged use.
The population density of the zooxanthellae is normally stable for any given coral species and environmental conditions, and ranges between hundreds of thousands and a few million cells per square centimeter of coral. This population density is maintained as a balance between the growth rate of the zooxanthellae (which tend to increase their density), that of the coral (which tends to decrease their density), the loss of zooxanthellae due to expulsion from the colony, and possibly, although not yet proven, the digestion of some zooxanthellae by the host. The main factors affecting the growth of the zooxanthellae population are nutrient supply and light intensity. In experiments where the level of nutrients, in particular nitrogen and phosphorus, was deliberately increased, the control of the zooxanthellae population broke down and the algae, rather than translocate the products of photosynthesis, retained them and used them, together with the now plentiful nutrients, to increase in numbers.
Such situations occur whenever human activity or carelessness results in increased levels of nutrients in the water, a process known as eutrophication. Increases up to fivefold in numbers of zooxanthellae in the coral tissue show up as visible darkening of the colonies. This process is detrimental to the corals because the growing zooxanthellae population now retains the products of photosynthesis instead of translocating them to the host. Furthermore, the dense zooxanthellae population now finds itself requiring carbon for photosynthesis at a higher rate than is available. This results in a decrease in the rate of photosynthesis of the zoo-xanthellae and a further reduction in their contribution to the wellbeing of their host.
Another instance of the breakdown of the regulation of the zooxanthellae population is known as bleaching. This term was coined to describe a loss of zoo-xanthellae from the corals to the surrounding waters, which become turbid and brownish due to the presence of large numbers of now motile algae in the water. Unless the affected colony is recolonized by residual zooxanthellae cells left behind in the tissues, the colony dies.
In addition to the Hexacorallians that are the main builders of coral reefs, some other zooxanthellate coelenterates also make a minor contribution to the formation of reefs. Among the most prominent of these "false corals" are the organ-pipe coral (Tubipora musica) an Octocorallian, and the common "fire coral," the Hydrozoan Millepora dichotoma. The latter form a distinct Millepora zone in many Red Sea reefs. Fire corals have numerous potent stinging cells used to immobilize prey, and possibly for defense, which may inflict fairly painful and long-lasting burns on unwary swimmers.
Reefs are inhabited by many species of sea anemones such as the large Condylactis gigantea, which lives in a mutualistic symbiosis with the clownfish, Amphiron bicinctus. This anemone also harbors numerous zooxanthellae in its cells. On soft bottoms next to coral reefs, in atoll lagoons, and in the bizarre "jellyfish lake" in Palau, there are many jellyfish. Some feed on zooplankton and small fish while others, such as Cassiopea andromeda, also harbor zooxanthellae and feed primarily on the products of their photosynthesis. Unlike any other jellyfish, this species basks in sunlit shallow waters in an "upside-down" position like no other, exposing its zooxanthellae-packed tentacles to the sun.
One of the most colorful group of coral reef invertebrates are the feather duster worms, a group of filter feeders that after their free-living larval existence undergo metamorphosis into a sessile adult. These worms dwell as adults in a calcareous tube embedded in the coral skeleton, which becomes part of the reef structure. Feeding and respiration are assisted by whorls of arms in constant movement.
Some species, like Spirobranchus giganteus, show an unexplained rainbow of vivid colors, unrelated to the color of the host coral colony. It has been suggested that these colors actually protect the population as a whole, since predators that are likely to associate a given color variety with their favorite prey will ignore individuals of a different hue. These polychaetes are quite abundant in reefs and may reach densities of many dozens on the same coral colony. Their distribution strongly indicates a preference for live coral over any other substrate. The motion of the cilia on their tentacles may create small currents, bringing prey into the reach of the coral's tentacles. Furthermore, any food captured and digested by these and any other filter feeders enriches the waters with nutrients in the immediate proximity of the reef. These are derived from prey arriving from relatively distant waters, thereby providing additional nutrients to be assimilated by the zooxanthellae and subsequently made available to the coral.
This diverse phylum contributes representatives to every type of functional niche on the reef and reef system. There are hermatypes integrated into the reef, bioerosive agents boring within the coral skeletons, species harboring zooxanthellae, herbivores, carnivores, sessile forms (oysters, gastropods and clams), as well as agile swimming forms (nudibranchs), and they may have soft bodies or hard shells. Some are camouflaged while others advertize their presence with bright, iridescent colors.
One of the many striking reef bivalves is the giant clam, Tridacna maxima. This is one of the largest of all mollusks, reaching lengths of over one meter and weighing over 881 lb (400 kg). Individuals of this size are found in the Pacific and Indian Oceans, but because of the length of time it takes them to reach this size and overfishing, they have become rare. After their discovery by seafarers, they became a prized trophy to be presented to many cathedrals, churches, and sanctuaries in Europe for use as baptismal fonts and a favorite ornamental motif in Baroque and Rococo art. Over the centuries these clams have been sought after for their meat and shells, and are now the focus of serious efforts to bring them under cultivation in centers in Palau and other countries in the Indo-Pacific. They are cultivated both for human consumption and for their shells. For food they are harvested at the age of 2-3 years, whereas the older and larger their shells, the greater their value. These bivalves also have zooxanthellae, although unlike corals they are not endocellular, but live in the body fluids. Algae provide much of their nutrition, the remainder being obtained from plankton filtered from the water.
Other sessile mollusks common on reefs are vermetid gastropods such as Dendropoma maxima, which following a free-swimming, planktonic larval stage, settle on the reef, and form an irregular shell extending like a net over the surface of the coral. These obtain their food by spreading a sticky mucus net over the surrounding surface and ingesting it periodically with the entrapped plankton. The shells of these organisms reach diameters of 1 in (3 cm), and lengths of 20 in (50 cm) and, like the shells of the giant clam, eventually become part of the reef.
Unlike the giant clams and vermetids that become part of the calcareous reef structure, there are species of mollusk that actually weaken the coral skeleton, actively boring into it by dissolving the calcium carbonate it is built of. An example of such a bio-eroder is the small drilling date mussel, Lithophaga lessepsiana, the size of a grain of rice, which lives in the skeleton of various species of living corals such as Stylophora pistillata, its favorite host. This date mussel, like all of its relatives, feeds by filtering plankton from the water it pumps through its siphons and over its gills. Other bivalves that drill into the coral prefer different hosts. A large-sized colony of S. pistillata may contain hundreds of Lithophaga lessepsiana that will eventually lead to the breakage and death of the colony. Nevertheless, it seems that in healthy coral colonies the tiny currents carrying food and oxygen into the date mussels are actually beneficial to the coral, whose zooxanthellae avidly take up any ammonium excreted by the clam.
Another group of mollusks (far more harmful than the diminutive date mussels we have already discussed) are those that, like the gastropods of the genus Drupella and especially D. cornus, actively feed on the living coral tissue. Infestations by explosively growing populations of such corallivores may have devastating effects on whole reef communities. Many other colorful snails either graze on coral reef algae or prey on various animals living on or next to the reef. Among these are the venomous cone snails, principally of the genus Conus, whose radula has evolved into a highly specialized hypodermic needle-like proboscis used to inject deadly venom into both prey and attackers. These beautiful snails have been prized by collectors and this has led to their extinction in many localities. Their potent venom may be lethal even to humans. Other striking reef snails such as the cowrie snails (Cypraea) are also collected by people living around the reefs, mainly for sale in vast numbers to tourists, often far from their origins.
Other highly visible coral reef dwelling mollusks include the various species of sea slugs. These gastropods lack the protection of a hard shell and in many cases rely on being poisonous or distasteful. They display vivid colors which may function as warnings and remind any potential predator of their taste. Other species combine the excretion of unpleasant tastes with perfect camouflage, allowing them to blend inconspicuously into the surroundings of the reef.
The Echinodermata is an exclusively marine phylum with many species represented in coral reef communities. Virtually all members of this phylum begin their life following external fertilization as planktonic larvae. As adults they show an external body plan based on a characteristic radial symmetry. Their locomotion is by means of special contractile "feet" called tube feet, unique to the echinoderms. These tube feet are a combined hydraulic-muscular system, each operated by a bulb that pushes water into the tube-like foot, and by muscles in the foot that determine the direction of its extension. At their tip the foot ends with a suction disk that allows the animal to hold on to surfaces and move, or to lift and move small objects and food. This unique water-vascular system is the means of locomotion used by starfish, sea cucumbers, and sea urchins. The main reef dwelling echinoderms belong to all the major classes of the phylum: crinoids or feather stars, sea cucumbers, starfish, brittle-stars or serpent stars, and sea urchins, none of which contributes to the formation of the reef. In fact two of the reef's worst enemies--the crown of thorns starfish (Acanthaster planci) and a species of the sea urchin Diadema--are members of this phylum.
Feather stars and sea cucumbers
The colorful, delicate feather stars, or articulated crinoids (Antedon, Leptometra), are among the most beautiful sights on the night reefscape. They have five arms, each branching into two near its base. These plankton feeders skim the reef waters with their ten feather-like arms, filtering out minute creatures that are then propelled towards the upward-facing mouth. They hold on to the reef substrate with claw-like cirri, which also allow them to move from their day-time hiding crevices towards their seaward-facing nocturnal outposts. This activity seems to be aimed at avoiding diurnal predatory fish, while at the same time capitalizing on the vertical night-time ascent of zooplankton towards the relatively shallow reef.
On the sandy flats surrounding reefs, derived in part from the erosion of the reef itself, many sea cucumbers (Stichopus, Thelenota, Holothuria) may be seen. Some species may reach up to 4.9 ft (1.5 m) and crawl sluggishly along the soft bottom, ingesting the sand or mud and digesting any organic matter in it. Because they crawl in the direction of their tentacle-surrounded mouths, their body plan has become elongated and, in some species, they have developed a secondary, bilateral symmetry. Some of the group members protect themselves by means of strong poisons, while others respond to suspected attacks in rather unusual ways. There are species that eject their entrails and leave them to the enemy, being able to regenerate them subsequently. Others entangle the foe in a sticky net formed when the Cuvier tubes are expelled through the anus and rupture, releasing a proteinaceous liquid that gels upon contact with the water. Certain species of sea cucumbers are prized in the Far East and the Pacific Islands as gastronomic delicacies. In their preparation special care is given to avoiding the toxic effects of the cucumber.
Starfish (Acanthaster, Protoreaster, Culcita, Linckia) are common residents of coral reef. These echinoderms have a characteristic radial symmetry and usually have five arms, although some species have up to forty arms (in multiples of five), while some have none at all and have evolved pentagonal forms with lightly pointed or convex sides. They are enclosed in protective plates and move about, like sea urchins and sea cucumbers, by means of water-powered tube feet. Starfish are active carnivores preying on sessile or slow-moving animals, either ingested or digested by turning its stomach inside-out and surrounding part of the prey. Many starfish eat clams and mussels, which they slowly pry open by pulling continuously with their numerous tube feet until the clam tires and opens.
Given the havoc wreaked on vast regions of coral reefs, especially in the Great Barrier Reef, by the crown of thorns starfish (Acanthaster planci) and the worldwide concern over the very survival of these coral reefs, we shall discuss this starfish in some detail. The crown of thorns is a large starfish that may attain diameters of up to 30 in (75 cm) over a period of 30 years. The adult has 16-17 arms equipped with strong poisonous thorns and regenerates even from fragments of arms, rendering it virtually immortal. An adult female may release millions of eggs in the course of a few weeks in the summer. The eggs hatch into planktonic larvae that spend 2-4 weeks in this state until, upon reaching the reef, they settle and metamorphose. The juveniles feed for a few months on algae and then switch to their main food, the coral. The crown of thorns is a most accomplished corallivore, with a uniquely specialized array of enzymes for the digestion of coral waxes. It prefers branching corals, although under epidemic conditions it will attack all species of coral. Under normal conditions, population densities of this starfish are very low and for the western Indo-Pacific, where no damage to the reef was observed, it was estimated that there were only six animals per square kilometer. When there is an epidemic outbreak, numbers increase explosively by three to four orders of magnitude above normal, reaching as many as 15,000 per square kilometer. With adults denuding about one square meter per day, an average 10 square kilometers of reef on the Great Barrier Reef could be destroyed in about two years.
The first carefully documented outbreaks of the crown of thorns occurred in 1957 in the Ryukyu islands south of Japan. Numerous subsequent outbreaks were documented from 1960 on the Great Barrier Reef, in the Mariana, Caroline, and Marshall Islands, and New Britain, in Malaysia, Fiji, the Philippines, Western Samoa, Tahiti, Hawaii, and Sri Lanka. On the Great Barrier Reef, their devastating impact was so severe that the Australian government established a special commission to study and, if possible, to solve the problem. The more commonly accepted view claims that the recent Acanthaster planci outbreaks result from human action. Suggested causes are the widespread marine pollution that reduces the resilience of corals and reefs systems, or human reduction of the starfish's natural enemies. An example of such an enemy is the giant conch Charonia tritonis, which avidly feeds on the crown of thorns starfish and which has been driven to the verge of extinction by widespread collection for human consumption and for the tourist souvenir trade. Additional specialized enemies, such as the fish Arothron hispidus (a Tetraodontid or pufferfish) and Cheilinus undulatus (a Labrid fish, the giant Maori wrasse), are also known, and human involvement in the reduction of the size of their populations is also assumed to have occurred.
Another highly visible group of echinoderms in coal reefs are the sea urchins. These have a large calcareous shell, or test, consisting of many plate elements that enclose all of the urchin's internal organs. The test is covered with movable spines, characteristic and different according to species. These range from the massive, over 4 in (10 cm) long and 0.4 in (1 cm) thick spines found in the slate pencil urchin (Heterocentrotus mammillatus) which are used to make mobiles, wind chimes, and jewelry; through the 8 in (20 cm) long, barbed, thin needles of Diadema setosum and related species; the 0.4-0.8 in (1-2 cm) long, 0.8-1.2 in (2-3 mm) thick spines of the Echinometra; to spines reduced to a velvety, furry cover found in bottom dwellers in sandy reefs like sand-dollars (Echinarachnius, Mellita) and similar burrowing species.
Many urchins have, in addition to spines and water-tube feet, special appendages called pedicellaria that also form part of the water tube system. These end with a three-clawed tip and are used by some species to clean the spines, while in others, such as Asthenosoma varium, they are equipped with powerful poison glands. Sea urchins have a five-toothed mouth located on their underside. The teeth are used to scrape the living cover of the reef that mostly consists of algae, but may also include various benthic animals such as young corals. Like all the echinoderms, sea urchins have external fertilization with planktonic larvae.
The sea urchins of the genus Diadema are of special interest because of their role in the bio-erosion and pauperization of coral reefs. When accidentally stepped upon or carelessly touched, these purple-black urchins inflict painful wounds with their hair-thin, barbed spines, which may take a long time to heal. These urchins graze in large groups around the bases of the reefs, eroding both living and dead corals. The visible result of their action has been named the "Randall halo" and it eventually leads to the breakage and death of whole corals. Most other urchins also rank among the coral bio-eroders, since they feed by nibbling at the live coral. They also weaken the reef structure by creating holes and crevices in which they hide during the day.
These echinoderms are avidly eaten by a number of fish who have found ingenious ways to overcome their defenses. Triggerfish (Balistes) expel from their mouths a strong jet of water that turns the urchins upside down and exposes the areas around the mouth that lack spines, thereby allowing the fish to crack the urchin open. Once this is accomplished many other fish join the feast on the now defenseless urchin.
The last and least conspicuous common class of echinoderms on coral reefs is the Ophiurida, or brittle-stars. These are the most agile of all echinoderms, scampering on and about the corals, propelled by their five long flexible arms. They feed mostly on detritus, although one group--the sea basket brittle-stars in which the five primary arms are profusely branched--are thought to filter plankton. These latter brittle-stars are rather conspicuous denizens of the nocturnal reefscape. During the day they hide in deep reef crevices and exhibit their remarkable lace-like, 28 in (70 cm) diameter, whorl of arms from dusk to dawn.
There are numerous representatives of this important group in coral reefs. Some are just attractive additions to the dazzling color display of the reef, whereas others fill important niches in the system. Many tiny crustaceans or larval stages of otherwise large species are part of the zooplankton which is, to varying degrees, the basic food supply of the reef. The many species of corals, sea lilies, fish, bivalves, and all the other planktivores--whether filter feeders or active zooplankton hunters--transform the reef into a wall of mouths extracting zooplankton, mostly crustaceans, from the water bathing the reef.
Like planktonic crustaceans, the sessile barnacles, the Cirripedes, as a group are not uniquely associated with coral reefs. These are common dwellers of intertidal rocky shores in almost all seas and they also inhabit many other living and inanimate substrates, from ships and piers to turtles and whales. Besides those barnacles that cover bare, exposed rocky shores next to reefs, there are others which thrive on dead coral or on nearby mangrove trunks. Of special interest are those highly specialized barnacles which settle on, and eventually become embedded within, the coral skeleton. This group consists primarily of species that live on only one or on a few related coral species.
It is far from understood how the planktonic juveniles manage to breach the formidable batteries of stinging cells employed by corals and hydrocorallians, penetrate through the host tissue, and settle on the skeleton. Although these barnacles cause in some cases deformation of the colony, as is most evident in the case of the barnacle Savignum milleporae on the "fire coral" (Millepora dichotoma), it may well be that both barnacle and coral benefit from the association. As in so many mutualistic symbioses found in coral reefs, the coral provides the substratum and a protected haven, whereas the barnacle creates micro-currents with its cirri and captures and digests zooplankton. The metabolic waste products of this digestion enrich the micro-environment of the coral colony inhabited by the barnacle. The nutrients excreted by the barnacles are assimilated by the zooxanthellae and are subsequently made available to the host coral in the translocation stream described above. All barnacles are hermaphroditic and, since fertilization is internal, they have to settle in proximity so that their gametes can reach each other. Upon hatching, the larvae join the plankton and eventually settle once they find a suitable substrate--usually next to other individuals of the same species that the larvae identify from extremely low concentrations of specific types of excreted compounds.
Another peculiar association between crustaceans and corals is that of the gall crab, Hapalocarcinus. The female settles at a branching point in the coral which, due to irritation caused by the crab, becomes modified into a cage-like gall that encloses the female. The zooplankton on which the crab feeds and oxygen reach the female through remaining openings in the prison-like gall. Fertilization and release of the larvae also take place through these pores.
A remarkable mutualistic symbiotic process involving crustaceans protects branched Pocilloporid corals (such as those of the genus Stylophora) from the crown of thorns starfish (Acanthaster planci). Small crabs (0.8-1 in [2-3 cm]), mostly from the genus Trapezia, live deep among the branches of the corals where they find shelter and food. They induce the coral to secrete mucus, which they then gather with their modified legs. When their host coral is approached by a crown of thorn starfish, the crabs emerge from among the branches, climb towards the tips, and extend their pincers and drive it away. It has been shown that experimental removal of the crabs renders the coral colony defenseless and likely to succumb to the attack of the crown of thorns.
Some additional rather striking examples of such associations are the delicate cleaning shrimps of the genus Stenopus, which hide in reef crevices and underneath corals with only their long, thin antennae protruding, beckoning to fish to come and be pampered. These shrimp, while feeding on various ectoparasites and bits of loose skin, help to keep their "customers" healthy. As will be discussed below, there are also fish that make a living in a similar fashion.
There are shrimp species that can be found only on or next to specific hosts or associates. For instance, the velvety sea anemone, Cryptodendrum adhesivum, is home to two different species of delicate, nearly transparent shrimps of the genera Periclimenes and Thor, which live on its surface. The nature of the association is not clear but the shrimp may gain protection and may also feed on mucus excreted by the anemone. When food was offered to the anemone in an experiment, a large robust xanthid crab was repeatedly seen to force open the anemone's mouth to steal the recently ingested titbit. This relationship is known as kleptoparasitism, or thieving parasitism.
On flat bottoms next to reefs, burrows housing couples of gobies and shrimp are a fairly common sight. The shrimp have strong, shovel-like claws that they use to dig the common burrow, but being blind, they rely on the sight of their fish-associates to warn them of impending danger and to forage for the food that the fish and shrimp share. The shrimp have long thin antennae with which they sense the movements of the fish. These relationships involve a number of species of gobies and shrimp in different regions and reef zones.
The hermit crabs are yet another group of crustaceans and are found in virtually all seas. These crabs have a soft abdomen that is considered to be a delicacy by the many hungry predators of the reef. The hermit crabs hide this vulnerable part of their anatomy in vacant shells of dead snails. These are cast off as the crab molts and outgrows them, moving to a "new," larger home. A large hermit crab, Dardanus, found on reefs, does not rely on the protection afforded by a shell. Instead, it collects up to a dozen highly stinging sea anemones that it transplants onto its own shell as a rather formidable defense system.
Various species of lobsters may be found (Panulirus japonicus, P. longipes, P. ornatus, P. versicolor, etc.) on many reefs. They usually hide in deep, dark recesses during the day and come out onto the reef flat to feed at night. These crustaceans are highly prized all over the world as a delicacy. The expansion of global trade and the numbers of gourmet tourists reaching the world's most remote reefs result in worldwide overfishing of all lobster species.
Fish are one of the groups that are most visible, abundant, species-rich, and important to the ecology of the reef itself, as well as to the economy of human societies living next to reefs. The many thousands of coral reef species range from those that totally depend on the reef to those whose interaction with the reef system is either loose or occasional.
Coral reef fish exhibit all the different types of reproductive behavior known in this group of animals. However, some generalizations may be made. Many fish invest in caring for their eggs, placing them in protected places. The clownfish (Amphiprion) attaches its eggs to the surfaces behind the sea anemone in which it lives. Others, like the triggerfish (Balistes, Canthidermis, Melichthys), build nests in which the female lays her eggs, which are then fertilized in a complex ritual pattern. The nest is guarded from predators and the parents keep it oxygenated by water jets that are aimed at the eggs until they hatch. The widespread occurrence of parental care in reefs seems to be in agreement with ecological theory, which predicts that in mature ecosystems, like coral reefs and tropical rain forests, many species will show K strategies (such as long lifespan, few offspring and high parental investment in caring for their offspring).
Many species of reef fish undergo sex changes in the course of their life. For instance, the Red Sea goldfish (Anthias squamipinnis) begins its life as a female in a school living around a knoll. Such a school may consist of tens and even hundreds of females. Hovering above them there are a few males sporting a distinctly different coloration, adorned with trailing dorsal and tail fin appendages. The males are more exposed than the females as they live above or outside the school and the relative safety its large numbers provide, and are thus far more likely to be devoured by reef predators such as groupers. When a male disappears, the largest, most dominant female turns into a male. The potential for sex change is possible due to the presence of undeveloped gonads of the opposite sex which are induced to take over by social or environmental, hormone-mediated cues.
Other reef fish, including many grouper species (Epinephelus, Mycteroperca), as well as some butterfly and clown fish (Chaetodon, Amphiprion), live in pairs for a whole reproductive seasonal cycle, or, as is the case in groupers, for life.
Coral eaters: butterfly fish and parrotfish
The two most important groups of coral-eating fish are the Scaridae, parrotfish, and the Chaetodontidae, butterfly fish.
The many, typically stout, fish of the Scaridae, known generically as parrotfish (Scarus, Scarops, Bolbometopon, Sparisoma, Cryptotomus) because of the characteristic form of their mouths and their bright coloring, range from 4 in (10 cm) to 39 in (1 m) in length. There are species which live in pairs as well as gregarious species which form large groups, and colors range from black and dull brown to a rainbow of bright blues, purples, greens and yellows. All members of the family have the teeth in the upper and lower jaws fused into a sharp, strong parrot-like beak with which these fish gnaw at the coral, eating its tissue and skeleton, leaving typical tell-tale scars. They also eat various algae which they scrape off the substrate. At night they sleep within crevices in the reef, wrapped in a mucous cocoon which their skin secretes.
The Chaetodontidae, the aptly named butterfly fish (Chaetodon, Chelmon, Heniochus, Forcipiger, etc.) are a group of brightly colored, laterally compressed, sub-elliptical fish, whose adults grow to 4-8 in (10-20 cm). Their anatomy is suited for precise maneuvering among corals and narrow reef passages, and their abrasive teeth (the scientific name Chaetodontidae means "bristle teeth") are used to nibble on coral tissue and other benthic organisms.
Seaweed eaters: the surgeon fish
Species of surgeon fish (Acanthurus, Zebrasoma, Prionurus, Axinurus, etc.) are common among the fish living in schools along the seaward faces of reefs. Their name comes from the sharp scalpel-like spines at the stem connecting body and tail. They graze on plant material which they digest with the assistance of a group of recently discovered protoctists living in their digestive system. These fish may be seen at sunset swimming in caravans converging from all over the reef towards a rendezvous point. Once there, the mass of thousands of individuals slowly begins forming a rotating, conical mass. As the density and speed of swimming increases, the cone becomes a frenzy in which the uppermost fish repeatedly break the surface of the water. A few males crowd a gravid female and simultaneously release eggs and sperm. The water becomes turbid with gametes to the delight of many plankton feeders waiting in the wings. Soon, peace and calm return to the scene, the orgy being repeated daily for some three months.
The large predators: the sharks and skates
No discussion of coral reef fish would be complete without dealing with sharks and their relatives, the rays and skates. Sharks and rays are by no means unique to coral reefs. However, there are species of shark, unique to coral reefs, which patrol the waters along the seaward face of reefs, frightening fish, swimmers and divers alike, though other species just visit the reefs (Carcharhinus leucas, Negaprion brevirostris, Gynglimostoma cirratum, Triaenodom obesus, Sphyrna zygaena, etc.). Most sharks do not venture on top of the reef table, except at high tide, and even that is done only by smaller species, like the black-tipped coral shark (Carcharhinus limbatus), and young individuals of other species. Larger and faster species patrol seaward reef and steep cliffs. Localities like Blue Corner in Palau (Carolines), and Ras Mohammed in the Sinai peninsula (Egypt), are considered favorite shark-viewing localities.
Skates and rays are common dwellers of sandy bottoms in both lagoons and seaward reef slopes. These cartilaginous fish possess an extremely flattened version of the shark body plan. The largest of the group, the manta rays (Manta, Mobula), resemble a majestic flying carpet spanning up to 13 ft (4 m) from fin tip to fin tip. These are, contrary to their awesome appearance, among the most innocuous of all reef dwellers, feeding on the plankton they filter from the offshore waters. The related skates and rays (Dasyatis, Urolophus) are also dorsally flattened bottom-dwellers and crush various molluscs with their hemispherical teeth. Their whip-like tails are equipped with barbed blades and when threatened they may use these tails to inflict severe gashes. In some members of this group, the spine even has a venom gland at its base to further add to the effect of this potent tool.
Fish schools: damsels, groupers and clownfish
Many fish species swim along the outer faces of reefs in schools ranging from a few individuals to many thousands. Such schooling behavior may be limited to juvenile stages, to the spawning season or be permanent throughout life. Schools are thought to have many advantages ranging from reducing hydrodynamic drag, thereby saving metabolic energy, to scaring predators who see the dense school as a large, threatening creature. The many fish in the school may also distract the attention of the predator, or, as is the case with herds of terrestrial herbivores, may encourage the survival of the fittest by sacrificing the slow and sickly.
There are species which use the reef for refuge from predators. These schools retreat into the safety of the coral branches at the slightest sign of danger which perhaps may be merely a shadow falling on the school. Normally small, these fish live within a permanent territory, or to be more precise, a particular coral colony. In most cases the school lives in the same coral for as long as the coral colony survives. Usually, a given fish species will prefer a specific coral species. Typical examples are the schools of small and colorful Pomacantrids such as Chromis caerulaea, made up of sometimes hundreds of individuals each, living in an Acropora colony, or the small schools of the striped damsel fish, Dascyllus aruanus, which also usually lives among Acropora branches. They venture away from the colony to gather food and will defend their territory from foreign intruders, usually conspecific fish. The defended territory is within a larger area in which food is collected. Slightly looser is the association between fish such as the Red Sea goldfish, Anthias squamipinnis, which has a territory consisting of a whole coral knoll, or reef section. Such a knoll is a multi-species coral community towards which the school withdraws. Near such knolls, in addition to the above mentioned species, all of the planktivorous, territorial pairs or single predators may also be found. Among these, special mention should be made of the colorful reef groupers (Epinephelus, Mycteroperca) which pair for life.
A special, highly conspicuous example of territorial, "fixed-address" group of reef fish are the clownfish (Amphiphron, Premnas) which live in symbiotic association with sea anemones. This group includes numerous species common in all coral reefs which live in pairs, or small schools, in species-specific symbioses with sea anemones. The nature of the symbioses is not wholly understood, but in many cases includes mutual protection from predators, an aspect seemingly more obligatory from the point of view of the fish, since no adult clownfish are ever found without a host anemone while anemones without clownfish are fairly common. In at least some cases, the fish have to become "conditioned" to their anemones in order to become immune to the stinging cells of the anemone. There also are nutritional relationships among the two partners. In many cases it has been observed that once satiated, the fish will bring excess food to the mouth of the anemone, which will then avidly swallow it. The clownfish not only hide within the anemone when threatened, but also attach their eggs to the wall behind the anemone where they are protected until they hatch. Other brightly colored fish, such as the emperor angelfish (Pomacanthodes imperator) may be seen feeding along the same reef stretch for many years.
It has been suggested that the bright coloration of many reef fish is a warning aimed at intruding members of the same species that the territory is occupied. The Austrian ethologist Konrad Lorenz coined the term "poster color" (Plakatfarbe) for this type of coloration. In some cases, including that of the emperor angelfish, the juveniles of the species have a totally different color scheme from the adults, possibly protecting them from the larger adults. The different colors make them appear members of a different, and thereby non-competing, species. More recently it has been argued by Paul Ehrlich that some of the most aggressively territorial fish have a drab coloration, while some vividly colored ones are seemingly non-territorial, or even live in schools.
The art of camouflage: scorpionfish and seahorses
As a striking contrast to the myriad of brightly colored fish species dotting the reefs, among the denizens of the reefs there are many masters of deception and camouflage. These include the stone fish (Synanceia verrucosa and other species of Synanceiids), the scorpionfish (various species of the genera Dendrochirus and Scorpaena, as well as other Scorpaenids) and frogfish (Antennariid family), all of which rely on their ability to blend all but perfectly into the reef background to conceal themselves from their enemies and prey. They lie patiently in ambush until an unwary prey passes by. The usually sluggish predator opens its enormous mouth virtually sucking it in. Many of the members of these fish have poison glands at the base of their dorsal spines and pose a very real danger to any human accidentally stepping on one. Such a sting may cause excruciating pain, paralysis and death. The near-perfect camouflage of these fish is sometimes further elaborated by the use of "flash color." When a stonefish or scorpionfish leaves abandons its immobility that makes it invisible against the background, it reveals the striking colors of its unfolded pectoral fins. The bright flash of the swimming fish suddenly vanishes when it stops, leaving a puzzled observer unsure of where all that color has gone.
Camouflage patterns may vary from a rock overgrown with seaweed, as in the case of the stonefish, to brightly colored sponges, as is the case in the frogfish, or even to floating algal clumps, emulated in fine detail by the seahorse, Phyllopteryx foliatus. Other species look like floating leaves with all of their anatomy rearranged to serve as disguise: their bodies are flattened and elongated, they have a greenish color with realistic looking blemishes, and, most strikingly of all, they swim in a direction perpendicular to the long axis of their body as do some centriscids. The head points down, and the propelling caudal fin, much reduced in size, is bent at a right-angles to the rest of the body.
Other color patterns aim at disrupting the overall body contours of the fish by means of different geometric patterns of stripes and color patches. In fact, some of the authors who reject Konrad Lorenz's "poster coloration" theory discussed above claim that the vivid colors of so many reef fish act more like the patterns painted on military aircraft, vehicles and buildings which break up their outlines. Yet another common device is the concealment of the eye. Eyes, due to their optical properties and colors, stand out against the surrounding background and thus draw attention of the observer. Furthermore, some predators, including the reef heron (Egretta gularis), try to spear fish through their eyes. Therefore, it is common to either hide the eye by means of a dark stripe running through it, or to have a false eye at some distant location on the body.
Spines and poisons: Diodontids, Tetradontids and lionfish
The reef is so extremely species-rich that there are numerous strategies employed to ward off potential and dedicated predators. The spectacular lacy lionfish (Pterois volitans) has poison glands at the base of the rays of its fins. No wonder it is able to swim in majestic serenity and advertise its venom by its bright coloration while it leisurely swallows small fry! Many swimmers and divers have been lured by its beauty and slow movement through the water into trying to catch it or touch it with their bare hands. The unexpected lightning speed stab with the dorsal spines is a painful, potentially deadly lesson to the unwary. A totally different strategy is that of the Moses sole (Pardachirus marmoratus) of the Red Sea. This fish is preyed upon by sharks, and fights them with a poisonous skin secretion which paralyses the shark's jaws. This neurotoxic poison is currently being studied as a promising shark deterrent for human use.
Pufferfish (Arothon and other genera of the Tetraodontid family) and porcupine fish (Diodon hystrix and other diodontids) use a unique combination of weapons to deter enemies. They are capable of inflating themselves by taking in water in order to increase their volume. In this way, they change their shape from an elongated "typical" fish shape into an elliptical balloon, in the case of pufferfish, or into a near perfect sphere, in the case of porcupine fish. In the latter fish, inflating its body also causes its strong, stout spines to change from a position parallel to the body axis to a perpendicular one. The names of the tetraodontids and the diodontids refer to the fact that these fish have all their teeth fused into two teeth (one on each jaw) in the diodontids, or four teeth (one on each side of each jaw) in the tetraodontids. In addition to their anatomical and behavioral defense mechanisms the latter family also produce one of the most potent poisons known to man, tetradoxin, used for medical purposes and in neurophysiological research.
5. The dark abyss
5.1 The biotic conditions of the abyssal zone
Contrary to the popular perception of the sea, 95% of its volume is a dark, cold environment with calm water although occasionally crossed by powerful currents and (apart from some "oases" of life) extremely poor in animal life (plant life obviously being absent because of the lack of light).
The presence of life in the depths
The lack of light, the extremely high pressure even at moderate depths (hydrostatic pressure increases by 1 atmosphere with every 33 ft [10 m] depth) and the predictable lack of food due to the absence of primary producers, led the English naturalist Edward Forbes to formulate the azoic theory at the middle of the last century. This theory that marine life was impossible below 1,640 ft (500 m) in depth was soon disproved by three different types of evidence. The first was that repairs to telegraphic cables between Europe and Africa showed heavy colonization by benthic organisms at depths greater than 3,281 ft (1,000 m). The second was that in some places on the coast of Italy, fishermen knew of rising currents that brought strange fish to the surface: they were dark and bioluminescent with large mouths and are now known to be mesopelagic. The third type of evidence was the results of the Challenger expedition (1872-1876), partly intended to confirm or disprove the azoic theory, and one of whose first conclusions was to confirm that animal life was present on the ocean bottom at all depths.
The zonation of the deep sea
The average depth of the oceans is about 13,123 ft (4,000 m). A vertical division of the ocean would divide it into an upper illuminated (photic zone) and a lower dark aphotic zone. The photic layer, which allows light to penetrate, does not usually exceed 328 ft (100 m). In the centers of the oceans, where the water is very transparent due to the low levels of plankton and suspended materials, light can be detected at depths of 656 ft (200 m) or more. Extremely slow-growing algae have been found on seafloor at depths of 820 ft (250 m), using the scant light reaching this depth. The rest of the ocean, from 656 ft (200 m) down to the greatest depths (more than 136,089 ft [11,000 m] in some Pacific trenches) is in total darkness, only broken by the bioluminescence of some abyssal organisms.
The salinity of the aphotic layer is remarkably uniform, but its temperature first declines rapidly with depth (the permanent thermocline, down to the first 3,281 ft [1,000 m]) and then maintains an almost constant thermal condition, with cold temperatures between 39 and 28[degrees]F (4 and -2[degrees]C); moreover it does not undergo the seasonal changes experienced at the surface. Oxygen levels are uniformly high (except in some highly localized anoxic basins), and as already mentioned hydrostatic pressure increases steadily with depth.
Almost all the underlying level's input of food comes from surface production, which is seasonal as well as reflecting variations in oceanic production. Upwellings and coastal areas show greater inputs than the ocean centers, and so abyssal organisms are slightly more abundant in these areas, both in the water column and on the seafloor.
The precise bathymetric limits given to the different subzones of the aphotic zone suggests they may well be artificial. The benthic fauna is better-known because organisms are "concentrated" on the seafloor and capturing them is relatively more efficient; it occurs in the bathyal zone (between 656 and 13,123 ft [200 and 4,000 m] depth, immediately below the sublittoral zone occupying the entire continental platform), the abyssal zone (between 13,123 and 19,685 ft [4,000 and 6,000 m]) and the hadal zone (between 19,685 and 36,089 ft [6,000 and 11,000 m]). The etymological derivation of these words is relevant; bathys means deep, abyssos means bottomless, and Hades is the underworld.
In the water column, immediately below the photic or epipelagic zone, is the mesopelagic zone (between 656 and 3,281 ft [200 and 1,000 m] in depth), where pelagic and planktonic animals are relatively abundant. These dark (black, brown, or red), animals possess bioluminescent organs and eyes and migrate vertically to the epipelagic zone at night. The lower zones of the mesopelagic zone are harder to define, although by analogy with the benthic zones they have been called bathypelagic (between 3,281 and 13,123 ft [1,000 and 4,000 m]), abyssopelagic (between 13,123 and 19,685 ft [4,000 and 6,000 m]) and hadopelagic (between 19,685 and 36,089 ft [6,000 and 11,000 m]). The very few animals of these abysses are whitish or transparent, with reduced or absent eyes, and lack luminescent organs.
5.2 Abyssal organisms
The scarcity of available food and the high pressure (which affects animal cell morphology and enzyme activity) are two environmental factors that help to explain not only the progressive reduction of the number of organisms with depth, but also the fact that some taxonomic groups are completely absent from deep waters, while others show extreme diversification. Sponges, for example, dominate in the first 6,561 ft (2,000 m) but form only a very small part of the benthic fauna at greater depths, disappearing completely at about 26,247 ft (8,000 m). Molluscs are not very abundant at any depth, but they also completely disappear at great depths. Starfish may account for 25% of the animal populations present between 9,843 and 22,966 ft (3,000 and 7,000 m), but are absent at greater depths. Holothurians, echinoderms that are scarce in surface waters, are the dominant organisms (50%) below 9,843 ft (3,000 m) and almost the only inhabitants of the hadal and abyssal seafloor (90%), where they show a diversity of forms and adaptations unknown in shallower waters.
The adaptations of the abyssal fauna
The difficulty of studying these organisms in their natural environment means that not all their adaptations have been discovered, nor is the purpose of some known adaptations well understood, but there are some notable characteristics that deserve comment.
The scarcity of food explains why many fish have a relatively large mouth, often with long thin inward-curving teeth to ensure captured prey cannot escape. The jaw is articulated to the cranium, articulated in turn to the spinal column, allowing the mouth to open so wide the fish can eat prey larger in size than itself. In some fish (Ceratiidae) the modified rays of the fins or barbs act as luminous "lures" to attract prey. Carnivores dominate the fauna of the water column.
Finding food in the water column is difficult because it is scarce and because it settles out (the bigger the particle, the faster it settles), but it is just as difficult to find food on the seafloor. The chance of food reaching the seafloor is very low and much of the organic material that arrives is not very digestible (bones, chitin, etc.). The animals of the deep benthos are basically sedimentivores, carrion-feeders and predators, although filter-feeders (suspensivores) are also present. Many organisms can change strategy with food availability. They all have a well-developed sense of smell and are attracted by the arrival of large fragments of food, such as the corpses of fish and cetaceans. Filter-feeders usually settle in sites where currents run and cast enormous nets (varying in structure and origin depending on whether the organism is a sponge, cnidarian, crinoid, etc.) that ensure a meager catch. Many of these organisms possess peduncles or similar structures that anchor them to a soft substrate and separate them from the seafloor. Some benthic fish (called tripodfish) "stand" on large stilts (the tips of the ventral and caudal fins).
The lack of food may explain the reduced size of most abyssal animals (especially bathypelagic fish and most benthic invertebrates). A typically abyssal phenomenon is giantism, especially among crustaceans, which can reach sizes ten times greater than relatives in shallower water. Amphipods and isopods 16 in (40 cm) in length and ostracods 2 in (4 cm) in length are not uncommon. High pressures and low temperatures might explain this phenomenon, which could also be due to a long lifespan. Body water content increases with depth and some deep-sea invertebrates (for example, cephalopods) resemble jellyfish, giving them the neutral buoyancy necessary to maintain their position in the water column with minimum metabolic effort. Protein content also diminishes with depth as a consequence of the lack of food. In mesopelagic fish there is a very clear correlation between the ability to migrate vertically and anatomical characteristics. Both types are black or silvery, with large eyes and mouths, and small bodies showing bioluminescence, but the migratory ones (such as Myctophidae, commonly called lanternfish because of the presence of photophores) have well-developed muscles, bones and a swim bladder, while non-migratory fish (such as Stomiatidae, called dragonfish because of their ferocious-looking mouth) lack a swim bladder and have poorly developed bones and musculature. Bathypelagic fish also have reduced eyes and if they do not migrate, their nervous and circulatory systems are less developed than in their shallow water relatives.
The low density of organisms on the seafloor raises problems when it comes to reproducing. Many invertebrates and some fish are hermaphrodite, and some species, after finding a mate, attach for life (such as the parasitic males of the Ceratiidae). It is not known how benthic invertebrates manage to congregate into large reproductive groups, but pheromones are probably involved. On the other hand, it is clear that luminous organs play some role in identifying animals of the same species (social roles) and appropriate partners (sexual). In some cases the life-cycle includes very short-lived larvae that settle in the same area as their parents, but in other cases there is a relatively longer larval phase in the well-lit surface layers.
The remarkable luminous organs of abyssal organisms, called photophores, are basically sacs containing slightly or highly modified light-producing bacteria. The most complex photophores have complex lenses to focus the light produced, reflectors to concentrate it, shades to turn it off at will, filters to modify the light's color (originally blue-green and cold, consisting only of the radiation of the color emitted, unlike electric light bulbs which emit much of the light in the form of heat), muscles to move the sacs, and some species can even empty them. The importance of these organs is shown by both their complex anatomy and their abundance in many different groups (fish, cephalopods, crustaceans, etc.). They appear to play a variety of roles, although many are no more than reasonable suppositions.
As mentioned above photophores play a role in reproduction and the identification of members of the same species (for example, in forming schools). Their ventral position and the fact that they shine downwards with the same intensity as the midday sun, has led people to think they serve to ensure their owner passes unseen as, when seen from below, they would be indistinguishable from the environmental backlighting and surrounding twilight. Some lures to attract prey are also luminescent, and it has also been suggested that the light emitted by a predator allows it to see its immediate prey. Some shrimp and squid emit a luminescent "cloud" that might confuse potential predators.
It thus appears that sight does play some role even in this dark or twilight environment. Bathypelagic and bathyal animals have large eyes, or tubular ones that concentrate the little light reaching this depth. Some species have dimorphic eyes, such as squid with one large eye pointing upwards and the other, smaller, one pointing downwards, the same direction as the photophores. Bathypelagic fish are black or brown, and the crustaceans are red (since red light does not reach this depth, they are effectively black). At greater depth animal eyes are reduced, but only rarely are they absent, unlike the situation in underground freshwater where the animals lack pigments or are transparent. It appears that some crustaceans in hydrothermal vents can "see" the emerging hot water with secondary "eyes" that detect very low, heat-bearing, wavelengths.
Since the formulation of the azoic theory, and in spite of its refutation, until the middle of the 20th century it was commonly held that the abyssal ocean bottom and waters were a biological desert. Nowadays this idea has been abandoned with respect to the variety of organisms found, but their extremely low production has been confirmed.
These eternally dark environments show great biological diversity. Different hypotheses have suggested that this diversity is due to the fact that these environments have been stable for extremely long periods of time, or because the organisms are extremely dispersed which would have prevented competitive exclusion between different species, a phenomenon that clearly occurs in other communities. Or it may be because the abyssal environment, whether benthic or pelagic covers an enormous area (the largest on the planet, as already pointed out), which would also allow great diversity.
Whatever the reason, this great diversity is accompanied by a very low level of production (apart from the exceptions discussed below). Planktonic biomass decreases by four or five orders of magnitude between the surface (where values are around 100 mg per cubic meter) and 22,966 ft (7,000 m) (about 0.01 mg). The values for the benthos are similar, and decrease from 1,000 g per square meter in well-lit waters to 0.2 g in the deepest trenches. Total production may be estimated at 0.1 g of carbon per square meter per year, although data are very scarce. These values may be 1,000-10,000 times greater in very specific locations, called abyssal (hydrothermal) oases.
Among the planet's most curious living communities are those discovered in the "rift" areas around the Galapagos Islands in the Pacific in 1977. These are areas where what are called hydrothermal vents emit water at tens of hundreds of degrees, like non-stop geysers. The communities found consist of strange worms and other animals, mostly unknown to science. The species were not only new but also belonging to new higher taxonomic groups, such as Riftia pachiptila in the group called vestimentiferan tube worms (related to the Pogonophora), of exceptional length for vermiform animals about 3 ft (1 m).
This extraordinary phenomenon has since been found to occur in other areas and oceans. It is remarkable not only for the enormous abundance of organisms in very specific areas of the seafloor (the reason why they are called oases), but because the food chains are not based on photosynthesis by plants (and are thus unlike the ones most marine animals depend on). In this case, the primary producers are chemosynthetic bacteria, especially sulfur bacteria (the heated water contains dissolved hydrogen sulfide), iron bacteria, and the bacteria using other metals dissolved in the vent water.
Some of the animals found in these oases are filter-feeders or feed on clumps of bacteria, which are very abundant. The main member of these populations, Riftia, possesses a specialized organ, the trophosome, containing symbiotic sulfur bacteria. The animal supplies them with carbon dioxide, oxygen and hydrogen sulfide, while they supply the vestimentiferan with much of the organic material they fix chemosynthetically. Other animals in these oases, such as worms and bivalves, also possess symbiotic bacteria and show highly modified metabolisms (hydrogen sulfide is extremely poisonous). This symbiosis is not the only remarkable aspect of their biology. The water that emerges from the vent may be as hot as at 392[degrees]F (200[degrees]C) or more. The life of a vent is short and a thriving community may fail in a few years as the vent disappears, while new ones may appear at a considerable distance. How these new oases are colonized is not well understood.
The discovery of these extraordinary deep ecosystems has aroused interest in both the abyssal seafloor and in surface communities rich in hydrogen sulfide. These deep-sea ecosystems are under threat from human beings. The fishing of highly-valued decapod crustaceans (prawns, crayfish, etc.) is impoverishing the bathyal seafloor. The dumping of dangerous wastes of all types (from the dumping of radioactive waste into the deep trenches to the dumping of urban and industrial wastes under consideration by large cities after "filling" the coastal areas that have so far been used for dumping waste) threatens the deep seafloor near the continents. The wealth and diversity of the eon-old environments is under threat even before they are fully understood.
Chemotrophic bacteria on seafloor without oxygen
More recently other unusual abyssal environments have been found where primary production by the chemosynthetic metabolism of different bacteria makes life possible for other organisms. In 1984 in a subduction trench off the coast of Oregon, at a depth of 6,562 ft (2,000 m), a cold vent was found (a few tenths of a degree above the temperature of the surrounding water) surrounded by large populations of bivalves (Calyptogena). The vented water is very rich in dissolved methane. The decomposition of the organic material of the accumulated sediment at the bottom of the subduction trench at high temperature and pressure (see volume 1, pp. 30-31) means that once oxygen has been used up, organic material is reduced to methane which then escapes from the sediment's surface (like the methane formed in the anoxic bottom of some highly eutrophic lakes, and called marsh gas).
There have been repeated findings of animals similar to those of hydrothermal oases in other abyssal ocean bottoms lacking oxygen for one reason or another, such as the case of a 66 ft (20 m) whale skeleton found in 1987 in the Santa Catalina basin off the coast of California, at 4,068 ft (1,240 m). Animals collected in the surrounding area, which was anoxic due to excessive oxygen consumption due to decomposition of the whale corpse, included species already known from oases (two giant species of the genus Pyropelyta, and large bivalves of the genera Idasola, Vesicomya, Calyptogena and Lucinoma). Large populations of vestimentiferans of the genus Lamellibrachia were also discovered in the Bay of Biscay near the remains of the 1979 wreck of a vessel with a cargo of beans, sunflower seeds and bales of sisal (a large quantity of organic material) whose decomposition led temporararily to a local depletion of oxygen.
Finding bivalves and vestimentiferans with symbiotic sulfur bacteria in an environment where there was no sign of hydrogen sulfide was surprising. There was debate between biologists (who maintained hydrogen sulfide had to be present) and geochemists (who said there was none because they could not detect it in water samples). Both were eventually shown to be right by the discovery on the sediment surface of sulfate-reducing bacteria. When the hydrogen sulfide they produce enters contact with the seawater it is oxidized very rapidly (the reason it did not appear in the chemical analyses) but the bivalves and vestimentiferans capture it while still nascent, supplying it to their symbiotic bacteria, which use it as their energy source for primary production.
The successive discoveries of populations of organisms previously only found in hydrothermal vents, such as vestimentiferans and bivalves, in other anoxic, methane- and hydrogen sulfide-rich environments, and of populations of metabolically versatile archeobacteria, some free-living and others in symbiosis with different animals, leads one to conclude that hydrogen sulfide-based chemosynthesis is a much more widespread basis for primary production than was thought just a few years ago, when hydrothermal oases were first discovered.
The dream of the Piccards
What a pair the Piccards were! Climbing Europe's highest mountains was not enough for them--they wanted to go even higher. Instead of resigning themselves to life in a land-locked country, they explored the ocean depths. Auguste (1884-1962) and Jean Felix (1884-1963) Piccard were twin Swiss engineers. Until the beginning of the space age, they held the records for reaching the furthest limits of the biosphere in both directions.
From their youth they were enthusiasts for aerostats. First Auguste Piccard flew in an aerostatic balloon, and Jean Felix soon followed him. After 1926 the two brothers converted their balloon into a real laboratory to respond to ever harder challenges. They repeated Michelson's experiment to measure the speed of light and Morley's to show the nonexistence of "ether," as well as measuring cosmic rays and the temperature distribution within the aerostat's gas. The final result was the two brothers' series of ascents in the 1930s.
On May 25th, 1931, few thought that Auguste Piccard and the engineer Paul Kipfer would be the first to reach 49,212 ft (15,000 m) in the pressurized cabin of the FNRS-1 balloon in their 16-hour voyage over the Alps. It was repeated in 1932 with a flight from Zurich airport to Lake Garda in Lombardy during which Auguste Piccard and the Belgian physicist Max Cosyns reached an altitude of almost 17, 00 m (55,577 ft [16,940 m], to be precise). This record was beaten in 1934 when Auguste's twin brother, Jean Felix Piccard reached 57,579 ft (17,550 m) with his wife Jeannette.
Once the stratosphere held no more secrets, Auguste Piccard turned to the abyssal depths. The presence of life in the ocean depths was passionately debated at the beginning of modern scientific oceanography. Edward Forbes (1815-1854) and Christian Gottfried Ehrenberg (1795-1876) engaged in a long argument on this point until repairs in 1860 to the telegraph cable laid between Sardinia and Annaba (Algeria) in 1858 at a depth of 7,218 ft (2,200 m), showed many unknown organisms (mainly coelenterates and molluscs) had settled on the cable in the two intervening years.
However, nobody had been down to see it for themselves, and there were many reasons to think that it was impossible for human beings to reach such great depths, or the even greater depths shown by systematic ocean soundings. In 1934, while the Piccards were soaring into the stratosphere, the American zoologist William Beebe (1877-1962) reached a depth of 3,028 ft (923 m) in a device called a bathysphere. Like the cabin of the Piccards stratospheric device, it was a 4.8 ft (1.45 m) diameter sphere for one or two persons and some equipment, suspended from a cable, and capable of descent to the desired depth. The bathysphere could not maneuver and there was always the risk that the cable might break. This achievement stimulated Auguste Piccard to renew work on an old project, or perhaps a childhood dream: to construct a device applying in water the same principles that the aerostat applied in air (lift is provided by being lighter than the surrounding liquid). This was the beginning of the bathyscaphe.
When he was a young engineering student in Zurich in 1905, Auguste Piccard had drawn up a design of this type. Just when the Antwerp shipyards were about to start construction in 1940, the German army invaded Belgium. His dream had to wait a little longer. The first bathyscaphe was finished after the Second World War, in 1948. Auguste Piccard called it the FNRS-2 to make clear the technical analogy with his 1931 FNRS-1 stratospheric balloon. It was tested near the Cape Verde Islands in collaboration with the French navy. In the first test Auguste Piccard and Theodore Monod descended to sandy seafloor 82 ft (25 m) deep and returned to the surface without problems. In the second test the bathyscaphe reached 4,528 ft (1,380 m) and returned successfully to the surface, although bad sea conditions damaged the buoyancy element and further tests had to be called off. A few weeks later the American Otis Barton's improved version of the bathysphere, called a benthoscope, reached 4,518 ft (1,377 m). The bathyscaphe's maneuverability, however, meant it would carry out the future exploration of the great depths. It basically consists of two parts: a suspension or flotation device, similar to an aerostat but full of a liquid lighter than water (rather than a gas lighter than air as in hot-air balloons and dirigibles), and a cabin for two persons and their equipment. The experience acquired in the 1948 tests led to improvements to bathyscaphe design, especially in the buoyancy device. Between 1953 and 1954 two new crewed bathyscaphes, the FNRS-3 and the Trieste, began to compete in reaching great depths. There was great rivalry between the two as differences had arisen between Auguste Piccard and his French and Belgian sponsors: although the FNRS-3 was basically the same cabin as the FNRS-2 with a new suspension element and closer to Piccard's initial design, he disowned it. Together with his son Jacques he designed the Trieste and found the means to build it in Italy.
Both the FNRS-3 and the Trieste were completed in the summer of 1953 and the first tests took place in the Mediterranean in August and September of the same year. The FNRS-3 crewed by the Frenchmen Georges Huout and Pierre de Willm reached a depth of 2,461 ft (750 m) on August 8, followed by 5,085 ft (1,550 m) on August 12 and 6,890 ft (2,100 m) on August 14 off the coast of Toulon. The Trieste crewed by Auguste (then 69) and Jacques Piccard descended to 2,296 ft (700 m) on August 26, 5,906 ft (1,800 m) on September 24, and 10,335 ft (3,150 m) on September 30 in the Gulf of Naples, off the island of Capri and in the Tyrrhenian trench south of the island of Ponza. A few months later on February 15, 1954, the FNRS-3 crewed by Huout and de Willm set a new record of 13,287 ft (4,050 m), 120 miles southwest of Dakar.
This was the beginning of research dives and the two bathyscaphes specialized in different ways. The FNRS-3 mainly pursued zoological studies, while the Trieste specialized more in research into physical oceanography, especially acoustic measurements. In 1958 the United States Navy acquired the Trieste and improved and redesigned the cabin. The new bathyscaphe crewed by Jacques Piccard and Don Walsh reached a depth of 35,814 ft (10,919 m) in the Marianas Trench in the Pacific Ocean on January 23, 1960. This is the greatest depth a living human being has ever reached.
Development of unmanned devices to collect samples and record images and data at great depth has gradually replaced crewed bathyscaphes. The feats of the Piccards have long been surpassed, but they will long be counted among the 20th century's greatest dreamers and creators.
81 Benthic life grows on any support available and colonizes it rapidly, as shown by this wreck in the Pacific off Port Moresby in southern New Guinea.
[Photo: K. Deacon / Auscape International]
82 Animals in benthic systems have developed a range of feeding techniques. Ascidians, or sea squirts, (upper photo) are filter-feeding prochordates like this colonial estielid (Botrylloides magnicoecum) on Seal Rocks, New South Wales, southeastern Australia. Individual organisms form groups called coenobia, which share a common tunic (in this case yellow) and a common cloacal space, and these coenobia then form larger colonies. The photo clearly shows the turquoise blue buccal syphons between the tunics of the different coenobia making up the colony. It also shows some of the cloacal spaces into which the anal syphons of the individuals of the colony lead. The lower photo shows a starfish, a member of a group of macrophagous carnivores that often eat prey about as big as themselves. They have an evaginable stomach that they apply externally to their prey, as this example of Patiria miniata is doing to a sea urchin of the genus Strongylocentrotus off California.
[Photos: Becca Saunders / Auscape International & Norbert Wu Photography]
83 Algae of the genus Padina are common in tropical and sub-tropical seas. In the Mediterranean Padina pavonica is one of the most abundant algae, especially in summer in shallow water.
[Photo: Juan Carlos Calvin]
84 Profile of light loss and decreasing color intensity with increasing depth. The light is extinguished much more quickly in productive, and thus turbid, water than in pure, infertile waters.
[Drawing: Jordi Corbera, bas-ed on several sources]
85 Halimedia incrassata is a chlorophycaceous alga that only grows in warm waters, such as those off Crane Point, Florida, where the photo was taken. [Photo: Enric Ballesteros]
86 Variations in trophic strategy and environmental factors relative to the marine benthos as a function of depth. Note that seasonal variations in temperature, nutrient availability, and the existence of particulate organic material are as great, or greater, than these variations with depth.
[Drawing: Editronica, from several sources]
87 Among the most notable dwellers of the kelp forests of the North American Pacific coast are the sea otters (Enhydra lutris), formerly hunted for their pelts. The photo shows one surfacing among the phylloids of Macrocystis in Monterey Bay, California.
[Photo: Norbert Wu / Planet Earth Pictures]
88 Conceptual model of the relations between kelp, sea urchins (Strongylocen-trotus), and mussels (Mo-diolus), drawn by Witman. As has been shown by removing the sea urchins from their natural habitat, their grazing has negative effects on the kelp (1) because it reduces the lower level of its distribution. The relationship between (Modiolus) and (Strongylocen-trotus) shows positive feedback (2 and 3). The mussel provides shelter for the sea urchin from its predator, while the sea urchins consume the kelp installed on the mussels, favoring the persistence of the mussels in case of storm (they are easily dislodged if covered with kelp). The relationship between Modiolus and Strongylocentrotus is thus an example of mutualism, as both species profit. Kelp recolonizes storm clearings quickly, but mussels recolonize slowly. This means that, depending on grazing pressure, Modiolus loses space to the recolonizing alga.
[Drawing: Jordi Corbera]
89 The proliferation of sea urchins (Strongylocentrotus) caused by the indiscriminate hunting of their predators, such as the sea otter (Enhydra lutris), has led to the disappearance of extensive areas of kelp "forests" of Macrocystis and Nereocystis on the Pacific coasts of North America. Similar phenomena are occurring in other parts of the world, although the causes of this proliferation of sea urchins are not yet understood.
[Photo: Norbert Wu Photo-graphy]
90 Attractive cleaner shrimp are frequent in the benthic communities of the Antilles Sea. These small crustaceans eat ectoparasites and bits of half-shed flesh from some fish, so their relationship is one of mutualism. Normally, they are hidden in cracks in rocks or reefs, showing only their antennae in order to attract possible "clients." The photo shows Stenopus hispidus in a population of the tunicate Clavelina picta in Pelican Cays, Belize.
[Photo: WWF / Tony Rath / Still Pictures]
91 The relationship of mutualism between hermit crabs and sea anemones is well-known. The photo shows a hermit crab (Dardanus calidus) and Calliactis parasitica. The crab is protected by the anemone on the shell within which the crab hides its soft abdomen. The anemone benefits from the crab's mobility and so can exploit the soft seafloor where it would otherwise be unable to establish.
[Photo: Juan Carlos Calvin]
92 The ability to occupy all available surfaces is one of the most unusual characteristics of sedentary benthic organisms. This beautiful photo shows submerged rocks in the Red Sea absolutely covered with alcyonarians and other anthozoans, turning this space into an explosion of life.
[Photo: Ron & Valerie Taylor / Ardea London Ltd.]
93 Distribution of macrofauna biomass in the oceans, in grams fresh weight per square meter.
[Drawing: Editronica, based on original by Zenkevitch, 1971]
94 Well-lit ocean bottoms close to the surface of cold and temperate seas have dense populations of seaweed. Kelp dominates in nutrient-rich waters but other phaeophytes (Cytoseira, Sar-gassum) occupy these environments in oligotrophic seas. The photo shows a community of Cytoseira mauritanica on the seafloor off the island of Alboran, in the Mediterranean near the Straits of Gibraltar.
[Photo: Enric Ballesteros]
95 Trophic relations be-tween the organisms living in the abyssal benthos at the bottom of the deepest oceans. Drawing: Jordi Corbera, from several sources]
96 The main marine angio-sperms. Except for Phyllo-spadix, which grows on rocky substrates, they all form underwater meadows on the sandy floors of oceans and seas throughout the world: Thalassodendron ciliatum, Thalassia testudinum, and Halophila ovalis in most tropical oceans and seas; Zostera marina in temperate waters (see fig. 227) of the northern hemisphere; Phyllos-padix scouleri is less frequent but is found in the temperate waters of both hemispheres; and Posidonia oceanica, which is endemic to the Mediterranean.
[Drawing: Jordi Corbera]
97 The growth of a colony of Posidonia over hundreds of years brings the mass of plants nearer to the surface. It may even form a veritable barrier. The photo shows a barrier of Posidonia in the port of Addaia, on the island of Minorca.
[Photo: Enric Ballesteros]
98 The leaves of Posidonia when observed closely are seen to be the habitat of many epiphytic organisms, mainly algae, hydroids, and bryozoans.
[Photo: Juan Carlos Calvin]
99 The meadows of marine angiosperms are veritable oases in the sandy seafloor. They are very productive communities, especially rich in fish, polychaetes, and other animals. The photo shows a Mediterranean meadow of Posidonia oceanica with schools of fish, (sparids and serranids) and by a tubicolous polychaete, the spiral tubeworm (Spirographis spallanzani), with its branchiae extended.
[Photo: Juan Carlos Calvin]
100 The Macrocystis communities of the coast of California seen from within recall a tall, dense, and shady forest (the stipes can reach to 131 ft [40 m] in height). The similarity is even closer if we analyze its structure, characterized by the presence of many animal species in the "canopy" (sea otters, for example), on the substrate (hidden fish, sea squirts, echinoderms, mollusks, sponges, cnidarians, etc.) and in the intermediate levels (fish swimming among the stipes, red algae, grazing sea urchins). Especially in the spring, filamentous algae, hydroids, and bryozoans are common on the fronds, or phylloids.
[Photo: Norbert Wu Photo-graphy]
101 The air bladders at the base of the phylloids of the stipes of Macrocystis prevent them sinking and keep them as close as possible to the water surface and the light when the tide completely covers the kelp "forest."
[Photo: Norbert Wu Photo-graphy]
102 The laminaria "forests" of the European shores of the Atlantic also look like submerged forests, although they are not as well-known as those of Macrocystis on the northeast shores of the Pacific. The photo shows Saccharhiza polyschides, which forms small "forests" along the temperate coasts of the eastern Atlantic, always in shallow water (less than 34 ft [10 m]).
[Photo: Juan Carlos Calvin]
103 The community of suspensivores on hard substrate like this coralligen off the island of Cabrera, in the western Mediterranean, is exceptionally rich in organisms and remarkably beautiful. Apart from gorgonians, in this case Paramuricea clavata, these ocean bottoms are colonized by many sponges, bryozoans, madrepores, sea squirts, and polychaetes.
[Photo: Enric Ballesteros]
104 This hard seafloor near the island of Lanzarote, in the Canary Islands, is not as rich as the one in the previous photo, although it is also an example of a community of suspensivores on this type
of substrate. The scene in the photo is dominated by black or antipatharian corals (Antipathes wollastoni) and sponges (Axinella).
[Photo: Enric Ballesteros]
105 The relative poverty of the soft seafloor of the platform is clearly shown in this photo of an area off the island of Cabrera, in the western Mediterranean. The only macrofauna visible consist of sea cucumbers (Holothuria), which feed on the detritus accumulated in the sediment. These areas are, however, very rich in organisms living buried within the sediment and can easily be missed.
[Photo: Enric Ballesteros]
106 The cryptic coloration of flatfish, such as this six-eyed sole (Dicologoglossa), allows them to pass unnoticed when they are immobile on the soft seafloor that is their habitat. Only the eyes and the undulation of the fins reveal this western Mediter-ranean small sole to the observer.
[Photo: Juan Carlos Calvin]
107 The megafauna is typically scarce on the bathyal and abyssal ocean bottom, although in some places benthic crustaceans, such as these shrimp (Pandalis borealis), are present in large numbers.
[Photo: P. Morris / Ardea London Ltd.]
108 Fringing reefs around some small forested Palau Islands in the tropical Pacific (see also figure 110 of this volume). In this panoramic aerial photograph, the transparent waters reveal a series of underwater reef formations around submerged rocks.
[Photo: WWF / D. Faulkner / Still Pictures]
109 The world distribution of Madreporarian reefs. The influence of cold currents on the western seaboards of the world's continents is obvious from the distribution of hermatypic Madreporarians, much more common on the world's eastern seaboards.
[Map: Editronica, from various sources]
110 Kayangel atoll in the northern Palau Islands, Micronesia (see also, figure 108 of this volume). The circular shape of the reefs around the central "lagoon" is clear, although only a few fragments of reef break the water's surface and enable terrestrial vegetation to thrive.
[Photo: Douglas Faulkner / AGE Fotostock]
111 The distribution of the number of hermatypic coral species in relation to depth and other environmental parameters. The only parameters with comparable distribution models are light and radiant energy, showing how much Madreporarian corals (or more accurately, their symbiotic zooxanthellae) depend on light.
[Graph: Editronica, according to Stoddart]
112 Coral diversity at just 10 ft (3 m) depth on the Trou d'Eau Douce reef on the island of Mauritius. The most common and most visible forms in the photo are Acropora. The few colonies of Fungia can be recognized by their similarity to the "gills" (lamella) on the underside of many mushrooms. The photo also shows some butterfly fish calmly swimming among the irregular shapes of the coral reef.
[Photo: Enric Ballesteros]
113 The flamingo's tongue (Cyphoma gibbosum) be-longs to the Ovulidae family of sea snails. Despite its smallness, it is a fearsome predator of Caribbean Gorgonia corals.
[Photo: Norbert Wu Photo-graphy]
114 "Coral bleaching" is a response to abnormal physiological conditions, such as periods of exceptionally high water temperatures. The polyps expel their zooxanthellae and as a result, the coral tissues turn pale as can be seen in this Madreporarian Agaricia agaricites in the Caribbean. If environmental conditions improve, the symbiotic algae will return to the polyps. If not the coral will die, as it has lost the food supply provided by the zooxanthellae.
[Photo: Norbert Wu / Still Pictures]
115 A large (approximately 3 ft [1 m] in diameter) cup-shaped Xetospongia on a coral reef in the Red Sea. The small forked-tailed orange fish are Anthias squamipinnis, the Red Sea goldfish, common in warm waters as well as around coral reefs.
[Photo: D. Parer & E. Parer-Cook / Auscape International]
116 Not all corals that live on reefs are hermatypic: there are also soft Octoco-rallians such as these Xenia from the Red Sea, some with their eight tentacles extended and others with them retracted.
[Photo: Peter Scoones / Planet Earth Pictures]
117 Polyps of a Hexa-corallian of the genus Favia on a southern section of Australia's Great Barrier Reef. The photograph shows the polyp at night with its feeding tentacles extended. Hexa-corallian skeletons have created the great coral reefs found in tropical waters.
[Photo: L. Newman & A. Flowers / Auscape Inter-national]
118 The characteristic grooves of brain coral (Platygyra) is because the coral colony's polyps do not separate completely when they divide. The photograph shows P. meandrina at a depth of 33 ft (10 m) near Hurghada on the Egyptian coast of the Red Sea.
[Photo: Manuel Ballesteros]
119 Zooxanthellae in a Madreporarian coral. These symbiotic algae play a fundamental role in the biological activity of corals. Those areas with the highest concentrations of algae are the most fluorescent.
[Photo: D. Parer & E. Parer-Cook / Auscape International]
120 This apparently inoffensive hydrozoa is a fire coral (Millepora platyphylla) which in some areas of the Red Sea forms Millepora distinct zones of coral reefs. The stinging cells of the fire coral are especially strong and may cause very painful burns to anyone touching them.
[Photo: Rafael Al Ma'ary / Bios / Still Pictures]
121 The cilia on the tentacles of this polychaeate (Spirobranchius gigantus) add a touch of color to Heron Reef on the Great Barrier Reef.
[Photo: L. Newman & A. Flowers / Auscape Inter-national]
122 Many gastropods feed on the living tissues of corals and Madreporarians on reefs. This is this case of the porcelain Diminovula punctata shown in the top photograph feeding on a soft coral Gorgonia ventalina on an Indonesian reef. In the lower photograph a juvenile form of the nudibranch Hexabranchus sanguineus, known in Australia as the Spanish Dancer, is feeding on coral (see also figure 113).
[Photo: Dave B. Fleetham / Natural Science Photos and L. Newman & A. Flowers / Auscape International]
123 Reef crinoids or feather stars such as this Astrophyton muricatum from the Caribbean Island of Santa Lucia are mainly nocturnal. These echinoderms leave their daytime hiding crevices and stir up the water with their arms, propelling their minute zooplankton prey towards their mouths.
[Photo: Allan Smith / Natural Science Photo]
124 Sticky filaments produced by the Cuvier tubes and expelled through the anus are used by many Holothuroidae such as this Bohadschia argus from the Australian Great Barrier Reef as a means of defense.
[Photo: Andrew Fraser / Auscape International]
125 The crown of thorns starfish (Acanthaster planci) is one of the most fearsome of all the predators of madreporaria. The photograph shows the effect it has on coral: the polyps have been devoured in the white strip on the right, while on the left the polyps in the coral are as yet untouched.
[Photo: Enric Ballesteros]
126 Among the numerous sea urchins of the world's coral reefs Heterocentrotus mammillatus is one of the most spectacular. Its thick, long spines have earned it the name of "slate pencil urchin" in the Hawaii Islands where this photograph was taken. It is also known as the "wind chime urchin" due to the use made of its thick, round spines.
[Photo: Norbert Wu / Still Pictures]
127 All but invisible within the polyps of an Indo-Pacific Octocorallian, a reef ophiurid twirls its delicate arms among the branches of a Madreporarian.
[Photo: Ron & Valerie Taylor / Ardea London Ltd]
128 Periclimenes yucatanicus is a typical Caribbean coral reef cleaning shrimp. The photograph taken off the coasts of Bonaire in the Dutch West Indies depicts a female with eggs inside the sea anemone that shelters it.
[Photo: Hal Beral / Natural Science Photos]
129 The 18 different Myripristis species are named soldier fish because of their habit of moving in compact formations. This photograph shows a shoal in the Rangiroa atoll in the Tuamotu islands in the Pacific. These nocturnal fish are common in all warm seas, especially coral reefs.
[Photo: Yves Lefevre / Bios / Still Pictures]
130 The cracks and crevices of coral reefs are excellent hiding places for fish such as this moray eel (Gymnothorax meleagris) photographed off the coast of Hawaii.
[Photo: David B. Fleetham / Natural Science Photos]
131 The Scaridae or parrotfish are notable for a number of features. They are dramatically colored, have a very peculiar mouth and make a loud noise as they rasp coral. One of their most remarkable characteristics, as seen in this photograph of a Scarus, is the mucus sac they secrete as a defensive mechanism before they sleep in cracks in the coral reef.
[Photo: Kurt Amsler / Jacana]
132 Despite its impressive appearance, this manta (Manta) swimming majestically through the waters of Lady Elliot Island in the Australian Great Barrier Reef, is not a ferocious predator but a plankton filter feeder. A few cleaner wrasse (Labroides dimdiatus) swim around its untoothed mouth feeding on the manta's ectoparasites.
[Photo: Ken Hoppen / Natural Science Photos]
133 The many different species of grouper such as this Mycteroperca photographed at rest on a Diploria coral in the Saba Bank near St. Kitts in the Lesser Antilles are among the coral reef's most notable predators. Large, tasty and brightly colored, they are highly prized and hunted by divers.
[Photo: Norbert Wu / Still Pictures]
134 The scorpionfish Diodon holacanthus has a very effective strategy to repel predators: inflating itself with water like a balloon, and turning its perpendicular spines into an armed globe. The picture shows a half-inflated scorpionfish in a coral reef in the waters off the island of Flores, Indonesia.
[Photo: David B. Fleetham / Natural Science Photos]
135 Elegant despite their ungainly appearance, these dugongs (Dugong dugon) are among the largest members of the delicate tropical marine fauna. This female and her calf are swimming in the waters of Shark Bay (Western Australia).
[Photograph: Ben Cropp / Auscape International]
136 Hatchetfish are typical mesopelagic fish. Like this Argyropelecus pacificus they have luminescent organs (photophores) that produce light by chemical processes (the oxidization of luciferin by luciferinase). They are small reddish fish from 2-3 in (4-8 cm) long.
[Photo: Norbert Wu Photo-graphy]
137 The enormous mouth, articulating the jaw, cranium and spinal column so it can open very wide, is typical of abyssal fish, such as Meleno-cetus johnsoni, 5 in (12 cm) long. Note the numerous sharp teeth and the frontal fishing rod-like appendage, bearing a photophore at its tip to attract prey.
[Photo: Norbert Wu Photo-graphy]
138 An even more disproportionately large mouth in comparison to its body is that of Euripharynx pelecanoides, another remarkable abyssal fish (24 in [60 cm] long, on average), that has the further distinction of being the only known teleost to have five gill arches and six visceral slits.
[Photo: Norbert Wu Photo-graphy]
139 A view of a hydrothermal oasis in the Pacific. This was photographed during an expedition using equipment adapted for use at extreme depth and shows the cushion-shaped seafloor lava flows covered in groups of bivalves Bathymodiolus and vestimentiferan worms Riftia pachiptila in the depressions, and some crustaceans higher up. In the foreground in the lower part of the image, the tubes of a group of vestimentiferans are visible, some showing the highly vascularized branchiae, reddish in the photo.
[Photo: Ken Smith / Norbert Wu Photography]
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|Publication:||Encyclopedia of the Biosphere|
|Date:||Oct 1, 2000|
|Next Article:||Clownfish and other artists.|