2 Pelagic life.
1.1 Life in the pelagic space
The pelagic environment covers approximately 70% of the planet's total surface (139,768,409 sq mi or 362 million sq km) with an average depth of 12,238 ft (3,730 m), and thus occupies a volume of approximately 1,350 million [km.sup.3], making it the largest environment on Earth.
From plankton to nekton
In a terrestrial ecosystem, the most important primary producers occupy fixed positions and many animals move in only two dimensions. The entire depth of the sea's water layer is inhabited, from the surface to the seafloor, and even within the sediment. Some of its inhabitants are suspended in the water, either swimming or drifting, and are called pelagic organisms. These organisms form part of ecosystems that are also called pelagic or, in other words, belonging to the open or high seas. These ecosystems show a significant degree of indeterminacy in the position of the individuals that interact in them and there is a considerable gradient of possibilities, ranging from those that seem to occur at random, such as interactions between non-mobile planktonic organisms, to ones showing greater determination, such as the pursuit of a mobile alga by a swimming animal.
The benthic organisms and ecosystems, which form the benthos, are distinguished from pelagic ones as they are close to or associated with the ocean bottom, whether rocky or sediments. This distinction is highly artificial, given that many pelagic species deposit their eggs on the bottom and many benthic species release their eggs and thus--together with their larvae--form part of the plankton until a relatively advanced stage of their metamorphosis. Furthermore, many pelagic organisms interact with the seafloor and many benthic organisms leave the substrate and make regular incursions into the water column. In practice, however, there is agreement that pelagic species are those whose adult forms normally live above the seafloor, within the water column.
Pelagic organisms are subject to the general properties of the marine environment: its fluidity and instability; the easy conduction of dissolved materials, including nutrients and externally diffused active substances (pheromones); and the propagation of compressional (pressure) waves. These organisms also experience turbulent movements, superimposed on a more regular and persistent circulation and stratification effects, caused basically by the absorption of solar radiation. The raised specific heat capacity of water and its movement mean that local temperature differences are not as marked as on the surface of the continents. It should be remembered that raising the temperature by 10[degrees]C roughly doubles the rate of most biochemical reactions (for example, respiration, in a negative sense), while photosynthesis (in a positive sense) is much less affected. As a general conclusion, lower temperatures favor relatively higher net production, as long as the water does not freeze, something that only happens on a very local scale.
A question of size
Pelagic organisms come in all sizes. Some of them could more appropriately be called semi-organisms, such as viruses, many of which have been found in ocean water in great numbers, attaining concentrations of 104 to 107 per ml. Bacteria are also widely distributed, although most are not very active. If they were, they would use a lot of organic nutrients and deplete the oxygen in the masses of deep water. Large whales are at the opposite end of the scale of size. The blue whale (Balaenoptera musculus)--which can reach 108 ft (33 m) in length, 130 tons in weight, and whose speed ranges from 7-23 mph (6-20 knots)--is surely the largest animal that has ever existed on this planet, the original Leviathan.
The range in size thus covers nine orders of magnitude. The name plankton is given to the essentially passive components of this world in suspension, a group whose limits have never been rigorously defined, although one criterion is that they are always at the mercy of the water movements. In short, plankton, as its etymological derivation suggests, drifts. Within the pelagic environment, plankton is distinguished from nekton, free-swimming animals that move at will in their environment, by its obvious limitations.
Plankton for study was first collected using fine nets. It seems that the first scientific samples were made by Vaughan Thomas (1779-1847) in the Irish Sea (1828) and Johannes Muller (1801-1858) in the Bay of Heligoland (1844). Plankton nets or filters were for a long time made from the same silk nets that were used for sieving flour, and so it was industrial considerations linked to the quality of the flour, rather than strictly scientific ones, that determined historically the distinctions between different groups of plankton. The smaller plankton, the microplankton, that account for much of the mass of the autotrophic plankton, was retained by the finest nets used, with a theoretical pore size of 40 [micro]m.
The scientific community soon realized that even smaller organisms were passing through the mesh of the nets, and scientists began to add fixing and preserving agents to the water so the organisms were killed and preserved virtually without deformation. The sedimented, dead plankton was examined using a microscope with a special apparatus that allowed the plankton to be viewed and counted from below (the Utermohl or inverted microscope). This led to the creation of the additional category of nanoplankton. Techniques for fixing the materials in the best conditions for observation, as well as collection techniques, have improved. Most fixatives have been suggested for some specific purpose, but often present certain disadvantages. For a long time the agents used were hot corrosive sublimate (mercuric chloride, HgCl2) or formalin. Nowadays, sedimented plankton is widely studied using a solution of iodine, and there are many very effective fixatives for specific purposes.
Mechanical devices are now available with optical or electromagnetic detectors that count the successive particles that pass through a narrow orifice and divide them into categories, originally on the basis of size and now also according to their fluorescence properties. The final category, the picoplankton or ultraplankton, was defined when the use of fluorescence or stains revealed the smallest organisms, such as heterotrophic bacteria, cyanobacteria, and other autotrophic bacteria. These distinctions and nomenclature are only worth retaining so long as they are still useful. This question is of historical interest because it shows how the importance attached to the different groups has changed as ever smaller organisms were identified.
1.2 The movements of pelagic organisms
Drifting in the water or moving at will may, from a certain size upwards, depend on the relative power attained by their organs of movement at the end point culmination of a particular evolutionary trend. A large jellyfish and an eastern Atlantic scad (Trachurus trachurus) are similar in size, but different enough for some sort of comparison to be made. Drifting or independent movement also depends on the local water movements, and on whether there are important currents with peripheral eddies, or whether the range of turbulence is restricted to minor fluctuations without any clear prevailing direction. These factors largely depend on the arrangement of the large water masses due to movements of the liquid, down to the smallest scales.
Moving at will or drifting
Superimposed on the more or less regular turbulent agitation of the medium, the trajectory followed by each individual can be considered as an example of a "random walk." This is basically the result of breaking a trajectory of a hybrid nature down into its basic steps. They are sometimes partly determined by the organism's own movement--down to nil--but are always partly determined by the influence of the complex range of different forms of turbulence, ranging from agitation to the circulation of the water. In more "scientific" terms, any part of the trajectory can be described so that the distance traveled, L, between its starting point and its finishing point, expressed in the number of elemental steps, N, is equal to a (reasonably small) number of elemental steps, N, raised to an appropriate power between 0 and 1; thus L = [N.sup.k] (where 0 < k < 1). In three dimensions, k may have three components, corresponding to the x, y, and z coordinates ([k.sup.2] = [k.sup.2.sub.x] + [k.sup.2.sub.y] + [k.sup.2.sub.z]). The vertical component [k.sub.z] is probably the most determinant of these, and the most important from the point of view of biology and evolution. This vertical component is perceived everywhere, and vertical migration may occur wherever there is a light gradient, even in water showing isotropic turbulence, not to mention the perception of the direction of gravity. These trajectories will also be influenced by the presence of other organisms of the same or different species, which will be perceived either as a gradient of attractive or repellent substances or as mechanical deformations in the liquid. Natural selection may have acted on the generation of these gradients, introducing factors that disorientate or confuse potential predators. The question of the distinction between plankton and nekton leads, if one wishes, to comparing the size and locomotor capacity of each organism with some of the small-scale mechanical properties of water, such as those seen in viscosity and in the range of turbulence effects. An organism's autonomous capacity for movement depends on its size, and in small organisms, on its degree of adherence to the immediate strata of water. The properties of the contact between liquid and solid are not only important in locomotion but also in the exchange of fluids and the effectiveness of organs that mechanically filter food particles.
The Reynolds number ([R.sub.e] = rVL/[micro]) is a good guide to how "planktonic" an organism is. This is a dimensionless number combining a measurement, L, considered as a characteristic of the organism (such as its largest dimension), multiplied by its velocity, V, with respect to the water (almost zero in passive organisms), and where r is density and [micro] is the kinetic viscosity of the water, expressed in poises (1 poise is equal to 10-1 N s m-2). The Reynolds number is much less than 1 for a phytoplankton cell that sinks slowly. Values up to 200 are found in laminar flows, while Reynolds numbers greater than 2,000 are found where flow is clearly turbulent. If it is 500,000 or more, the organism is a large fish. This parameter thus allows us to distinguish between different situations: plankton proper, which shows greater adhesion to the water and is its slave, to such an extent that the strata in contact with small organisms are renewed only with difficulty and always by sliding; small active swimmers, such as dinophytes and the nauplius larvae of copepods; and the true nekton. The higher the Reynolds number, the more noticeable the series of eddies and perturbations the organism leaves behind it that can serve--to its detriment--as a guide or track for predators. The use of different mechanical methods for dealing with the surrounding fluid is thought to be of defensive importance because they are an attempt to throw predators "off track" by reducing eddies, or by making them deviate, thereby deceiving the predator.
Neither plankton or nekton
The Sargasso Sea houses a special community, an example of what botanists call pleuston (creatures that are neither planktonic nor nektonic), that consists of free individuals of at least two species of Sargassum of Atlantic-American origin. These algae continue growing close to the surface at the center of the North Atlantic anticyclonic gyre, thanks to the buoyancy of their air bladders. A more complex kind of life with interesting, or even spectacular, biological relations depends on the sargasso. Toxic dinophytes frequently grow on the it, making its consumption dangerous. Some animals in this unusual community adopt an appearance similar to the alga, and this mimicry of the sargasso may thus provide them with some protection. The density of Sargassum in the regions where it accumulates does not usually exceed 0.6 to 1.6 g per square meter.
Another type of community, comparable to phytoplankton, consists of the organisms in the polar ice in the saline liquid between the grains of ice making up the polar pack ice, which, as a mass, behaves like a plastic material. They are microscopic algae that are partly the same as those of plankton, partly algae of the same groups, but whose behavior is more benthic (Amphiprora, Frustilia, etc.) and are similar to some species that also live on the sand of beaches or littoral sediments.
Making sure of permanence
Just as in a river every population eventually multiplies locally in a way that adjusts to the risk that its members run of being eaten or carried away, so in exactly the same way in plankton the rate of reproduction and the probability of sinking from the initial level eventually reach some sort of balance. In passive phytoplankton, a fraction of the population is continuously being lost, and it is essential that conditions are present (light, nutrients) that allow sufficient reproduction for populations to persist. However, those species whose members can maintain themselves at a specific level, for example by swimming, and have some defense against potential predators, can thus "negotiate" within the eternal bargaining of natural selection some reduction in the rate of reproduction required to maintain their populations. A broader point of view would relate the time needed for the renewal of the population or for the persistence of ecosystems (from days to weeks in the phytoplankton, and years or centuries in a forest) to the time that sets the framework within which can be described the important changes or deformations that occur in their physical medium (from minutes to years in the oceans, from decades to million of years on the continents).
Planktonic populations, especially autotrophic ones, are highly transitory. Furthermore, the sea's structure is very complex, at all scales, from the global to the small discrepancies and vortices that appear in measurements taken continuously from a vessel or buoy, whether drifting or under power. Discontinuities are maintained between different and/or confluent volumes or masses of water if there is a renewal of either or both of the water masses in contact. Under these conditions it is probable that interesting things, such as an increase in production, will occur. A three-dimensional interpretation and explanation of distributions should be sought that is compatible with the lineal information obtained from exploratory transects. Nowadays, this is complemented by remote detection from space. The distribution of plankton is not random and its organization can be interpreted at all scales of space and time.
The productive zone is a relatively thin surface layer, but a good part of the phytoplankton sinks and is consumed at depth. Migratory zooplankton is very effective at bringing about a relatively uniform and constant redistribution of the few morsels of nourishment in the form of plankton that reach the inhabitants of the great depths. The ocean is an example of an ecological system whose activity is maintained by a relatively sparse surface layer, and which is only about one hundredth of the thickness of the water whose life it sustains. This means that the return pathway of the chemical elements will be difficult, and total recycling slow. This alone would be enough to understand why marine primary production is, per unit area, only about a third of that on the continental surfaces. Moreover, only about 5% of total marine primary production can be attributed to the coastal benthos.
2. Primary producers: the phytoplankton *
2.1 Phytoplankton organisms
Phytoplankton consists of unicellular autotrophic organisms and also includes others that are clearly derived directly from autotrophic organisms, even if they are clearly totally or partially heterotrophic. They are small (generally between 2 and 200 microns and occasionally more then 1 micron) and in many species, the cells, although still autonomous, form chains or filaments, sometimes covered in mucilage, that may be visible to the naked eye.
Cyanobacteria and protochlorophytes
The smallest members of the photosynthetic plankton are the cyanobacteria (formerly cyanophytes or "blue-green algae"), prokaryotic organisms that are usually round (Synechocystis) or elongated (Synechococcus), and approximately 1.5 microns in diameter, or less. These organisms are slaves to the viscosity of the water, and can only renew the few micrometers of water around them with great difficulty. If they are actively sought, they are found almost everywhere, in concentrations that may reach hundreds of thousands of cells per milliliter, although densities are normally much lower. Preliminary studies exaggerated their role in total primary production, although they may account for between 20-40% of the total (often less), depending on their greater or lesser local abundance. Their nature and persistence means they are found almost everywhere, in a more or less inactive state, in a great depth of water, ready to photosynthesize when the water reaches sunlit levels. These organisms may be consumed, together with other bacteria, by relatively abundant and diverse small heterotrophic flagellates in the plankton.
The pigments of cyanobacteria are found on thylakoids at the edge of the cell and not in discrete chromatophores, and this gives the cells a diffuse color. They contain chlorophyll a and several phycobilins and carotenoids. These phycobilins confer on them the distinction of being the only members of the phytoplankton that can photosynthesize using the radiation in the intermediate band of greenish light. In addition to the cyanobacteria, there are other prokaryotic organisms in the photosynthetic plankton that, given their small size, (between 0.6 and 0.8 microns) look similar but possess chlorophyll b. They are protochlorophytes, also found throughout the oceans. Their organization has been compared to that of a plastid surrounded by a cell wall.
In freshwater, cyanobacteria with larger cell sizes--and thus an organization even further removed from that of other prokaryotes--are common and diverse, although this is not the case in the sea, except for some of the less saline areas of the Baltic Sea. One of the few exceptions is the genus Trichodesmium, which forms long filaments joined together in bundles and is especially frequent in stratified tropical waters, usually outside or on the edge of upwellings. It has been stated, although not universally accepted, that this organism, like most other cyanobacteria, can fix atmospheric nitrogen. Obviously, the insignificant presence of these cyanobacteria in the open seas must be considered evidence that nitrogen is not a major limiting factor in the open ocean. On the contrary, these cyanobacteria thrive in fresh water undergoing denitrification and rich in phosphates, situations brought about nowadays mainly by human activity.
The filaments of Trichodesmium are visible to the naked eye, and support other organisms, such as hydrozoans and even fungi, which potentially make them a kind of pelagic lichen. The masses break up quickly when the water is agitated, and when the filaments separate they are no longer visible. Richellia forms short filaments, generally with a heterocyst (a differentiated nitrogen-fixing cell) at one end, and they are usually found as internal symbionts within larger diatom cells.
Dinophytes (or Pyrrophyta, Dinophyceae, Dino-flagellata or Dinomastigota) ** are eukaryotic, but with an unusual, especially primitive nucleus whose chromosomes lack histones and are permanently condensed. These chromosomes are usually clearly visible during the interphase of division and make the nucleus look like a ball of string, possibly a useful character when identifying unknown cells. Different species show differing levels of polyploidy and may show polymorphism in size, with an apparent increase in the frequency of larger cells during the cold season.
The organization of the dinophytes is extremely varied; they form a group with a remarkable evolutionary capacity, and are probably the oldest of the forms that now dominate the plankton. However, they have not developed true multicellularity. They could be considered as a potential phyletic lineage that aborted, probably because other forms of organization (i.e., the true eukaryotes) arrived first. The few forms that have attained some form of multicellularity are parasites of planktonic animals, such as copepods and tunicates.
The dinophytes as a whole now show a very wide functional range that is more diverse in the seas than in freshwater. They range from autonomous photosynthetic organisms that normally possess flagella, to large cells 0.5 microns that behave essentially like animals. The genus Noctiluca even ingests "higher" animals, such as tunicates or the eggs of anchovies. The most primitive--and most common--dinophytes possess chromatophores with chlorophyll a and c and carotenoids (peridinin and other specialized compounds). They are generally yellowish green or brownish green in color, but the blooms of some species appear reddish ("red tides").
The cells of dinophytes are always asymmetric. The commonest shape in the most numerous families consists of an equatorial girdle twisted at the ends (forming a right- or left-handed helicoid) that meets or intersects with another longitudinal girdle (the sulcus or groove). The bases of two more or less differentiated flagella are located where the two grooves meet. Pseudopods of clear cytoplasm may form in this special region and are either linear or take the form of a large feeding membrane for extracellular digestion. This region is also where the intracellular cavities (pusules) open. Other advanced features are found in some dinoflagellates, such as ocelli, which are able to perceive light, and tentacles of varying maneuverability. Many species are capable of emitting light, often through specialized organelles (scintillons).
Very potent specific toxins that vary greatly in their chemical composition and produce ill effects on some animals, are produced by many dinophytes, including the planktonic genera Prorocentrum, Dinophysis, Gonyaulax, Alexandrium, Pyrodinium, as well as Gambierdiscus and some forms of Prorocentrum that live on Sargassum, on other macroscopic marine algae and even on grains of sand. These varied compounds (such as saxitoxin) are molecules with rings containing nitrogen, and a molecular weight that is normally greater than 1,000 daltons. These substances may reach human beings (see p. 239) via the organisms that eat them, usually lamellibranchs (food poisoning as a result of eating mussels or clams) or fish ("cigatuera fish poisoning" in some tropical countries). Some, such as Cochlodinium, form rod-shaped bodies (trichocysts) of different sizes that can be rapidly extruded and form sticky filaments (possibly also poisonous) that stick to and harm the gills of fish.
The surfaces of dinophyte cells have variably shaped covers, ranging from simple membranes, to complex structures consisting of several different plates joined by complex sutures. Sometimes the cover includes a pre-formed region through which the cell, after adopting a spheroid shape and enclosed within a new relatively thin covering, can abandon the old cover, like a pilot ejecting from a fighter plane. The cell may enter a quiescent state during which its covering becomes thicker and accumulates materials similar, at least in terms of their resistance, to the sporopollenin of the walls of pollen grains and other plant spores. This allows it to be preserved for long periods. In other dinophytes the outside is calcified.
A good fossil record exists for the dinophytes, proof of the group's antiquity; the remains of dinophytes similar to contemporary species are known from the Silurian and similar forms, such as some acritarchs, are even older, dating from the Cambrian period or before (see volume 1, p. 105). Their age is also shown by the fact that the corals (and other marine animals) adopted them as symbionts long ago, at the evolutionary origins of symbiosis. These surprisingly uniform symbionts are generally identified as Symbiodinium pseudoadriaticum. The careful study of symbionts from different hosts shows that the differences between strains are minimal.
Dinophytes or dinoflagellates are found everywhere in contemporary marine plankton and are represented by organisms generally 10-200 microns in size that vary greatly in their forms of feeding. There are more heterotrophic forms than might be thought, with internal feeding (ingestion) and external feeding (the feeding membrane found in many Protoperidinium). They may contain internal or semi-external symbionts (such as the cyanobacterium Histioneis). The advanced assimilation of some symbionts through dinophytes has led to the evolution of chimaeras or mosaic organisms. Dinophytes with heterotrophic nutrition are especially diverse and abundant in the so-called "twilight zone," below the chlorophyll maximum in stratified waters.
The transverse flagellum makes the cell rotate around its anterior-posterior axis. The prefix "dino-" in dinophyte is derived from the Greek root dinos meaning to spin like a top, and not from deinos, meaning terrible, as in dinosaur. The transverse flagellum is normally more robust and often acts against the irregular or flattened shape of the cell. This usually bears a wealth of detail (Ceratium, Dinophysis, Ornithocercus, etc.) although all show an unusual asymmetry. The flagellum's opposing action increases water flow over the cell, leading to increased absorbtion. At the same time, the movement of the longitudinal flagellum allows the organism to maintain itself at appropriate levels of light and nutrient concentration within the water, and even to undertake moderate vertical migrations.
The cryptophytes ***, in a sequence of increasing cell complexity and size, are generally small, normally between 5 and 20 microns, and more or less elongated, asymmetric cells, often pointed at the anterior. Their two flagella emerge from a type of "gullet" and are associated with ejectosomes, "rods" that fire like the trichocysts of dinophytes. They also possess chromatophores with complex pigments, and thus vary in color: greenish, reddish, or even bluish and pinkish forms are found. There are heterotrophic forms, some of unknown descent, such as the very common colorless organism Leucocryptos marina, and others that eat bacteria. It has been shown that many cryptophytes, and maybe all, are really chimeras, or compound organisms, whose former symbionts have been assimilated into the organism.
These organisms used not to be mentioned much in discussions of marine plankton, but they are, in fact, frequent. They are often found forming discontinuous swarms in surface water, often after intense local mixing. The most important genera are Cryptomonas, Rhodomonas and Hemiselmis.
Chrysophyta or chromophytes
Rather than referring to a specific taxonomic group, this catch-all collective name is used here to include, in addition to some less important groups, the groups of haptophytes (including coccolithophorids, diatoms, and silicoflagellates) that will have to be reclassified when they are better known and a consensus has been reached on the affinities of these diverse flagellates, now more widely studied thanks to electron micros-copy ****. In general these organisms have yellowish chromatophores (chlorophyll a and c and fucoxanthin are the basic pigments) that never accumulate starch as a reserve, with differentiated flagella (when present), clear plasma, and a cell covering of small scales rich in structural detail, some of them mineralized, that may extend to varying degrees over the flagella. Their study requires the use of electron microscopy, and for technical reasons reliable information on their distribution is necessarily relatively recent. The diatoms (Bacillariophyta) are included in this group and are relatively large and possess silica covers. As has been known for more than two centuries, this covering, or frustule, consists of two halves (the valves), one of which overlaps the other like the lid on a box. The large size of the cells, the nature of the valves, the absence of flagellate forms (except in some heterogametic forms) and the diploid nature of the vegetative cells has meant that the diatoms have been considered the zygotes of other chrysophytes. They are also relatively more recent; their greatest expansion took place at the beginning of the Tertiary period, and might be related to the development of marine regions with intense upwelling. The diatoms are, in short, post-dinosaur.
The haptophytes or prymnesiophytes
The haptophytes or prymnesiophytes are a group of chrysophytes, quite small in size (10-25 microns) that normally possess two functional flagella, and a third filament (the haptonema) that is often coiled into a spiral. The haptonema's function and structure are unlike that of a flagellum, as they lack the two central and nine peripheral pairs of tubules found in normal flagella (see volume 1, p. 90). The name haptonema suggests they might serve to fix the cell to a substrate, but in some prymnesiophytes (Chrysochromulina) they serve to attract and guide the bacteria they eat, thus making ingestion easier.
Phaeocystis cells may bear flagella, although the most common form consists of very small (2-4 microns) spherical cells immersed in a mucilaginous matrix that may form important masses and block the mesh in plankton nets and even the gills of fish. North Sea fishermen have long known that fish flee from areas where Phaeocystis is abundant. It is regularly found in the Mediterranean, but more frequent or larger blooms occur in colder seas, even in the seas around the Antarctic, where their abundance was thought to be due to the scarcity of bacteria in the digestive systems of the animals that eat material synthesized by them. Phaeocystis and some species of Chrysochromulina are toxic and there was considerable alarm in summer 1988 (and the following years) when a species of Chrysochromulina reached local concentrations of 80,000 cells per micron in the North Sea. The many species in this genus range from the simplest, a few micrometers long, to ones 13 microns or more in diameter.
The most important group of autotrophic and planktonic haptophytes, important primary producers, is without doubt the coccolithophorids, whose cells are covered with scales of calcium carbonate called coccoliths. Most of these cells do not possess functional flagella. There are cases of polymorphism, in other words, alternation between different forms of organization, or at least between forms bearing different scales. The coccolithophorids with the most highly devolved scales (Scyphosphaera, with calcareous scales that look like cut-glass, Rhabdosphaera, Discosphaera, etc.) seem to appear towards the end of ecological successions, when cells divide more slowly and prepare to deposit calcium carbonate, and possibly other related chemical elements. Species that multiply extremely quickly (such as Emiliana huxleyi, without a doubt the most common organism in the marine plankton, and possibly the entire world), have thinner scales (the greater the rate of cell division, the thinner and more easily segregated the scales), and are usually only a few micrometers in size. Consequently, they are difficult to study and identify using a normal optical microscope. More than 80% of the coccoliths that accumulate in the sediments of the Mediterranean are E. huxleyi. Coccolithophorids multiply quickly in appropriate conditions, often close to fronts. It has been said that some water turbulence observed from planes, for example in tidal fronts to the west of the English Channel, is due to the proliferation of coccolithophorids. The presence of calcium carbonate plaques may increase cell density and help them to sink in rising water. They contain carbon that is removed from circulation when the scales or coccoliths sink, thus reducing the greenhouse effect to some extent. Coccolithophorid species are very ancient and widespread, and have changed regularly over geological time, making their fossils suitable for studying the distribution and diversification of plankton types over long periods of time.
Bacillariophyta or diatoms
The other important group of chrysophytes is the Bacillariophyta, or diatoms. Since their discovery, these organisms have attracted attention because of their siliceous covering, often preserved in ancient sediments. The surprisingly detailed and delicate structure of the frustules could be seen with the optical instrumentation commonly available in the 19th century. Studying diatoms became a hobby, the first step of which was to boil the diatoms in acid to clean the frustules. Thus a lot of work has been done on the taxonomy of the group, now possibly over-detailed and with an excessive number of synonyms. The same situation has happened with other organisms, such as the mollusks, which have the good or bad fortune to bear hard parts. Electron microscopy has helped to identify many of the small structures of the frustule, some of which may be of great importance in understanding specific details of the diatom's life. The frustule is not inert, and its complex of pores and chambers may play a significant role in nutrition. It often channels the production of filaments of mucilage that join the cells together or swell to form large mucilaginous masses (Chaetoceros socialis, Thalassiosira). The organic matrix of the frustule deposits hydrated silica (SiO2 x nH2O), or opal, polymerized in the form of a continuous molecular network. Organic material occupies the free valencies, at least in the form of an external film, and prevents the frustules from dissolving in alkaline water that is not saturated in silicon. The siliceous part varies in thickness depending on the species and on the conditions in which it lives; each population shows variation in thickness and silicon is rarely a serious limiting factor. The cells are often only slightly silicified and apparently flexible in marine plankton, especially if the diatoms are growing rapidly or if the silicon content of the water is low (as in the Mediterranean, where alkalinity is slightly higher than the ocean average, and where calcium concentration is also higher). In the Mediterranean, only the thickest frustules are preserved in the sediment, often proceeding from the littoral, as is the case in the widespread Paralia sulcata or the resistant forms (hypnocysts) of Chaetoceros and some other common genera. The valves of freshwater diatoms also frequently reach the sea.
Diatoms are generally large organisms, reaching a size measured in millimeters. They are divided into two main groups: centric and pennate. Centric forms have valves showing radial symmetry, and oogamous reproduction. The pennate forms have elongated valves and their reproduction does not involve forms bearing flagella, but usually shows formation of gametangia that copulate as a whole. There is also Phaeodactylum, a curious organism with just one valve, that is common in pools on rocky shores and thrives in aquaria, but which is only found by accident in the open sea. Most marine planktonic diatoms are centric, mainly belonging to the genera Thalassiosira, Coscinodiscus, Chae-toceros, or Rhizosolenia (now subdivided). The pennates are usually coastal, such as Asterionella, Thalassionema, and Thalassiothrix.
Diatoms used to be considered the marine equivalent of grasses, innocuous and generous producers, with the sole vice of depositing silica. Recently it has been learned that some species of Nitzschia produce potent toxins, such as domoic acid, an amino acid that among other effects may lead to amnesic shellfish poisoning in humans. The cells of some larger diatoms, mainly of the genus Rhizosolenia, which are vacuolate and float in nutrient-poor waters during the summer, house nitrogen-fixing cyanobacteria (Richellia intracellularis). Other diatoms are associated with ciliates that help to maintain them in suspension. Chains of empty cells of diatoms of the genus Dactyliosolen are often found bearing flagellated cells; these have been given the name of Solenicola, but it is suspected that they could belong to the same diatom's life cycle.
Dictyochophyceae or silicoflagellates
The silicoflagellates are medium-sized flagellated protoctists (20-70 microns), with a thin membrane, numerous chromatophores and a highly distinctive internal reticulate skeleton, generally showing four-fold or six-fold symmetry. They are made of tubular structures of silica (opal), which is more compact and is preserved better than the frustules of diatoms. A second skeleton that forms within the cell before division is the mirror image of the existing one, except in some populations that lose their skeleton in periods of rapid growth. Fossil remains have been found dating from the end of the Mesozoic period and their expansion has been parallel to that of the diatoms, although silicoflagellates are very morphologically conservative and species-poor. Among the most common forms, the quadrangular Dictyocha fibula is always slightly more thermophilic than Distephanus (=Dictyocha) speculum.
The true green algae (Chlorophyceae) are freshwater organisms that contain starch, and are colored green by the chlorophylls they contain. In the marine plankton, we find the prasinophytes, a sister group, ecologically parallel to the chlorophytes but distinguished from them by cytological characters *****. There are many species with four equal flagella (Pyramimonas, Tetraselmis) and covered with superficial scales, even on the flagella. Species of the genus Halosphaera have quite large spherical cells (40-100 microns in diameter) that form multiflagellated propagatory cells.
The euglenoids and raphidophytes
The euglenophytes ****** are flagellates with a complex structure, whose cover is made of interlocking elastic strips that allow continuous deformation of the cell. They generally have two flagella, or at least one that is functional if the other has been secondarily reduced. They have green pigments and a glycide reserve (paramylon). They are common in the marine plankton of eutrophic waters, such as ports. Eutreptiella gymnastica is a typical species.
Another phylum of protoctists living in conditions similar to the euglenophytes is the small group of raphidophytes *******, represented mainly by the genus Chattonella, which probably includes some species first described by the generic names of Olisthodis-cus and Hornellia.
Symbionts with simplified organization
Complete cells that can be considered as members of one of the groups already described (such as cryptophytes) and other cells showing varying degrees of simplification (often reduced to simple chromatophores) are found as symbionts in ciliates (Mesodinium) and in other organisms.
Cells that have not been simplified or modified, whose affinities can still be recognized, live within foraminifera, acantharians, and radiolarians. They may make a large contribution to primary planktonic production and many of their host organisms have attained a level of trophic independence comparable to that of corals. Several of the organisms in the dinophytes and cryptophytes are really chimeras, consisting of associated components of very different genetic origin.
2.2 Phytoplankton distribution and diversity
The density of phytoplankton populations (microplankton and nanoplankton) in the photic zone is usually between 10 and 1,000 cells per milliliter. Many are cells of partially or totally heterotrophic organisms. The number of picoplankton cells (cyanobacteria and protochlorophytes) may be 10-1,000 times greater (104-106 per milliliter) but they are extremely small organisms, each of which is only about one thousandth of the average volume of nanoplankton. Populations in deep waters are sparser, although it is impossible to say how far down they are found. Cells of various species are always found at depth, out of reach of light.
The small cells of the picoplankton or ultraplankton rarely receive specific names and at most a generic name, although it is known that there are different forms since not all populations behave the same in culture. The larger organisms are easier to describe, and their study began and progressed at a time when taxonomy was considered more important than now. The classic works and very detailed monographs published between the end of the last century and the middle of this century have beautiful illustrations. Many species have never been described, which becomes obvious to anyone investigating phytoplankton in detail in any specific location. Many groups, such as the cryptophytes and several groups of small flagellates (including some with hard parts, such as coccolithophorids) are particularly not well known, and the same is true for the numerous and frequent heterotrophic dinophytes found in the penumbra levels.
Low diversity, wide distribution
Alain Sournia and collaborators published in 1991 a census of known species of marine phytoplankton and gave a very low figure of less than 5,000 species, far less than the number of known freshwater plankton species. This relative poverty is surprising, especially when compared to the large number of species found in any family of insects. This lack of species in the oceans may be due to the intense mixing of the water, which has the effect of countering genetic isolation. Lakes may well have been more effective at confining populations and promoting speciation. Even so, the marine planktonic "flora" has changed quite quickly over geological time and is not charcaterized by a low level of speciation.
In conclusion, biological diversity may be lower than expected, even though not all species are found everywhere. Without doubt, the continuity and movement of the oceanic waters help to reduce the separation and speciation that reflect past history and geography in continental or freshwater environments. It is clear that our knowledge is still limited because of the lack of accurate descriptions and only limited use is made of taxonomic criteria based on genetic and biochemical differences. It cannot be denied that there are many species of southern diatoms and that many dinophytes, mainly of the genera Ornithocercus, Amphisolenia, and Histoneis, have only been found in the highly stratified waters of tropical seas. Some of these organisms, such as Dinophysis miles, even show "clines," or gradients, in their shape over large areas.
Certainly, planktonic ecosystems are not as diverse and clearly established as tropical rainforests or the arctic tundra, but each area of ocean does have its own set of conditions and its own dynamics, and this defines the relative abundance of different species.
There appears to be no problem maintaining a "genetic bank" rich enough to allow effective colonization of water in any new situation that may arise. There has been speculation about the possible importance to blooming of the availability of enough resistant cells in the bottom sediment of blooming areas. Although present, these cells may not be indispensable, because detailed studies of widely varying places always show live cells of most, if not all, the usual species of the local flora that proliferate alternately during the course of annual or seasonal successions. Quiescent cells are relatively numerous in deep waters, where they are still alive even though they are obviously not photosynthesizing.
If the number of species is relatively restricted and geographical differences are small, then clearly similar communities may be found in very different locations. If we are able, or wish, to distinguish between different communities, then they often represent different stages of the ecological succession typical in plankton, starting from populations showing low diversity and often rich in diatoms (or coccolithophorids), to situations where populations are locally heterogeneous and show higher diversity, especially of dinophytes.
Taxonomy is not fashionable and studying phytoplankton organisms is often very difficult because they are small and fragile and their fixing, sectioning, and study using electron microscopy requires, at the very least, patience, skill, and time. Other aspects of modern biology such as studying the possible existence of clones or different races within each of the "classic" species, mainly shown by biochemical and physiological differences, have a more positive impact on the analysis of phytoplankton populations. The "species" where these races or clones have been sought are those of genera such as Phaeodactylum, Emiliana, Gonyaulax, Skeletonema, Thalassiosira, and Prorocentrum, which are most commonly cultivated in laboratories. They show physiological differences between strains with respect to temperature and salinity, heterotrophic capacity, vitamin requirements, and other properties that clearly define their relative probabilities of survival in a marine environment that is never uniform.
There are some well-known differences between comparable pairs of species, such as Ceratium furca and C. fusus, that occur together but which diverge in terms of their preferences. C. furca is more thermophilous, less halophilous, requires more phosphorus, and multiplies more actively at the surface. A further example is the differences between Nitzschia delicatissima and the species of the seriata group of the same genus, which are found in colder, deeper waters, with higher salinity and phosphorus levels. Local observations repeated over time suggest many other similar ecological divergences. In pairs of organisms with very simple morphology, such Synechocystis and Synechococcus in the phytoplankton, biochemical, physiological and genetic techniques are required to illustrate these differences.
Census information from a single region can be plotted on a graph showing the logarithms in decreasing order of the number of individuals of a species, arranged from more to less frequent, thus giving a good expression of diversity. This method sometimes gives surprising results. For example, the Mediterranean turns out to have one of the greatest diversities, greater than any comparable sea, and even greater than more "tropical" ones, such as the southern part of the Caribbean Sea. This difference is consistent with the fact that the density of plankton and its productivity is slightly higher in the Caribbean than in the Mediterranean.
Diversity and production
In general, there is an inverse relation between diversity and biological production and even more so between diversity and fluctuations in production, whose frequency and intensity in the oceans shows a strong correlation with production. The periods of peak production are typically characterized by populations with one or a few very abundant (in reality dominant) species, and there is a long list of species in reserve, represented by only a few individuals.
These relationships can be visualized by graphically representing the relations between the number of individuals and the number of species. These show the irreversibility nature of all real changes, especially those dealing with living systems. Increases in biomass--and total plankton density--are due to just a few species. Once maximum biomass has been attained, the number of contributing species increases and, eventually, the biomass present decreases but sufficient numbers of individuals of certain species are still spread about to serve as a basis for future growth and spread.
This mixed, species-rich population, although mostly quiescent, might be compared to a "seed bank," and is located in dimly lit water, and so it is at this level that maximum overall diversity is often found, which is the asymptotic ceiling of the spectra of various localities. This is comparable to persistence mechanisms in rivers, where a sizeable reserve of propagules of many different species is available on the sides of rivers and at different water levels, often in very thin soil or even far from the flowing water, and this is the explanation for the continuous recolonization of mountain streams and seasonal rivers.
This highly diverse reserve is made up, in an alternating and discontinuous fashion, from the results of the evolutionary experiments continuously undertaken in the more active parts of the ecosystem. These ecological, genetic, and evolutionary experiments will, if relevant, enrich the genetic diversity of the reserve over time. This is one of the functions of the rapid and abundant phytoplankton blooms that are always taking place somewhere in the ocean.
2.3 The primary production of phytoplankton
The primary producers of plankton are small. Most measure between 2 and 200 microns, and because they do not have fibers, nor vessels, or wood, they allow us to understand the question of production better than does terrestrial vegetation. They are suspended in water, where they obtain food and nutrients.
The photosynthetic pigments
Chlorophyll and other pigments active in photosynthesis are easily extracted with the appropriate solvents, and easily measured by colorimetry or fluorescence. In volume 1, pp. 180-190, information is given about the distribution of light within the water and about the structure and function of the photosynthetic apparatus that is applicable to the biology of the phytoplankton. In marine phytoplankton, the ratio of the total weight of chlorophyll (which contains 44% carbon) and total weight of organic carbon is generally between 1:30 and 1:300, a much higher proportion than that found in terrestrial vegetation, as the latter contains a high proportion of support and transport structures that are disproportionately rich in carbon.
The American biologist Alfred C. Redfield proposed for phytoplankton an average ratio between the relative concentrations, in atoms, of C:N:P (carbon, nitrogen, and phosphorus) of 106:16:1, which is generally accepted and widely used. Multiplying by the respective atomic weights gives the ratios by weight. In terrestrial vegetation, the relative quantity of carbon is at least two to five times greater, a ratio that agrees with the statement in the previous paragraph. It is thus not correct to compare the phytoplankton to the grass in a field that has been ground up and in suspension. For the comparison to be correct, the ground-up material would have to be limited to the photosynthetic tissues of the leaves. Terrestrial vegetation usually contains 1-1.5 g of chlorophyll per square meter. In the oceans, the active phytoplankton is in a layer about 100 m thick, approximately the same as the height of the tallest trees, but the quantity of chlorophyll present is smaller and normally does not exceed 0.1 g per square meter.
The pigments present in the photosynthetic systems mean that the effective photons are those between 400 nm (blue) and 800 nm (red): This is the active radiation in photosynthesis. There is a relative gap in the absorption by the pigment at the wavelength at which water is most transparent (greenish blue), centered around 520 nm. Only phycobilins found in some cyanobacteria can absorb radiation in this segment of the solar spectrum. It is surprising that this window is so little used, as cyanobacteria are relatively infrequent in sea waters, unlike in the waters of the continental surfaces, where they are very abundant. This radiation is correctly expressed as energy or is counted in photons (mE), which is justifiable because it seems that all photosynthetically active photons are about as effective, independent of their respective energy. The vertical distribution of available light is a function of the water's transparency. There is a critical zone between two and two-and-a-half times the maximum depth at which a Secchi disc can be seen, and coinciding with the chlorophyll maximum, where a considerable part of production takes place. The carbon assimilated per gram of chlorophyll rarely exceeds 4 g per hour of light, and decreases rapidly (logarithmically) below 60 (mE per square meter per second (about 8,000 "lux").
Production is studied using oxygen exchange, or radioactively labelled carbon (14C) in small confined volumes of water with its plankton. Photosynthesis includes a reaction that is photochemical and is thus less dependent on temperature than the later metabolic steps. The speed at which the nutrients contained in the seawater are consumed makes it possible to fill in the picture. On the basis of pigment concentration, or more accurately fluorescence, attempts have been made to estimate production. The search for an indicator of real production that could be perceived from space is understandable, but at the moment the relationship between potential productivity and real production is indirect and unreliable.
The role of nutrients
If we draw up two parallel lists to compare the concentrations of the different chemical elements in organisms and in seawater and their respective quotients, phosphorus is nearly almost always the relatively scarcest element, and thus the one that limits or controls production. As in an industrial production line, the speed of the operation depends on the component present in the least proportion. Carbon never appears to be limiting, unless, as occasionally occurs in certain organisms, it is for some specific physiological reason. The elements that make water saline--such as calcium, magnesium, strontium, sodium, potassium, and fluorine--are never limiting. It is not clear how and why many marine planktologists have, for some time, appeared to consider that the element that most frequently limits primary marine production is nitrogen (Harvey, in 1955, correctly considered phosphorus more limiting factor than nitrogen). It is true that the quantity of dissolved combined nitrogen (nitrate, nitrite, ammonia) may be relatively small, often as a consequence of bacterial denitrification that converts the nitrogen from a combined state to its molecular state which, because it is a gas, dissolves in water. This gas molecule (N2) is in equilibrium with the atmosphere, and so seawater normally contains about 13 mg (=10.5 [cm.sup.3]) of nitrogen per liter. The level of combined forms of nitrogen dissolved in seawater is usually only 1/100 to 1/1,000 of the concentration of gaseous nitrogen. If nitrogen was the limiting factor, it is difficult to believe that there would not have been a more massive invasion of the phytoplankton by cyanobacteria, as has happened in continental waters and is now evident in waters enriched in phosphorus. There is not enough combined nitrogen in these waters and cyanobacteria fix atmospheric nitrogen, so that eutrophic lakes are filled with them. Cyanobacteria are present in considerable numbers just about everywhere, although in the sea significant visible blooms of filiform cyanophytes (Trichodesmium or Oscillatoria, Nodularia) are scarce, and they are often found precisely where combined nitrogen is not lacking, perhaps due to the previous activity of these cyanobacteria populations.
Phosphorus concentrations are low and are decisive for water fertility. Although the unlit levels of the oceans contain a considerable reserve, with concentrations of 30-60 mg per cubic meter (in the Mediterranean as low as 5 mg per cubic meter), in the illuminated strata the action of organisms often maintains the concentration of phosphorus at undetectable levels. Part of the phosphorus available to organisms is in relatively unreactive organic forms, making it even more difficult to measure. Phosphorus concentrations in surface water are usually negligible; when more arrives, it is rapidly used up.
The behavior of nitrogen and phosphorus show marked contrasts (see volume 1, pp. 129 and 165-166). Nitrogen forms soluble compounds and circulates between the water and the atmosphere. Phosphorus, on the other hand, is found in organisms in the form of compounds of phosphoric acid, never reduced to the element, and in seawater it is found combined with organic bases or as orthophosphate (HPO4=). As its compounds are relatively insoluble, it cycles basically between the water and the sediment, where it is continually being lost or immobilized. In the dynamic of the biosphere, phosphorus acts as a major regulator, or "buffer."
All sediments contain phosphorus, especially those formed under very productive water (in upwellings), and these sediments are rich in phosphorites. In these regions, seabirds obtain phosphorus from the oceans and temporarily immobilize it in guano, thus reducing the productivity of the pelagic systems they depend on. This behavior is equivalent to that of the small migratory planktonic crustaceans whose compacted excrement also slows down global dynamics by accelerating the export of phosphorus to the depths. It is as if the phosphorus cycle always has to pay some price.
This type of regularity is not always welcome. When attempts have been made to artificially fertilize marine areas, it has been found that a considerable part of the phosphorus is lost in the first cycle, precipitating as insoluble phosphate, and so it is not possible to stabilize production at desirably higher levels. The continuity of life requires the redissolution and mobilization of more phosphate, and this occurs, to a large extent, on the continents.
Significant correlations are not established between concentrations. Instead, they should be based on suitable processes, for example, the consumption of phosphate and plankton growth. This relationship is naturally that of an asymptotic process, slowing down as the mass of organisms increases and the concentration of the element being assimilated diminishes. Moreover, there may be further limitations at any given moment, but this does not exclude the possibility that other elements or compounds are present in excess.
A widely used indicator is the concentration of an element that shows an absorption velocity that is half the maximum possible value. A typical phytoplankton cell contains between 0.3 and 2 pg (picogrammes, 1 pg=10-12 g) of phosphorus, and the concentration of semi-saturation may be between 0.02 and 0.5 mg at P per liter or mM P (i.e. between 0.6 and 15 mg of phosphorus per liter). Nitrogen has a semi-saturation constant that varies depending on the type of ion or molecule assimilated, but is about ten times greater than that of phosphorus, which is not surprising if we remember the relationship advanced by Redfield.
It has often been considered that the chain of production could be broken by the scarcity of some essential element other than phosphorus or nitrogen. This might be a micronutrient such as cobalt, selenium, or the others that appear to be necessary for marine plants and animals. Seawater is a sort of extract of the Earth's crust and it appears to contain all the elements in sufficient quantities, although there may be relative shortages locally. In the 1980s iron was suggested as a possible factor limiting phytoplankton growth, and it was suggested that the southern oceans should be enriched with soluble iron compounds to increase phytoplankton production. This would help to fix more carbon and perhaps reduce the greenhouse effect. There are, however, no convincing reasons for affirming that iron is a limiting factor anywhere.
Marine phytoplankton also shows vitamin requirements and many organisms require the presence in the environment of specific organic molecules, already synthesized, such as cobalamines. However, this can only rarely change the most common conditions of production because there is always enough diversity of organisms available as a whole for them to be able to produce in most given circumstances.
New production and recycled production
Primary production by the phytoplankton is the basis of life in the seas. The oceans also receive a relatively small subsidy from the continents in the form of the dissolved materials transported by rivers. This is from 1-2 g organic carbon per square meter per year. Much of this material cannot be directly biologically used and just slowly decomposes in the water.
It is not easy to draw up a critical summary of the available information about production. It has been suggested (see volume 1, p. 191) that the world average of carbon fixed per year per square meter of section is about 100 g. This type of figure requires the correct integration of a range of figures for production obtained at varying depths from the surface to the lower limit of photosynthesis. Most published data on oceanic production refers to net phytoplankton production after deducting respiration by the algae, and in reality these values show great uncertainty.
Experiments carried out to measure primary production highlight how complicated it is by recycling and by the difficulties of quantifying this. To carry out this type of measurement, the plankton and water are usually confined within a flask. It is recommendable to remove the large animals by straining the water through a mesh that allows phytoplankton to pass, but retains the animals. All in all, this task is contradictory or downright impossible, because there are algae, such as diatoms with large appendages that are bulkier than many animals. Sometimes these precautions are not taken and what is being examined in the confined space of the flask is the metabolism of an entire system, whose components cannot be distinguished. If we remove the large animals, we are left with the small ones, and in any case it is impossible to remove the bacteria, which cannot be separated in a physiologically practical and effective way from planktonic algae. All experiments to measure production, whether by oxygen exchange or by the use of 14C (perhaps even harder to interpret), express the overall result of complex biological activity, in which internal recycling of part of the elements has never ceased. This difficulty is extremely obvious in highly integrated symbiotic systems such as corals or some non-photosynthetic planktonic protoctists that show negligible net production to external observation, given that they recycle their chemical elements internally, using energy provided by light.
It has been pointed out that the cycles in the Amazon show a similar internalization, and thus provide almost no oxygen and absorb almost no CO2. After all, the Earth as a whole recycles and we reach the conclusion that the distinction between "gross" production and "net" production is a consequence of the intellectual limits we place on the entity in question and how we interpret it. The real functioning of ecosystems makes many of our conceptual schemes unworkable.
More pragmatically, pelagic space can be divided into overlying strata. The level just below the limit at which light is sufficient for photosynthesis is especially important because it separates an upper photic region from a lower aphotic layer, the latter with very little or no light. The normal functioning of the pelagic ecosystem results in the net transport of nutrients downwards and their accumulation in the lower compartment.
For the last few decades, it has been usual to expose collecting devices, for one or two weeks at standardized depths, in order to gather the material that is continuously settling, such as dead plankton or its hard parts, excrement, material that arrives transported by the air (pine pollen is found almost everywhere, for example), and so on. The results are often unreliable due to the inclination of the recipients and interference by horizontal currents, but it is generally found that both the quantity of material and its nutritional value diminish with increasing depth.
A considerable fraction of the elements (nitrogen, phosphorus, etc.) are assimilated in the photic zone: The phytoplankton is eaten by little animals, and these may excrete voluntarily or involuntarily (when they are eaten) at the same or a lower level. Small primary producers, such as cyanobacteria and other photosynthetic bacteria, are ingested by tiny ciliates and flagellates in a cycle called "microbial" because the organisms recycling part of the primary production are small. These organisms may often be dispersed, but more often they are associated with dead material in flakes, often large and visible as "sea snow." The quantity of tripton (non-living, detritic, organic material suspended in water) is about ten times that of plankton. This goes unnoticed if we restrict our understanding of plankton to what can be retained by the cloth of a sieve or net, and to cyanobacteria and other tiny photosynthetic bacteria. This detritic material in turn absorbs various organic compounds and can concentrate the secretions of organisms. All in all, it is a different, but important, twilight world.
To the previous elements we must add the part of primary production that serves as food, mainly during the hours of darkness, for the many small crustaceans that migrate alternatively from upwards and downwards, leading to an even more definitive loss of essential nutrients from the upper stratum. These crustaceans as such are less important than their compacted excrement, which sinks quickly until it breaks up on reaching considerable depths due to the action of the bacteria that are always found adhering to the film that surrounds them and keeps them compact. This of course only happens if the excrements are not captured for their own use by needier copepods living at greater depths.
Below a certain depth, life only continues to exist because it receives a contribution or subsidy from above (the only exceptions are the "oases" at great depths, which are maintained by chemosynthesis around submarine hydrothermal vents, described in chapter 3.5, section 1 of this volume). However, this manna would soon cease to fall if the process of primary production was interrupted by a lack of nutrients. The return of mineral nutrients to the surface is necessary to avoid interrupting the production cycle and requires the energy provided by oceanic circulation. This is called external, or exosomatic, energy, to distinguish it from the internal energy or endosomatic energy associated with light and the metabolism of organisms.
For every site and every season it is possible to measure, at least in theory, a level corresponding to the "center of gravity" around which the function of primary production is distributed, as well as another barycenter, or center of gravity around which the respiratory activity of the system is distributed. The difference between the two mentioned centers of gravity is related to the average path taken by a carbon atom from the site of assimilation to the site of respiration. This distance is related to the degree of superimposition in the distribution of the factors of production. These two centers of gravity can never coincide, but they will be closer together in a highly turbulent system, and will be further, possibly much further, apart in a more stratified system. If we distinguish between compartments, all show some internal recycling and an external circle made up of important export routes that are equivalent if the situation remains more or less stationary.
Naturally, the lower limit of the zone where photosynthesis is possible is particularly appropriate for siting an imaginary or conceptual frontier. There will always be some loss of organic material downwards towards the unlit depths. If the situation is stationary for more or less prolonged periods, this requires the entry into the superficial compartments of equivalent supplementary nutrients (some P and N), whether by horizontal transport, local upwelling, or seasonal vertical mixing. This allows production considered as new, unlike the production measured in the surface layers, which is associated with biological recycling within the surface strata.
The ratio between new production and total production is usually designated by the letter f, and this is an important local characteristic of marine ecosystems. The value of f is high in well-mixed systems and low (for example between 0.1-0.3) in ecosystems that are stratified for long periods and that show relatively intense upwards metabolic recycling, perhaps because selection has favored organisms (swimmers) that have a lower tendency to be lost through sedimentation. Several oceanographers, especially, R.C. Dugdale, R.W. Eppley, and J.J. Goering, have pointed out that the flow of different forms of nitrogen might serve to estimate the value of f, if it is accepted that the recycling of nitrogen mainly affects ammonia compounds (the form in which N is excreted by animals and other heterotrophs) and that new production is based on the receipt of nitrogen in the form of nitrate, proceeding from somewhere else, usually from below.
In stratified seas, or in the seasons when the water is stratified, one can recognize a clearly defined level (often horizontally discontinuous) just below the chlorophyll maximum that is considerably enriched in nitrite. This is where the gradient of reduction in light is strongest and the light becomes inadequate for photosynthesis, and where nutrient concentrations suddenly increase (the nutricline). Here, the planktonic algae that are settling pass through a zone where light is insufficient for photosynthesis, but where they can absorb nitrate and carry out the first stage of their chemical reduction (to nitrite). Nevertheless, they do not have enough light to assimilate it and it probably escapes, which would explain its accumulation at such a precise level. One would expect the stratum with maximum nitrite to show greater contrast when the f value is low.
2.4 The dynamics of phytoplankton production
Victor Hensen (1835-1924) who introduced the term plankton in 1887, undertook a series of painstaking studies of the bay of Kiel. This was the beginning of the quantitative approach to the study of plankton and attempts to understand the environmental causes and interactions between the different organisms involved in the dynamics of pelagic life. Hensen also took part in the plankton expedition of the National (1889), the first oceanographic expedition devoted to plankton and the beginning of an overall quantitative approach to studying plankton (for the entire Atlantic). Around this time, and even more so at the beginning of the 20th century, interest in understanding variation in fish populations led to laboratories being set up in many coastal localities, such as Ostend, Belgium (1843), Konk-kerme (Concarneau) in Brittany (1859), Roscoff, also in Brittany (1871), Woods Hole in Massachusetts (1873), and Naples, Italy (1874). One of their functions has always been the study of local fluctuations in plankton populations, correctly considered to be the basis of the fertility of the water. What started off as keeping records of plankton changes led to a study of their causes.
Variations in production in space and time
In temperate regions, at least near the coasts, a great abundance of plankton--first diatoms, then copepods--can be observed in the spring as the days lengthen and the surface waters warm up. In 1906 W. Natanson realized that the increase in fertility was mainly due to deep nutrient-rich waters rising up to the illuminated surface. The commentaries on new production and recycled production, in the section above, are fully applicable to the more stable situations that follow: Marine blooms always occur in fits and starts whose origins are often unclear.
Observations by the Norwegian oceanographers Haakon Hasberg Gran and Trygve Braarud (1935), first off the coast of Norway and then in the Gulf of Maine, showed the lack of uniformity in the spring plankton peak, a discovery that led them to recognize the factors controlling production. In very turbulent water whose nutrient content is uniformly distributed throughout its depth, the phytoplankton increases first in the shallower areas, where the seafloor places a lower limit on the possible dispersion of plankton towards less illuminated levels. If the depth is greater than 328 ft (100 m) and the water is very agitated, the cells spend too little time under sufficient illumination to allow them to reproduce indefinitely. These situations led to a delay in the beginning of net production with a surplus. The greatest production started as spring progresses and the light penetrates further, also because this starts thermal stratification of the water that limits the extent of vertical mixing. For production to take off, the depth of mixing (measured from the surface) should not exceed a certain relation to the depth of compensation--the depth where the production of the system is equal to its respiration, and there is therefore no net production. According to the Norwegian Harald Sverdrup (1953), this limiting relation is between 1.5 and 5.5, depending on other local circumstances. As this relation decreases due to increasing light and reduction in the thickness of the highly stratified layer, the massive production of phytoplankton gradually extends from regions nearer the coast to deeper open waters.
This onshore view can be improved by contemplating what happens from the high seas. The centers of the oceans have long been considered especially barren: neither dense populations of diatoms nor schools of fish ever develop there. The Sargasso Sea has always been the classic example of this situation. However, relatively recent data have shown a significant activity in which the minuscule organisms of the picoplankton play an important role.
Production and upwelling areas
The situation is very different in areas of upwelling. Here, the action of the winds, interacting with the direction of the coastal currents and in conjunction with the forces associated with the rotation of the Earth, makes the surface water flow away from the coast, to be replaced by water from the depths, richer in nutrients. This is the reason for their uninterrupted high primary production over long periods. These areas have always been important fishing centers.
One can calculate the velocity of ascent of deeper water and the quantity of nutrients it brings to the photic zone, as well as the kinetic energy obtained from the hydrosphere-atmosphere system to carry out the local mechanical work that supports this continuous high primary production. This exosomatic energy is at least 25-50 times the light energy involved in biological production. A similar relationship is also found in terrestrial vegetation, where the exosomatic energy involved is mainly in the form of evapotranspiration. In agriculture, it is also necessary to include the additional energy used in irrigating, fertilizing, and cultivating the soil. The application of the models of ecological interaction formulated by Alfred J. Lotka (1925) and Vito Volterra (1926) to plankton did not take place immediately, even though Volterra was specifically inspired by a problem related to fish production. The basic difficulty is that these models only sought to describe the interaction between species, and between groups of species, as entities abstracted from their setting, and they did not take into account either spatial organization or external energy, both of which are obviously very important in marine populations.
The water column model
Gordon A. Riley surreptitiously introduced space, by means of the concepts of sedimentation and diffusion, the latter of which is associated with the energy of turbulence. The conclusions of an ecological approach to Atlantic plankton by Riley, Stommel and Bumpus (1949) suggested a model according to which dF/dt = (r-gZ) F - V dF/dz + Azd2F/dz2, where (if appropriate) we consider r-gZ = r'. In this expression, F represents the phytoplankton, Z the zooplankton, V is the speed of sedimentation (=0.001-0.02 cm per second), and A is the coefficient of vertical diffusion, which is a measure of the turbulence; z indicates that it refers to the vertical dimension. A, the first letter of Austausch, or change, is a coefficient of diffusion, expressing the transmission of heat, salinity, or movement in a liquid, in g/cm per second (such as dynamic viscosity, divided by density, which is approximately 1, the kinetic viscosity, expressed in [cm.sup.2] per second). Plankton is scarce close to the surface, not because of excessive light, but because of the discontinuity represented by the surface of the sea, from which the plankton sinks but that it can only enter by cell division. A can be calculated approximately by measuring the downwards transmission of heat along a specific thermal gradient. With reference to the vertical (Az) and the photic zone of the Mediterranean, the values obtained are less than 2 between May and July, from 2-5 in April-May and July-August, and higher than 5 between September and April, when the waters are more agitated and more productive. In the horizontal direction, Ax, it reaches much higher values.
In the form proposed above, the model describes a vertical column of water and cannot be directly applied to the real world where horizontal differences, or those between different columns, are very important. The physical structure of the sea is very complicated with discontinuities that are almost as mobile as those occurring in the atmosphere. This means that predicting changes in planktonic populations is as difficult as predicting the weather.
Heterogeneities and asymmetries
The pelagic world contains a set of chemical reactions that take place in a space that is progressively structuring itself, as happens in some colloidal systems. In fact, ecological succession in pelagic systems occurs in a medium that is becoming more structured or, at least, is becoming progressively more thermally stratified. Smoluchowski's (1918) considerations already suggested expressing production (P) as dF/dt = P = AxC, where A continues to represent the energy that is dissipated in turbulent mixing and C is the covariance or degree of superimposition in the distribution of the factors of production, basically chlorophyll, light, and nutrients. If external recycling occurs, it should be considered as a ring that passes outside the space of reference and joins imports (I) and exports (E). Thus, P is the locally retained production: P + E = I + AC and P = AxC. In its simplified form, without the recycling ring, this expression can be derived with respect to time, giving:
[d.sup.2]F/[dt.sup.2] = dP/dt = C dA/dt + A dC/dt
which expresses succession rather elegantly, making it possible to interpret how the decrease of available energy in diffusion or turbulence is usually combined with a reduction of covariance in the distributions of the factors of production. This decrease in the covariance is equivalent to an increase in the segregation between elements, an interaction that obviously contributes to production: The tendency is always for nutrients to be depleted where there is light, and so nutrients only accumulate where there is no light.
All the heterogeneities that arise show asymmetries. For example, if eddies form that rotate in different directions, interference from the rotation of the Earth leads to the breakdown of the initial "impartiality" of any irregular mosaic, in the sense that the centers of higher production associated with cyclonic eddies (anticlockwise in the Northern Hemisphere) end up as isolated patches in a background of lower production, and not the other way round.
Nowadays, structures of this type can be recognized in images obtained from space. Oceanography has routinely included continuous analysis and transects (temperature, salinity, and chlorophyll, generally measured by fluorescence), on the basis of which we can postulate a reasonable general two-dimensional structure into which we can expect to fit and interpret the heterogeneities revealed by the linear segments analyzed. The only compatible structure turns out to consist of more productive, but discontinuous, patches, dispersed in a background of lower productivity or biomass. These fertile patches obviously, although not always, coincide with cyclonic vortices.
The logarithmic transformation of plankton concentrations X [x = log (X + l)] along a transect makes graphs mosty symmetrical and reminds us of the way that many of the distributions of plankton in space are like the fractal profiles of mountain chains. If they are in two dimensions, they show peaks that appear to be isolated or discontinuous. These peaks, in our case, correspond to centers of high production from which phytoplankton populations are dispersed. This is a very generalized pattern in nature, and is surely the most common pattern in the distribution of marine production in which local patches or concentrations are always a feature.
Nowadays, computers offer many exciting possibilities that allow the simulation of how plankton might multiply and evolve in accordance with specific assumptions. It is natural that models of flows and salinity, which show continuity, should be more acceptable than biological models, in which history intervenes with all its uncertainty. The scarcity of real data often leads to excessive interpretations that are not always correct, bearing in mind the frequency of local discontinuities and disturbances. The prospect for correct predictions, on any scale, are still not very promising.
2.5 The processes of succession and biological types
Ecosystems never maintain the same organization for a long time. If they maintain their activity within a reasonably stable environment, they can always continue occupying space with slightly different (but equivalent) structures that imply a lower maintenance cost, or by enriching their own complexity without increasing the energetic cost. Normally these changes are associated with the gradual consumption and diminution of the quantity of nutrients available. This is the essence of ecological succession (see volume 1, pp. 226 and following). In plankton, succession shows the special characteristic, due to the time-scale of the pelagic ecosystem, that all events and changes are much faster than in benthic or continental ecosystems. This greater speed facilitates the appearance of local differences.
Succession in phytoplankton
Succession in plankton never shows constant or uniform characteristics between separate, even neighboring points. Normally, local differences have been generated in time, either because changes have occurred more rapidly in one area than another, or because equivalent sequences have started at different times, depending on local differences in the water turbulence, nutrient concentration, and the distribution of light. Changes are always asymmetric: Gradual changes, which are self-organizing and relatively slow, are interrupted by sudden, random disturbances, usually accompanying an intensification in the turbulent mixing of water or the displacement of water masses from one level to another.
The dynamics of the plankton populations combine time and space. More than once plankton blooms have been compared to clouds in the sky, because the cells multiply most where there are movements of water of the right strength and direction, which are especially effective when they move nutrients closer to the light. However, all these movements, whether they are unidirectional, like sea currents and upwellings, or alternating and confused, such as turbulence, depend on external energy that comes eventually from the Sun. Water is slightly less dense than the organisms themselves, increasing slightly with increasing depth, and receives light, heat and mechanical energy mainly at the surface level. Growth will be intense while cells (or chlorophyll), light, and nutrients coincide in space. Water tends to warm up on its surface and stratify by density, and this acts against local vertical mixing. Mixing is weak and may be caused indirectly, in association with horizontal transport movements.
Excessively strong vertical mixing in deep waters means that each cell of the phytoplankton, on average, enjoys light for too short a time, leading to little or no growth and the excessive dispersal of the population. If the thickness of the mixing layer exceeds by a certain factor (between 1.5 and 5, depending on other circumstances) the compensation depth (where biological production and respiration are equal), there are too many losses and the plankton does not increase. Even if conditions are optimal, the coincidence or high covariance in the distribution of the factors or agents of productions soon decreases, either because the population sediments and sinks to layers where light is insufficient, or because of nutrient exhaustion, or more commonly for all of these reasons.
A basic principle of planktonic life is that every atom of an element that passes from the medium to the body of an organism will probably return (from the same organism or another, such as a planktophage or predator) to the environment, but at a lower level (i.e., closer to the center of the Earth), than the level at which it was assimilated. The net result is that there is a generalized downwards transport of the elements in the water that are necessary for life. In spite of temporary local ups and downs, the relatively stationary situation reached is the result of interaction or interference between biological processes and water movements. Normally the highest biological activity is at almost twilight levels in terms of light availability--at 131-328 ft (40-100 m) in depth. This stratum is only a few meters thick and shows moderate biological production, stimulated by the daily cycle of activity and by possible internal waves between the upper fully illuminated and sterile level and the lower nutrient-rich but dark zone. Since growth is controlled by the supply of nutrients, it is not surprising that when the phytoplankton multiplies in the twilight, it apparently makes poor use of the light that, in fact, is available in excess.
The greatest quantity and activity of the phytoplankton is thus located relatively deep, not because the surface light is noxious due to excessive intensity, but because the surface of the sea, in addition to being exhausted in nutrients, is a discontinuity from which organisms sink but which they can only reach from below, and even then generally only as a result of turbulent mixing of the water. In fact, most of the light reaching the ocean is simply absorbed by the water and is of no direct use to living organisms. It is understandable that the quantity of chlorophyll that is found per square meter of ocean is, generally, lower (often much lower) than that found in vegetation on the continental surfaces. Normally, per unit area, this value is only 1/10 to 1/20 of that found in terrestrial vegetation.
For phytoplankton to produce, nutrients, light, and organisms must occur together. Organisms are in general denser than water, and there is thus an unstoppable flow downwards, although often slowed down by the various mechanisms allowing swimming or passive floating, which is as fatal as death for humans.
The return of the necessary chemical elements to the illuminated surface waters and the continuation of the cycle of pelagic life depend on external or exosomatic energy. Primary productivity, or phytoplankton production, is proportional to the supply of necessary elements. Phosphorus is the most important, then followed by nitrogen and others. This seems to be the normal order, although it is possible that it may vary locally and an element other than phosphorus may be limiting. It appears that carbon is never limiting, or perhaps only locally, for organisms that have evolved relying on a large excess of CO2 would be at a disadvantage in excessively alkaline waters where most inorganic carbon is present in the form of bicarbonate (HC[O.sup.3-]).
No situation can ever maintain itself stationary, persistent, and uniform unaided. Nature in general, and the sea very clearly, moves in fits and starts. Both storms and waves, whether superficial or internal, introduce discontinuities on many different scales. These intermittent influences affect the photic surface levels most, and these are the only productive levels. Of course, there is a rich and varied life in the abysses, supplied by the material that falls from the higher levels and this manna falling from heaven does so in a way that is highly uniform, given that it is made up of many small scattered episodes. These episodes activate the photic zone irregularly, within a frame of time and space large enough to allow the integration and evening out of the flow of part of its net production on its way to the depths.
Each of the major taxonomic groups of phytoplankton has its own "vocation" as a consequence of its fundamental characteristics (for example, possessing ballast of opal or of calcite), or as a result of an adaptive secondary evolution (the presence of different size of appendages). Generally, the representatives of each particular group live and multiply best--and are thus selected--under a specific set of environmental conditions, or at particular stages of successional sequences that are associated with respective productive episodes of variable length, generally lasting from weeks to months.
If the surface water is nutrient-rich, production is fast and will be even faster if the water is rising and the nutrients are continually renewed where light is intense. In this situation, it is advantageous to sink against the rising current, as this still maintains an acceptable level of illumination. In calmer and poorer waters, cells do not divide so fast and it is worth staying at the same level and increasing, as far as possible, the capacity to absorb the little remaining food. It is worthwhile devoting some energy to maintaining the cell in motion, using flagella, and it is even better if these swimming movements lead to vortices that increase absorption. This can be achieved by cell shapes that might seem capricious to us, but clearly respect the laws of hydrodynamics. These forms, possibly with small modifications, may also play a defensive or dissuasive role against potential enemies.
The main biological types discussed below are stages in a sequence, rather than discontinuous classes, although the divergent evolution separating them may have included the need to solve some dilemmas. Diatoms and coccolithphorids are immobile or only slightly mobile organisms, with ballast, that can multiply rapidly and sink easily; silicoflagellates might also be included in this ecological group. All these organisms practise what in population dynamics is called an r strategy. They multiply quickly, using the nutrients available at the time, without concern for what might occur the future. On the other hand, there are organisms, typically swimming organisms such as the dinophytes (the ancient lords of the plankton) and other smaller groups whose survival is due to their K strategy, where relatively low reproductive rates combine with constant swimming and some other way of surviving in a relatively resource-poor environment. Marine phytoplankton is generally highly mixed, but relative alternation of dominance by these two groups in time and space is worth noting. Organisms with K strategies, especially the most diversified dinophytes, can always persist in basically rich, fluctuating populations. As soon as external conditions allow production to accelerate, the pre-existing vegetation is joined by the result of rapid, often very local, blooms of diatoms, coccolithophorids or Phaeocystis.
Regularities and variations
The pattern of change in the conditions of life may vary greatly from place to place. Approximately the same situations may occur every year and in sequences that correspond to the seasons: In the winter there may be intense mixing of the water, shown by populations of diatoms, while throughout the rest of the year the water is stratified and the surface layer is almost depleted of organisms. These extreme situations may show up to 10-fold or greater differences in production.
Irregularly distributed and rapidly varying phytoplankton blooms encouraged by minor eddies (between 6-12 mi [10-20 km] in diameter and generated by the local action of winds) often occur. If there are eddies rotating in different directions, the cyclonic ones cause water to rise in their center; they are more productive and usually contain more diatoms, while the anticyclonic eddies are more passive. Another form of circulation generated by the impulse of the wind takes the form of narrow parallel bands (hundreds of meters long) called Langmuir cells. They are often visible from airplanes, especially close to the coast, from which they look like bands, hundreds of meters wide, with alternating shiny and more opaque areas. The shiny areas show clear surfaces, ascending waters, and more diatoms, while the more opaque areas show descending circulation and a higher proportion of swimming organisms.
Research transects across a region with many heterogeneous structures give quantitative sequences that take the form of the outline of a mountain range. They are compatible with a distribution consisting of highly productive patches that are isolated and discontinuous, just like typical cyclonic eddies, and dispersed over a background of lower productivity.
Marine fronts are located on the edges of currents, or where currents or water masses with different movements come into contact, whether this movement is convergent, divergent, or involves lateral sliding. When they meet they perform work and may provide nutrients. These nutrients are often complementary, and this means that they are the sites of higher biological production; as in more genuine upwelling regions, they may contain blooms of coccolithophorids or diatoms, possibly dominated by the latter. Tidal fronts, with mixed water, often contain dense populations of coccolithophorids.
Situations of stratification may receive a continuous, often horizontal, nutrient supply. This happens in bays or other coastal systems with similar characteristics, often in persistently stratified situations, caused by the advection or horizontal drag of the less salty water. There swimming organisms sustain themselves (often multiplying profusely), which may even give rise to "red tides" or "red seas" in which toxic dinophytes are frequent. Some marine regions are especially affected by these conditions, and this may have been aggravated by the increasing flow of nutrients from land to sea. This sort of episode usually ends in intense vertical mixing.
The distinction has often been made between neritic (or coastal) plankton and oceanic (or open sea) plankton. The edges of the continents interfere in the dynamics of the sea, especially in the coasts with tides, and the energy of interaction produces a local mixing of water and the corresponding local fertilization. This often leads to irregular proliferations of diatoms that coincide with wind or sea movements that mix the shallow waters. The study of situations of this type has helped to clear up the basic mechanisms of marine primary production. We know that the characteristics of the marine environment are very variable, both in each volume of water and in the form of changes that take place. There is a large number of organisms, many far removed from the general behavior of the taxonomic group they belong to, which makes it difficult to find regularities that are generally valid. Diatoms multiply rapidly, but some species persist in cultures that are continuously illuminated, while others do not thrive unless they are subject to a daily or circadian rhythm of alternating light and dark. They also settle rapidly and Riley, Stommel, and Bumpus, in their model for Atlantic plankton, used a settling velocity for diatoms of 4-6 in (10-15 cm) per hour at 32[degrees]F (0[degrees]C), and twice that at 77[degrees]F (25[degrees]C). Various other observations fall between 0.4-20 in (1-50 cm) per hour. Particular species have their own resources and escape from being included in what might appear a general law. Oceanic diatoms of large volume contain vacuoles with fluid that is lighter than seawater, and which is maintained by the expenditure of additional metabolic energy (such as the replacement of metallic cations with ammonia).
During the summer, in surface waters, diatoms survive in association with tintinnid ciliates. These function like outboard motors maintaining Chaetoceros, and more rarely, Planktoniella in suspension. Other diatoms (Thalassiosira) excrete strands of mucilage and make masses that may also remain in suspension, or at least, change these organisms' habitual form of life. Phaeocystis is another organism whose cells are often covered in mucilage. Thus the fundamental condition for phytoplankton production is the presence of nutrients in the illuminated layers, or in other words, a high coincidence (expressible by a covariance, C) in the distributions of light, nutrients, and cells. The maintenance of the exosomatic energy necessary for mixing to continue is provided by a measure of the turbulent diffusion (A). Combining the two possible categories of both of these descriptors allows the creation of a graphic with four compartments that helps to sum up several aspects of phytoplankton biology.
The same diagram may be rotated through 45[degrees] to change the coordinates, which then become respectively the quotient C/A and the product AxC that now correspond better to stratification and productivity. Using separate diagrams it is possible to mark the statistical distances between different species, based on the probability of these species coinciding in real samples of water. If a simplified representation of this type is projected adequately on to a C-A diagram as mentioned, it reinforces the meaning of this type of representation, for which the name plankton mandala has been suggested.
3. The primary consumers: the zooplankton ********
3.1 The organisms of the zooplankton
Within marine trophic chains, zooplankton constitute the step that channels the energy produced by autotrophic organisms to the secondary consumers. To put it simply, the zooplankton make the energy generated by the phytoplankton available to the large carnivores. Even so, the role of zooplankton in marine ecosystems is much more complex, due to its diversity of organisms and forms, and the range of strategies followed by different species and groups. Zooplankton consists of all the heterotrophic organisms--although some are known to be autotrophic as a result of their symbionts--that live in suspension in the water masses and depend on the water's dynamics, given that they lack the ability to move.
Meroplankton and holoplankton
Although most zooplankton organisms are small, their actual size range is between 20 micrometers and 7 ft (2 m). Among the smallest are the flagellates, while the largest include the jellyfish and siphonophores. Leaving to one side formal classifications based on size and zoological groupings, it is important to distinguish between two different types of zooplankton organisms: those that pass all their life in the plankton (holoplankton) and those that only colonize the pelagic environment at some stage in their life cycle (meroplankton). This is the case of the larval phases of many organisms, such as sessile or not very mobile benthic organisms, that use the pelagic medium to disperse themselves. The larvae of fish and many species of benthic decapod crustaceans, for example, develop entirely in the plankton.
During their period in the planktonic medium, the organisms of the meroplankton pass through different stages of morphological transformation until they reach their juvenile phase, very similar in form to the adult. How long the larval phases reside in the plankton varies greatly depending on the species, but for all of them it is the most critical period of their life cycle. In addition to the larvae of decapod crustaceans mentioned above, other groups of benthic organisms contribute in the same way to the zooplankton communities. Among the most important are the larvae of echinoderms and the medusa phase (polyps) of many benthic cnidarians, as well as those of many fish. These larval stages reside in the plankton for a period that varies between weeks and months, and for short periods of time, may represent a high percentage of the zooplankton biomass of coastal systems. Many other groups of benthic animals, such as sponges, polychaetes, and bryozoans, also produce a large number of planktonic larvae during their period of sexual reproduction. Unlike the groups mentioned above, the larvae of these animals only remain in the plankton for a few hours or days and undergo their first metamorphosis as soon as they have found a substrate to become established. The mortality of these larvae is enormous; they take advantage of the planktonic medium to disperse, but have to pay the high price of forming a very important seasonal source of food for other organisms of the coastal zooplankton.
Although the meroplankton may be an important component of zooplankton communities, most of the biomass of these communities consists of holoplankton. Copepods are by far the dominant group, forming 50-90% of the individuals in these communities, and their biological cycle takes place entirely within the plankton. The highest percentages of copepods have been found on the continental platforms in the northern half of the Atlantic Ocean, with the lowest in the tropical areas of the Indian Ocean. With respect to biomass, in the North Atlantic copepods represent slightly more than 50% of organic carbon in oceanic areas and nearly 75% in coastal areas. This difference in biomass is largely explained by the presence of large oceanic populations of euphausiids (krill), which can account for more than 30% of the zooplankton biomass. The tendency observed in the North Atlantic is repeated in other oceans, although in the tropical areas of the Pacific and Indian oceans the biomass of krill is greater, and in addition, other groups, such as amphipods, chaetognaths, cnidarians, and pteropod mollusks each represent about 5% of the total biomass. These figures generally underestimate the biomass of gelatinous zooplankton, formed by jellyfish, siphonophores, ctenophores, pteropod mollusks, and thaliaceans or salps. These gelatinous organisms are not collected efficiently with the normal sample nets used for zooplankton because of their large size and the fact that they form dense accumulations or long colonies. Recently it has become possible to assess both their biomass and activity in some areas. In addition to being very abundant, some gelatinous zooplankton (especially large medusas) are voracious carnivores, competing with fish larva as predators of the small zooplankton.
The trophic structure of zooplankton is clearly dominated by macroherbivores (filter-feeders and browsers) and omnivores (in reality herbivores able to eat small inert particles and tiny organisms). In temperate and polar areas these two represent more than 70% of the zooplankton biomass. In tropical seas there is a notable abundance of predators (carnivores) that represent nearly 40% of the total biomass. These trophic differences are related to the lower phytoplankton biomass and production of tropical seas, caused by their poverty in nutrients. Near coral reefs herbivores represent less than 10% of the total biomass, as phytoplankton are scarce because reefs act as nutrient traps, developing a rich flora of endobionts and symbionts.
The values given above refer to an annual mean. However, as in terrestrial ecosystems, marine ecosystems show seasonal variations, and these increase with distance from the equator. This temporal variation is shown by an oscillation in the number of species and individuals, basically caused by changes in activity related to modifications in the hydrographic conditions of the water column.
In temperate seas, zooplankton show two periods of maximum abundance, one in the spring and the other at the end of summer. Cold seas only show one peak, in the summer. In tropical areas zooplankton concentrations are constant throughout the year. The peaks of abundance respond to a hydrographic model in which, when the number of hours of light increases, the photosynthetic activity of the phytoplankton also increases, making use of the nutrients from the previous winter.
The increase in phytoplankton leads to an immediate response by the herbivorous zooplankton. This mainly consists of copepods, which consume 20-30% of the daily primary production. Continuous browsing by copepods gives rise to a biomass peak in the spring, made up of larger individuals than during the rest of the year. They can grow quickly and reach sexual maturity in a few days. Their life expectancy is about 20 days and for the last 10 they ceaselessly lay eggs.
The females of some species lay hundreds of eggs a day, although production decreases at the beginning of spring, as a result of the depletion of nutrients, and thus phytoplankton. In general, production by herbivorous zooplankton is very rapid and the biomass of zooplankton can increase by 10 times that of winter concentrations. The success of the copepods is largely because their metabolism allows them to grow very quickly. They invest more than 33% of the energy they absorb in growth and reproduction, and the degree of assimilation of the food they capture is nearly 60%; they are thus very effective when food levels permit.
One should also note that in warm seas during the spring, in addition to herbivorous copepods, there may be high concentrations of salps (Salpa), which are able to consume more than 40% of daily primary production, especially when they form dense swarms. These swarms can clog fishing nets, which may gather several tons of these organisms in a few minutes' trawling. As they form colonies of many individuals, the salps can compete effectively with the copepods for their common food. The copepods may reach densities of 5-10 individuals per liter, while salps may exceed 20 individuals per liter.
Many carnivores, ranging from copepods to large jellyfish and fish larvae, increase at the same time as the herbivorous zooplankton peak. The activity of the carnivorous zooplankton does not prevent herbivores from exploiting the phytoplankton effectively, or the phytoplankton from exhausting the nutrients. As zooplankton activity increases, the summer warming of the surface waters leads to increasing stratification. This change in hydrographic conditions and the activity of the organisms both lead to a diminution in the abundance of the zooplankton. In autumn, sea level winds help break up the summer thermocline, making nutrients available to the phytoplankton by once again suspending all the organic material generated during the summer, which was largely trapped below the surface layers by the thermocline. This leads to a second peak in zooplankton concentration consisting of smaller, very active, and efficient herbivorous copepod species (less biomass than in the spring) and a peak in production. Later, when winter arrives, falling temperatures and shorter days considerably reduce phytoplankton activity, leading to a corresponding reduction in zooplankton biomass.
In warm seas there are large-scale phenomena of seasonal variation in zooplankton biomass and diversity. These are similar to those described for temperate seas, although they depend on factors other than thermal variations, which are very moderate in tropical areas. An important difference is that in tropical seas they are local and occur more frequently close to the coasts, whereas in temperate seas seasonal zooplankton variations may occur anywhere. Large-scale meteorological phenomena are a good example of this, such as the seasonal changes of the monsoon regime in the Indian Ocean. For almost half the year, the prevailing winds are persistent and blow from sea to land, and during the other half of the year they blow in the opposite direction. When they blow offshore, surface water is displaced towards the high seas compensated by upwelling of deep, cold, nutrient-rich water that causes a period of great abundance of zooplankton. During this period the community is dominated by species whose life cycle occurs in coastal areas with a large meroplankton component. On the other hand, when onshore winds blow from the open sea, the zooplankton community is dominated by oceanic species, and productivity decreases as the deep layer is trapped under the photic layer. An example of this type of seasonal variation is found in the species composition of the population of hydrozoan medusas on the eastern coasts of Papua New Guinea. During the period of offshore winds, most species undergo a benthic polyp phase that produces many small planktonic medusas. These medusas stay in the plankton for a few weeks, until their larva, the result of sexual reproduction, return to the seafloor. During the period of onshore winds, however, the community is dominated by larger medusas whose life cycle takes place totally in the plankton, where they remain for several months.
The far more intense genuine monsoons generate important, large-scale seasonal differences in the zooplankton of warm seas. Monsoons are periods of torrential rain, during which rivers discharge large quantities of water on the continental platform. The high concentration of transported nutrients in this water rapidly starts a cycle of biological production favoring the development of dense populations of herbivorous zooplankton. The length of the monsoons means that these continental inputs are continuous, and so succession in the planktonic ecosystem allows the proliferation of a large number of carnivorous species and other secondary consumers, although they do not attain the level of structure and complexity observed in temperate seas during the spring.
The zooplankton contains animals that live in continuous suspension in the water, but with a limited capacity of movement. Most marine activity and production takes place in the top (656 ft [200 m]), so the main strategy of zooplankton is to prevent themselves from sinking. To achieve this, they have either developed morphological modifications or perform some sort of activity that keeps them afloat. One of the most common adaptations is having a range of appendages or body extensions, increasing their surface and offering more resistance to sinking in the water column. This also reduces the need to move continuously, and thus the metabolic expenditure it represents. There are many examples of this strategy, such as the expansions of echinoderm larvae, the appendages and prolongations of decapod crustacean larvae, molluskan parapodia and the feathery appendages of many crustaceans.
One alternative strategy is the inclusion of low-density fluids, globules of oil, or even small gas chambers within the body. Fish eggs contain diluted fluids to ensure their buoyancy; otherwise they would rapidly sink to the bottom, as they are spherical and lack any locomotor ability. Siphonophores have gas-filled spheres in the upper zooid of the colony that maintain them permanently and almost effortlessly in suspension. Many euphausiids and copepods contain oily inclusions in their adipose tissues that, together with their capacity to move, helps them to float. Gelatinous phytoplanktonic organisms (jellyfish, siphonophores, ctenophores, pteropod mollusks, salps [thaliaceans]) can change the ionic balance within their tissues and so regulate their buoyancy. Some siphonophores and other organisms, such as the dinoflagellate Noctiluca, contain cavities with iso-osmotic solutions of ammonium chloride that they can regulate to improve floatability.
A large difference has been observed between species whose adaptations include bodies with almost neutral buoyancy (meaning they need exert almost no effort to maintain their level), and those forms whose structure forces them to swim continuously to prevent themselves from sinking. Thus, for example, the chaetognaths of the genus Sagitta need only swim from time to time to maintain themselves at the desired depth, while mollusks of the genus Cavolinia have a heavy shell and must swim vigorously with their wing-shaped appendages to prevent themselves sinking. In general, organisms living in tropical waters (which are less dense and viscous than temperate and polar waters) are smaller and have more appendages and projections than species in other seas.
3.2 The distribution of zooplankton
The distribution of zooplankton depends mainly on the movements of water on a global scale. Although the oceans are interconnected, complex ocean currents and macro-scale and meso-scale hydrographic structures mean that very few zooplankton species have a worldwide distribution. Species that do have a worldwide distribution have had to follow a long process of dispersion and adaptation since their appearance, overcoming hydrographic obstacles, such as areas of convergence and divergence, as well as large-scale currents, such as the Cromwell Current (186 mi [300 km] wide), which circulates eastward under the equator at a speed of three knots.
Zooplankton are suspended in different masses of water and adapt their physiology to its hydrographic characteristics, as well as to its specific values of temperature and salinity, and thus density. The adaptation of different species to a specific water mass gives rise to a very heterogeneous pattern of distribution because of the wide range of different bodies of water that may be found within a single ecosystem.
The adaptation of zooplankton communities to specific water masses responds to the classic view, contested by more recent ideas, that attributes a predominant role to hydrodynamics in explaining large- and medium-scale zooplankton distribution. It might be that the dynamics of water gives rise to the mechanisms that create heterogeneity in the distribution of planktonic organisms.
Zooplankton distribution is not only influenced by environmental factors, but also by biological factors resulting from their activity, morphology and physiology. Zooplankton distribution is heterogeneous in both space and time. It is generally, though not universally, accepted that spatial variability is due to physical factors, while temporal variations are due to biological factors. Much has been written about this controversy, although in reality both types of factors are interrelated in each particular area, and the preponderance of one of the two factors depends on the scale at which the phenomenon are observed.
On a large scale, ocean currents and cyclonic gyres mark the limits of the biogeographical regions of the different planktonic fauna. In areas where these types of currents meet, frontier zones or currents develop and physically limit the distribution of species. In the southern hemisphere, the confluence of the Benguela Current and the Agulhas Current (from the southern Indian Ocean) on the western coast of southern Africa gives rise to an area of divergence that acts as a frontier between the faunas of the South Indian Ocean and the Atlantic fauna. Oceanic-scale areas of convergence-divergence, such as the polar front in the southern hemisphere, act as natural frontiers preventing species from entering the Antarctic Ocean and Antarctic species from leaving.
Heterogeneity in space and time on an intermediate scale in the zooplankton (between approximately 6 and 62 mi [10 and 100 km], and between three months and 15 days) is governed by a series of more or less persistent hydrographic structures that cause dispersion and concentration. As mentioned before, zooplankton does not show a uniform distribution, but tends to concentrate in certain areas, where hydrographic phenomena on the most suitable scale occur. It appears to be evolutionarily positive that different species should have adapted their biology to the existence of more-or-less permanent hydrographic variability, as this means they can live together in the same marine system without dispersing very much. The organization provided by the spatial framework is of vital importance for the maintenance of the marine foodchains, in which the investment in seeking food cannot be greater than the returns provided by the food that is found.
Advective processes are among the best-known mesoscale hydrographic phenomena. The currents that regularly displace bodies of water over the continental platform are responsible for the zooplankton gradients along coastal zones. For example, the continuous nutrient-rich incursions of the California Current are the cause of the area's year-to-year variations in zooplankton biomass and change the structure of the zooplankton community by increasing the quantity of herbivores associated with the southern tip of the current. The proliferation of herbivorous zooplankton will lead to an increase in the populations of carnivores off California. In this way variations from one year to another in intrusions by the current determine the supply of prey for fish larvae and affect the growth of the annual populations of commercially important fish species.
The impact of advective processes on local zooplankton communities is not always so positive. For example, when there is a diminution of the upwelling in the north of the Benguela system, warm water enters from the Angola Current. These waters bear many medusas and siphonophores, which are such voracious predators that they may have negative effects on the rest of the area's zooplankton. In fact, the low concentration of copepods in the north of the Benguela Current (one third that observed to the south during the relaxation of the upwelling into surface waters) is thought to be due to the high predation by what is known as the gelatinous zooplankton present in the intrusions from the Angola Current. In other cases, such as off the coasts of Oregon and Catalonia, the displacement of a current parallel to the coast tends to mark the spatial limit of the platform zooplankton communities. Thus, the zone situated between the coastline is characterized by a zooplankton that rarely strays far from the coast, while on the other side of the current the community that develops is dominated by holoplanktonic species. Between them and associated with the current, there is a typical platform community that acts as a transition between the coastal and oceanic communities. Slackening of the current will allow meroplanktonic species to penetrate nearer to the coast, increasing species competition or leading to the dispersal and possible loss of coastal species.
A further type of advective process that is of great importance for zooplankton are the intrusions of continental waters from large rivers like the Mississippi. High nutrient concentrations make these inflows of water productive and are highest at the tip of the intrusion, where large agglomerations of zooplankton serve as food for fish larvae, whose population increases in accordance with the quantity of materials provided by the river.
Internal waves are also a source of variability in zooplankton communities. The flow of currents over the continental platforms and the relief of the seafloor together generate a series of internal waves associated with nutrient concentration phenomena and an increase in primary production. At the same time they act as transport waves favoring local concentrations of zooplankton. Their importance is clearly shown, for example, by the way some populations of decapod crustacean larvae move along the coast by the stratum closely associated with these internal waves, taking advantage of the food concentrations to survive and go through metamorphosis.
Hydrographic fronts act as areas of convergence, creating an important discontinuity in the horizontal distribution of water masses. They are associated with high plankton production, which gives rise to an increase in the production and biomass of zooplankton. Thus, fronts act as zones of accumulation as well as areas of zooplankton retention and transport. Along the front water rises and falls, thereby keeping the organisms close to the surface and preventing nutrient sedimentation by causing mixing processes. Localized fronts in the Ligurian Sea or in the North Sea show concentrations of copepod larvae that are much higher than the surrounding waters. In a front in the English Channel, concentrations may reach 75 times greater than the "normal" values for the surrounding coastal waters. This provides an ideal habitat for the proliferation of a rich carnivorous zooplankton, such as fish larvae.
While oceanic frontal systems act as zones of retention, those of the platform and slopes also act as barriers to dispersal. In a front located at the end of the continental platform in the western Mediterranean, large agglomerations of the larval forms of fish whose adult forms live in coastal waters have been observed. The larvae of these species might be dispersed towards the open seas, but the platform and slope fronts prevent their loss and encourage their later settlement. Many larvae of mesopelagic species are also associated with the front, thus increasing interspecific competition for food, but possibly solved by the high rate of plankton production associated with the front. As in other platform and slope fronts, the current circulating on the ocean side is responsible for the formation of the front, in which the waters of the platform collide with those of the slope. Therefore, this hydrographic barrier effect limits the dispersal of the zooplankton of the platform.
Tidal and estuarine fronts are also associated with greater plankton productivity and biomass than in surrounding waters. For example, in the Georges Bank, a tidal front acting as a barrier has been shown to prevent dispersal of planktonic species to the exterior. Furthermore, the external part of this front shows a high associated zooplankton biomass, which enters the interior of the bank by means of a compensatory bottom current. This current associated with the front is very important because it supplies the food needed to maintain the populations of icthyoplankton, vitally important for maintaining stocks of the locally exploited species of fish. In some estuaries on the eastern coast of Canada, it has been shown that there is a synchronization between the existence of an estuarine front and the development of the population of fish larvae. The front moves towards the exterior of the estuary, and many larvae are associated with the zones of mixing. Towards the interior of the estuary the larvae are very small and feed on copepod nauplius larvae. As the front reaches the mouth of the estuary, the larvae are found to be larger and feed on small copepods and then, eventually, on adults. The feeding adaptation of the larvae through increase in size ensured resources were not exhausted before the end of development.
The western coasts of continents show a regime of winds that favor the upwelling of deep water. These upwelling waters are so rich in nutrients that they are the starting point for productivity high enough as to place them among the most productive areas in all the world's oceans. The zooplankton respond by producing dense populations of opportunistic species, mostly herbivorous, resulting in communities that are little diversified and are dominated by calanoid copepods. The system can support a large biomass of zooplankton, the basis of the food supply of secondary consumers (fish and cephalopods).
The displacement of the surface bodies of water towards the open sea generates the divergent Ekman flow, used by many fish larvae to leave coastal areas. This displacement may, however, have negative effects because it removes the larvae from production centers. The solution adopted to avoid this forced transport has been the development of vertical migration, which situate individuals below the layer of water being displaced when the winds blow from the land to the open sea. On the coasts of Namibia and Peru it has been observed that when upwelling weakens, zooplankton communities become more complex as the number of species increases and the number of individuals of the dominant species falls. At the same time, the more opportunistic species of copepod are replaced by species with slower potential growth rates and lower egg production. The densities of copepods in the Benguela upwelling range from more than 4,000 individuals per cubic meter in weak upwelling to more than 12,000 when upwelling is strongest.
Very strong currents often produce a series of lesser divergent currents that displace large water masses to the exterior of the central body of the current. These water masses form eddies that encircle a zooplankton community similar to that in the current they originate from. These eddies are surrounded by other bodies of water with very different zooplankton communities. The continuous circulation of eddies means that their zooplankton community can maintain itself close to the surface and evolve. After a time, organisms from the surrounding water masses penetrate the eddy's interior, thereby mixing and changing the community's structure.
The development of isolated communities of plankton has been studied in eddies created by the Gulf Stream that may persist for several months. Similar structures--such as the rings or circles of warm water associated with the Kuro-Shivo Current or that to the east of Australia--act as minisystems maintaining very specific zooplankton communities in isolation for a certain period of time. The many species within these hydrographic structures develop almost without contact with the exterior. It has been observed that eddies in waters around Hawaii include a large number of fish larvae of species whose adult form is found in coral reefs. These larvae flee from the habitat of their progenitors because adult fish of the same species are the main predators of the larvae. They grow within the eddies until they reach the juvenile stage, and then they return to their adult habitat to gather. These retention mechanisms are considered very important in ensuring larval survival, since within the eddy they have easier access to more concentrated food resources than in the exterior, where organisms are more dispersed.
Other processes on a meso-scale contribute to increasing the zooplankton's heterogeneity in space and time. Phenomena such as residual currents associated with eddies or fronts, the formation of discrete layers of plankton accumulation, and circulation within marine canyons, all introduce variability into the mesoscale distribution of zooplankton. In the submarine canyons of the Georges Bank, for example, euphausiid density is high (more than 1,000 individuals per square meter). This helps to explain the area's high production, as the zooplankton biomass of the interior of the bank and its production do not explain how the needs of the fish population are met. The discovery of these dense concentrations of crustaceans, associated with the bottom currents of the bank's submarine canyons, closes the productive cycle.
Although meso- and macro-scale variability in the distribution, abundance, and production of zooplankton is mainly governed by hydrodynamic processes, it seems that on a small scale biological factors acquire greater importance. There is, however, a series of physical phenomena related to the formation of convection cells, or Langmuir cells, that may influence plankton distribution on a small scale 33-328 ft (10-100 m).
The factors that influence distribution
Heat loss from the surface water produces an increase in its density. Therefore, during the night it sinks and is replaced by warmer water from below. This generates convection cells, with water sinking and rising. Organisms with positive buoyancy can locate themselves in convergence areas, taking advantage of the rain of food from the surface. Organisms with negative buoyancy will tend to be in the divergence areas, while those with neutral buoyancy may concentrate at the base of the cell or at the surface. This physical support for the distribution of plankton favors the tendency of each species to aggregate in order to occupy the most suitable space. The heterogeneity achieved is quite varied, as a convection cell may range from a few meters to almost 656 ft (200 m) in size. However, factors related to the social behavior of species, their demography, life cycles, and intra-specific relations all play essential roles when it comes to explaining small-scale distributions.
The level of heterogeneity (variation in the number of species or of individuals) found in a horizontal kilometer is about the same as that found in roughly ten vertical meters. Most zooplankton organisms tend to concentrate in the top 656 ft (200 m)--the photic zone or a little below. For example, on the continental Atlantic platform of North America average annual zooplankton biomass in the first 164 ft (50 m) is 199 [cm.sup.3] per 1,000 [m.sup.3] of water; between 164-328 ft (50-100 m) it is 94 [cm.sup.3]; 35 [cm.sup.3] between 328 and 656 ft (100 and 200 m); and below 1,640 ft (500 m) it is lower than 20 [cm.sup.3] per 1,000 [m.sup.3] of water. These differences in zooplankton biomass are less pronounced in other areas, such as the Sargasso Sea or the Gulf Stream, but biomass values in the top 328 ft (100 m) are always at least double those found at 656 ft (200 m), and ten times greater than those found at 1,640 ft (500 m). Parallel to this greater abundance of zooplankton in the surface layers, there is a pattern of vertical displacement by organisms that is the result of an environment which is more active than the rest of the oceans.
Swarms of organisms
The tendency to live in groups, forming single-species patches or clouds, is a common strategy among zooplankton organisms. Causes leading to aggregation include differences or gradients in salinity and temperature, gradients of light intensity, the distribution of food resources, the presence of predators, and social behavior. The size of the patch or swarm depends on the species, and the size of the individuals varies with external factors and also during their development. For example, in copepods the swarms of nauplius larvae are generally larger than the swarms of adults, possibly because there is a larger number of individuals in the swarm. At the same time, a swarm of adults may increase if it finds an accumulation of food, or decrease if it detects the presence of a predator. Thus, swarms function like an accordion and fluctuate in size.
The size of the zone where a species occurs may fluctuate during the day, over its development, or depending on the areas where it is found. A species may show phases of aggregation and of dispersal. This fluctuation in distribution makes it difficult to assess population density using conventional methods (nets or suction pumps). The density at the center of a copepod swarm is 100-1,000 times greater than the average density of the total population of the area. Furthermore, the role of prey or predator in the trophic relationships of the community changes greatly depending on whether the copepods are grouping or dispersing.
The advantage or adaptive value of swarm formation is still hotly debated. If we look at a swarm of sardine larvae, we will see that the individuals at the center of the swarm are very well protected from predators: They are, however, relatively isolated from the food supply on the edge of the swarm. One option is to remain together during the day to avoid predators and disperse at night to feed. In general, and on the scale of a system, the formation of aggregations facilitates the distribution and recycling of available energy. Solitary individuals have to displace themselves continuously to capture prey, and it is also unlikely that they will be captured, so there are many possibilities that they will be lost to the trophic chain (at least in the top 656 ft [200 m]). Zooplankton excreta contains vital nutrients for the phytoplankton. Products excreted by swarms are easier for algae to capture because they are much less dispersed than those produced by isolated individuals.
The characteristics of a swarm or aggregation vary greatly from species to species. However, if we compare two species of copepod, Calanus finmarchicus and C. tonsus, we can see that their behavior is different. C. finmarchicus forms swarms that last between 12 hours and a few days, which then break up and reform again a few days later. These swarms are between 3-10 ft (1-3 m) in diameter, with a density of more than a million individuals per cubic meter. C. tonsus forms swarms ranging from 328 ft to 0.62 mi (100 m to 1 km) in diameter, with a density of 10,000 individuals per cubic meter. The average distance between the individuals in a single swarm varies greatly. In copepods it may be less than 0.4 in (1 cm), while in euphausiids it is from 1-2 in (3-5 cm), and in large medusas it may be 39 in (100 cm). Studying copepod swarms living on coral reefs has shown that a single group may form swarms with different characteristics. They form dense single-species aggregations about a cubic meter in volume just above the surface of the coral colonies with densities of more than half a million individuals per cubic meter. There are even swarms consisting of individuals of the same size but of different species, showing no social relationship. Other swarms may show social behavior, as many fish do.
The swarms of a single species show a differentiated demographic composition. For example, in aggregates of medusas like Ropilema sculentum (with an umbrella 8-16 in [20-40 cm] in diameter) the individuals of the same size are grouped by their ability to swim, forming a group of swarms within a larger swarm. All the different swarms move together to find food, at a speed of about 656 ft (200 m) per hour. In many species, swarming was originally reproductive. All the individual members of a swarm were produced at the same time by an adult population. For example, the adults of a swarm of sardines all lay their eggs at the same time, so the eggs form a single aggregate at the mercy of the currents. As the individuals grow, the swarm loses a part of its population, especially those on the periphery, while the others continue together until they reach the juvenile, or even adult, stage.
3.3 Vertical displacements of zooplankton
Vertical displacement of zooplankton species is due to various causes, although light is the factor that appears to trigger migration. Vertical migrations may also have an ontogenetic component, as swarms of larval, juvenile, or adult forms of a single species may follow different migration patterns. Although adult chaetognaths move throughout the water column, juveniles form swarms at very specific depths, close to the level where the swarms of small copepods they prey on are most abundant.
Most species rise to the surface during the evening or night, and descend when the new day arrives. As has been shown for some species of copepod and other crustaceans, very slight changes in light intensity at the surface cause an increase or decrease in displacement, depending on the frequency of the stimulus. Some types of obstacles that cast a shadow on the receptor organism also stimulate vertical displacement. Although most migrations take place in the upper layers of the water column, they are also habitual in organisms that live below 1,640 ft (500 m) depth. The difference is that in the photic layer the rhythms of activity are very short, because they respond to the day-night cycle, while at greater depths the slower rhythms of migration last a few days.
The speed and intensity of vertical displacement depend on the group and the hydrographic conditions of the geographical area. Medium-sized copepods, for example, can rise 98-197 ft (30-60 m) in an hour, while euphausiids can rise 328-1,312 ft (100-400 m) in an hour. Some more littoral species, such as the larvae of the acorn barnacles of the genus Balanus, only rise 49 ft (15 m) in an hour, although for this organism it is important for the larvae not to stray too far from the habitat of the adults because, if they migrated large distances, they would be swept away by currents. Descent, using gravity, may be faster with the consequent advantage of escaping from predators. Furthermore, in many species migration may be inverse, that is to say, descending at night to evade predators.
Migration represents a certain metabolic cost, compensated by the benefits it provides. The evolutionary meaning of migration is based on the relevance of these benefits. On the one hand, displacement within the water column is related to the search for food. Many copepod populations are found below the level of maximum chlorophyll and rise to eat during the night, while other species remain at the surface where they graze on the phytoplankton. The migration of copepods leads to a synchronous displacement of their predators, in search of rising or falling swarms. Many predators, such as fish larvae, hunt visually and so during the day their prey migrate towards less illuminated areas, making them harder to locate. Many researchers consider migration as a strategy to escape predators. A different, metabolic, explanation is that copepods produce a larger number of eggs in warmer surface waters and show higher growth rates. In deeper, colder waters their metabolism and growth rates are slower.
All researchers agree that migration is governed by a set of intimately related biological factors. The following is a typical explanation of migration. A swarm of a particular species of copepod that occurs at 328 ft (100 m) depth during the day, starts to move towards the surface when the sun sets. The swarm displaces in a regular way, so that the individuals at the top remain at the top. When they reach the layer of maximum density of phytoplankton, they begin to graze continuously, and the individuals that are satiated begin to descend while the other members of the group rise. At dawn, the population descends rapidly, with stomachs full of algae that make them visible to predators.
While at the surface they eat and excrete continuously, and because their metabolism is faster, they also produce a larger number of eggs. In fact, egg production occurs mainly at night, as has been observed in the copepod Acartia pacifica in the Sea of Japan. During the day production is about 30 eggs per cubic meter per hour, while at night it is about 150. Once they have reached the colder layers they reduce their movement and, as their metabolic activity decreases, they spend their time digesting the prey captured during the night.
Many zooplankton organisms, such as chaetognaths and medusas, are transparent and during the hours of light they are almost invisible to their predators who hunt by sight, and so they can stay at the surface. But when they eat, the prey ingested makes them visible to predators, and they have to leave the illuminated surface zones. They go down to darker layers where the temperature is lower, and where they can digest their prey more slowly and wait for the night or the following day--depending on the speed of digestion--before rising to hunt again.
There are many species that in certain circumstances do not migrate. If a predator is in an area with sufficient prey, then it need not migrate and thus saves the costs it would represent. If the center of the swarm coincides with an adequate concentration of available food and no predators are detected nearby, the swarm opts not to move.
Apart from trophic circumstances, physical factors also alter the migration of many species. The existence of a clearly formed thermocline may act as a barrier to migration. An example of the action of the thermocline is the vertical distribution pattern shown by zooplankton groups in the north of the Benguela ecosystem. In this area the intrusions of hot water from the Angola Current give rise to a strong thermocline of about 43[degrees]F (6[degrees]C), at a depth of about 164 ft (50 m). Many species of medusas, chaetognaths, and amphipods concentrate just above the thermocline. The high concentrations of copepods at the surface throughout the daily cycle and the high cost of crossing the thermal discontinuity of the thermocline, are the reasons why some species do not move, or only perform short movements between the thermocline and the surface.
One way in which a plankton community gains from migration is related to copepod excretion. They release their excrement in the upper layers in the form of fecal packets, contributing to nutrient remineralization, because bacteria close to the photic layer can decompose the products of defecation as they fall.
Flagellates are also important and in addition to showing heterotrophic nutrition, like most protoctists, they also possess pigments that make them autotrophic. Zooplankton organisms that ingest these protoctists manage to increase the yield of the planktonic trophic chains by more than 50%.
The fact that most species of the plankton zone are concentrated in the photic layers raises the question of density dependence. This implies that the different species spread out--often by migratory movements--within the water column, occupying levels that are often highly discrete. For example, studies of the vertical distribution of some species of copepod in the Black Sea showed that each species located the center of its population at a specific depth. So Acartia clausi was 30-36 ft (9-11 m), Paracalanus parvus between 13-16 ft (4-5 m), and Oithona nana was between 16 and 36 ft (5 and 7 m) deep.
Density-dependent problems also arise in competition for food. For the larvae of different fish studied on the coasts of Britain, one solution was to select the type of prey according to size and to the level of distribution of the different species. Thus, one species specialized in the predation of one species of copepod, while other larvae ate small copepods of another species. This small-scale prey selection process (in the top 197 ft [60 m]) appears to be vital for the survival of zooplankton communities as varied as those found in surface waters.
Other examples of habitat compartmentalization are the distribution of euphausiids swarms at different levels in the Benguela ecosystem, and the selection by hyperid copepods of different species of gelatinous zooplankton (situated at different depths) as substrates for establishment and for feeding when environmental resources become scarce. In zooplankton communities, interspecific relations are much more subtle than was thought until recently. One case is the compartmentalization of the habitat between the larvae of the anchovy and the saurel in the North Atlantic. Anchovy larvae are less mobile and their small mouths allow them to capture small prey, but they form large swarms. The more active larvae of the saurel capture larger prey that is less common but energetically more profitable.
3.4 Interspecific zooplankton relationships
Interspecific relationships at a small scale and an intermediate scale are reflected in the structure of zooplankton trophic chains, while in zooplankton communities biological processes are coupled to physical processes on the same scale.
Trophic relations are usually highly complex, as it is necessary to consider not only the abundance of prey and predators, but also the possibility of the two coming into contact in the planktonic environment. This is exemplified by the trophic relations in the communities of the coast of the island of Vancouver.
An example of the complexity of the trophic chains in the plankton system is a community consisting of 1,000 individuals per 1.3 cubic yard (1 [m.sup.3]) of the copepod Pseudocalanus minutus (1 mm in size), 400 of the copepod Calanus plumchrus (4 mm), and 10 of the euphausiid Euphausia pacifica (20 mm), which are all competing to graze on a population of diatoms of the genera Chaetoceros (23 microns). The euphausiids consume most, reducing the population of Chaetoceros by 50% and leaving the rest for the copepods. The copepod Calanus plumchrus compensates its diet when it finds a swarm of a flagellate of about 10 microns, while Pseudocalamus minutus eat Chaetoceros.
After a few days, large quantities of euphausiid eggs are produced, and in three or four weeks these will give rise to a new generation of larvae that compete with the swarm of Calanus plumchrus to eat the flagellates. The two species thus have a higher rate of production than Pseudocalamus minutus. The development of swarms of larvae and of Calamus plumchrus compared with that of P. minutus means that they are detected more easily by the larvae of the salmon Oncorhyncus gorbuscha, up to 8 mm long. Possible secondary predators of salmon larvae include jellyfish (considered voracious predators of fish larvae) whenever swarms of the two coincide. Jellyfish also compete successfully with fish larvae, consuming larger quantities of copepods. At this stage salmon larvae prefer copepods of smaller species (and their larval phases), while the medusas take the larger species.
Recent studies in Chesapeake Bay have shown that in one day a population of the scyphomedusa Chrysaora quinquecirrha can reduce the copepod community by more than 90%.
Biological and physical processes
The development of a species from its origins until it reaches sexual maturity follows a spatial and temporal development path that depends on the structure and dynamics of the bodies of water it comes across during its life. One example is the life cycle of the herring (Clupea harengus) off the coasts of Scotland. The adults spawn in an area of the continental platform where turbulent conditions favor the eggs' buoyancy, enabling them to float. A current bears the eggs north and the larvae find food easily when they hatch, as they are near the densest plankton patches. As the larvae grow, they drift within the same water mass that contains a rich zooplankton community. Calanoid copepods growing at the same time give rise to several generations that allow the larger larvae to find swarms of larger prey. The larvae have already reached juvenile form and size when the current bearing them deviates towards the coast, forcing them to migrate towards the bottom and to swim actively back to their area of origin. During their development, the water mass protects them from many predators without isolating them from their food supply.
In the high seas, life in the depths is a little different from the description already given. That part of the ocean that is deeper than 0.62 mi (1 km) occupies almost 75% of the space where life is found on Earth. This large space is totally lacking in light, even ultraviolet, and on an oceanic scale varies little in temperature and salinity. The organisms that develop in these quiet water masses are of relatively little-known types because they are difficult to trap with traditional sampling techniques.
Recent studies with submarines have made it possible to observe a living system that is much more complex than previously thought. Organisms are widely dispersed in the oceans and, except for some crustaceans, displace themselves slowly. Gelatinous organisms--such as siphonophores, medusas, salps, ctenophores, and pteropod mollusks (sea butterflies)--are the most common. They are very large in comparison with surface forms and have a life expectancy of several years. They have delicate transparent bodies because they do not need to protect themselves from ultraviolet light. They have neutral buoyancy and although they are carnivores, they can pass long periods without eating. Some are strong swimmers, capable of moving many kilometers a day.
The scarcity of resources has meant that gelatinous organisms develop very sophisticated hunting techniques. For example, a colony of physonectid siphonophores no more than 1.6 ft (0.5 m) in size extends a complex net of fine tentacles that may reach 66 ft (20 m) in diameter. Other species develop interspecific relations, such as hyperiid amphipods, which live in association with medusas or even within their gelatinous bodies. They exploit some of the prey captured by the medusa, as well as eating the medusa itself if necessary. Many of these gelatinous organisms form dense populations, especially the physonectid siphonophores, which have gas in their pneumatophores, and their distribution in the deep sea coincides with what is called the deep scattering layer (DSL). The fact that they are so common has led to talk of a predator zone in the middle layer of the water, spread throughout all the oceans.
4. Secondary and tertiary consumers: large invertebrates and vertebrates
4.1 A bountiful but dangerous environment
Lacking the refuge and cover provided by the substrate, the organisms inhabiting the pelagic environment are surrounded by food, but also run the risk of being eaten. As already pointed out, in addition to the permanent plankton there are many eggs and larvae that are there temporarily. It is not uncommon for the larval stage of some large predators to be consumed by adults of species that form part of their normal prey. Most organisms pass through different stages in which they are primary consumers when they eat phytoplankton, secondary consumers when they change to eating zooplankton, and finally tertiary or greater consumers when they reach adulthood.
In general, pelagic organisms show greater diversity in tropical regions than in temperate ones, which in turn show more diversity than cold ones, However, especially on the continental platforms, the specific diversity of pelagic organisms in each biogeographical region is lower than that of their benthic equivalents. The diversification of forms is closely related to the heterogeneity of the environment: the larger the number of microhabitats in an environment, the larger the number of forms that can develop in the ecosystem. The relative homogeneity of the pelagic medium does not lend itself to diversification.
The fact that few forms are possible means that natural selection is undeniably more severe because it is not possible to avoid interspecific competition through specialization. However, the abundance of pelagic fish is notably greater than that of benthic species, given that they are intimately related to the layer of most important primary and secondary producers, and because the absence of high diversity favors the concentration of biomass in a few species.
The main taxonomic groups represented at the level of secondary or tertiary consumers in the pelagic environment are fishes, some crustaceans (especially euphausiids and galatheids), some mollusks (squid and cuttlefish), birds, and mammals.
In a pelagic environment it is not possible to apply most of the strategies that benthic organisms employ to improve their chances of living and leaving offspring (adopting cryptic coloration, burying themselves in sand, seeking shelter among rocks, covering themselves with other organisms to blend in with the substrate, etc.). In the pelagic medium, the only appreciable differences in a given point of the water column are the light colors (above) and dark colors (below), with variations due to reflections and waves. The only possible cryptic coloration is the lack of color, or what is called countershading, which consists of having a dark, shaded dorsal surface which will not stand out against the ocean bottom when seen from above, and a clear, reflective ventral surface that may be mistaken for the surface when seen from below. This type of coloring also makes the organisms less conspicuous because the dark dorsal color compensates for the illumination it receives from above, and vice versa. Most organisms that live in the euphotic zone of the pelagic environment have this sort of coloring. Other defense strategies are based on the velocity of displacement or in the grouping of many individuals into compact patches. Despite this, predation is intense and most pelagic organisms are eaten before they reach adult age. In these conditions of exposure to predation, populations obviously require strategies that ensure sufficient survivors for reproduction. Thus, currently, the only species in pelagic ecosystems are those that have achieved this type of response to intense selection.
These responses by the population include strategies based on rapid growth and the production of many offspring, a tactic present to a varying extent in small, medium, and some large species. Another specific strategy consists of being large from the beginning and protecting the young. Both sharks and cetaceans use this type of survival strategy. Finally, the pelagic environment attracts organisms that are temporary residents there and eat the permanent residents, and then reproduce outside this very risky environment. This is the strategy adopted by seabirds and pinnipeds.
Genuinely pelagic fish usually produce large quantities of eggs, some as many as a million. The small fish grow and mature as quickly as possible in order to reproduce before they are eaten; most small fish have a lifespan of less than six years, and start to reproduce when they are three. Strictly pelagic octopus and cuttlefish usually only live for one year and most females die after reproducing. Other medium and large fish tend to grow and reach the adult state rapidly, and so contribute to reducing the level of predation by other species. Some tuna grow until they are a thousand million times heavier than when they left the egg! In general terms, the transference of energy to the pelagic environment follows the ecological principle that adults increase their adult size and reduce their biomass with increasing distance from the primary producers of their trophic chains. This principle has many exceptions in any environment, and some of the most notable are in the pelagic ecosystem. The largest animals that have ever existed on the planet shorten the food chain and basically eat zooplankton.
Migrations are also a common characteristic of the pelagic environment, and most nektonic species migrate in one form or another. Many organisms, especially those of oceanic tropical regions, show daily vertical migrations. Mesopelagic fish are an example of vertical migration of great importance. However, horizontal migrations are more spectacular. The distances that can be covered by the larger organisms of the pelagic environment are impressive: There are reports of migrations of nearly 10,000 mi (18,000 km). Sometimes the precision of migration is surprising, especially in organisms that reproduce in exactly the same place as they hatch. Bearing in mind that this environment is almost entirely lacking in visual references, this is an astounding achievement.
Productivity in pelagic systems
As explained before, the distribution of productivity in the ocean is not at all uniform, although superficially all seas look the same. In general terms, the continental platforms are much richer than the open sea, seas at high latitudes are richer than those in the tropics, and upwellings are the most productive areas. The poorest areas of the pelagic environment are, of course, the centers of the large gyres, one in each hemisphere and in each ocean. The richest areas are those where upwellings favor extraordinarily high productivity. Pelagic species are most abundant in regions where productivity is very high.
The ecological efficiency (i.e., the proportion of energy transferred from one trophic level to the next) also changes greatly. Areas of upwelling are much less efficient than tropical areas, as their production is so high that there are no effective mechanisms to use it fully, and much sinks to the bottom.
The existence of many strata of diatom remains and phosphorite deposits is clear proof of this considerable loss of production. The situation is totally different in tropical oceanic ecosystems; their primary productivity is much lower and their ecological efficiency is much higher, and all the organic material is used at the top of the much deeper water column. The production that occurs in the photic zone is consumed, degraded, and remineralized in the top 1,640 ft (500 m). There are almost no organic remains on the ocean bottom in the central regions of the oceanic gyres. Even though the transfer coefficients between levels are three times greater in poor ecosystems, the difference in primary productivity between rich and poor ecosystems is usually very large.
The abundance and reproduction of pelagic species depend not only on the ocean region, but also on the annual cycles of the species they eat. Production cycles show wide amplitudes (i.e., there is a large difference between the average minimum and maximum productivity within a year) in high latitude regions where periods of maximum productivity are short. Pelagic organisms in these areas have very short reproductive seasons, and in the case of the herring (Clupea harengus) it only lasts two or three weeks. The synchronization of reproduction is thus crucial in an environment where high production favoring larval food supply lasts only a short time.
In temperate upwellings, high productivity lasts longer and reproductive seasons may be much longer. Spawning by the California sardine (Sardinops caerulea, S. sagax) may peak over a period of three to four months. Furthermore, depending on the area where the population spawns, there may be a single peak for the entire year (for example to the south, off California), or two (for example in Magdalena Bay, in the southwest of the Baja California peninsula). In cold years, spawning in the first region may be limited to a few weeks, but in hot years it may occur in almost every month of the year.
In tropical zones, spawning usually occurs throughout the year, as reproductive cycles show minimum amplitude between different months. In this case, spawning may be restricted to an area within the oceanic gyre that is upstream from the area most suitable for larval growth, so they will drift to areas where they have a greater chance of surviving.
Exploitability of the pelagic environment
In the middle of the 20th century when catches were growing faster than world population, there was a generalized optimism that the ocean might represent humanity's greatest food reserve. Serious researchers calculated that total world catches could reach 200 million tons before the year 2000. This goal now appears quite unattainable. Potential catches have recently been recalculated, suggesting that an annual catch of 140 million tons might be possible, if current catches were adequately administered and as yet unused traditional resources were also exploited.
Although it is clear that the potential of the pelagic environment is much greater, the exploitation of these large volumes is not as simple as it once seemed. Some species cannot be caught economically using contemporary technology. Even if new technologies gave humanity access to these non-traditional resources, we would be in a difficult dilemma. Should we seek to increase catches by catching species at lower trophic levels? The need for raw materials and food might require a decision of this nature.
Most fish consumed today belong to higher trophic levels and changing fishing objectives would have important repercussions because humans would come into competition with these species for food. We may well end up exchanging one kilogram of tuna for 10 kilograms of lantern fish (Myctophidae). Maybe future imagination will find practical ways of solving the oceanic paradox of a nutrient-poor illuminated photic layer resting on a nutrient-rich layer lacking light.
4.2 Typical pelagic consumers
Trophic chains in the pelagic environment are generally short. Furthermore, apart from a few exceptional cases, they are poorly defined. The smallest fish, for example, are primary and secondary consumers, as they eat phytoplankton and zooplankton. The smaller secondary (mid-sized pelagic) consumers basically eat zooplankton, although they also consume juvenile fish. The larger members of this group are definitively ichthyophagous (fish-eating) and eat the smaller pelagic species.
Squid and cuttlefish exemplify the poor definition of trophic chains in pelagic environments. They consume fish and large plankton, and in turn they are food for a wide range of higher-level consumers. One particularly interesting trophic chain occurs in tropical areas where mesopelagic fish (especially Myctophidae) eat zooplankton and are eaten by tuna. Most researchers refer to production of zooplankton-eating fish and their consumers as tertiary production; although this is not strictly true, it is a practical and convenient approach.
Fish and small crustaceans
The larvae of many species of pelagic and benthic fish live in the plankton during a short but important part of their life. Their enormous abundance means they play a large role in the energy flow of the ecosystems.
Apart from these organisms, normally studied as part of the zooplankton, only a few types of adult small-sized fish are found in abundance in the pelagic environment: some Clupeiformes (herring, sardine, and anchovies); the mesopelagic species, mostly Myctophiformes (lantern fish); and skippers and related species (Scomberosocidae). Of course, there are many other species of fish in the pelagic ecosystem, but they are much less abundant and much less important within the community's energy flow.
Together with some crustaceans and other organisms of the micronecton, small fish represent the most important link between primary production and secondary production within the rest of the trophic chain in the pelagic environment. They are very abundant compared with the other species and form the basic prey of larger fish, in both the pelagic and in much of the benthic environment. This is partly explained by the fact that these small fish (especially Clupeiformes) may obtain part of their food from the phytoplankton given that their symbiotic intestinal bacteria can produce cellulase. The resulting shortening of the trophic chain means that these populations can reach a very high biomass.
Sardines and anchovies
Although more than 300 species of Clupeidae belonging to 80 genera are recognized in the specialist literature, the two main genera Sardinops and Engraulis (sardines and anchovies) represent more than 60% of the total world catch of Clupeiformes, which in turn constitute about 20% of the total world sea and freshwater fish catch. Both genera include various species or populations of sardines and anchovies of warmish waters where temperate and tropical waters mix. Most of these areas are found where upwelling occurs, on the eastern barriers of the great oceanic gyres, off California, Peru-Chile, the Canary Islands, and Benguela. However, one of the most important regions where these Clupeidae live is around Japan, where there is no upwelling. In each of these areas of special abundance, the populations of these two genera represent the dominant small fish of the system. Other genera of Clupeidae, such as Sardina or Sprattus, occupy the same position as Sardinops in the Canary Current and in the Mediterranean, where they are also very abundant.
One of the most surprising characteristics of these fish is that their abundance varies drastically over very short periods of time. The best-known and most impressive example is the Peruvian anchoveta (Engraulis ringens), catches of which fell from nearly 13 million tons a year to almost nothing in less than a decade. The populations of sardines (Sardinops) in Japan and in Peru and Chile, on the other hand, grew so much that the combined catches reached more than 10 million tons in less than ten years. The relative abundance of one or the other genus has been checked using historical records, and when sardines were abundant, anchovies were scarce, and vice versa. Even so, it is more interesting to know that these alternations occur in parallel in areas sometimes separated by whole oceans. The coherence of the synchronic behavior of sardines and anchovies in Japan, Chile and Peru, and California, and in their simultaneous changes (although they are out of phase, as the anchovy is abundant when sardines are abundant in the rest of the systems and vice versa) in the Benguela Current seems to demonstrate that there is some cyclic factor of a planetary nature that determines the dominance of one population or the other.
Some upwellings have almost anoxic areas of sea floor that preserve organic remains especially well. Analysis of these areas has shown that the scales of many fish are preserved perfectly in strata of deposits, called laminated sediments. This type of deposit has been analyzed off Baja California, both in the ocean and in the Gulf of California, and also in South Africa. Samples are also now being studied in other regions. Although it used to be thought that fishing was the factor determining the relative abundance of the populations of anchovies and sardines, analysis of scales found in laminated deposits of several systems has shown that these populations typically showed large fluctuations in abundance long before they were exploited by human beings. Independently of the fact that fishing magnifies and accelerates changes in abundance, they occurred in the past and will surely continue to occur in the future, as a reflection of the profound changes, as yet little-known, that affect an entire ecosystem.
Herrings (Clupea harengus) are particularly abundant in the north-eastern Atlantic, where they are one of the most traditional catches. They reproduce close to the substrate and deposit their eggs on the seafloor near the coast. When the eggs hatch, the larvae form part of the plankton. Spawning is closely linked to environmental conditions: The date of spawning can be calculated for each population to within roughly a week. Furthermore, it has been shown that about 80% return to spawn in the same place where they hatched, and the remaining 20% allow recombination between populations. There are also herrings in the northern Pacific, although they are considerably less abundant than in the Atlantic. In terms of biomass, herrings are the most important clupeids that make use of periods and areas of high productivity in the cold-temperate seas.
Other clupeids are coastal and channel primary and secondary production from the continental platform, the most productive areas. There are also Clupeidae in more tropical regions although their biomass is much less than those of temperate and cold-temperate waters, which produce about 80% of all the catch of clupeids. The most abundant genera include Brevoortia, (the "menhaden" of the coasts of the Gulf of Mexico and the southeast of the United States), Sardinella (the anchovies of the Atlantic, Indian and Pacific), and Opisthonema (of the tropical coasts of the American Pacific).
Small mesopelagic fish
In regions further from the coast, the main fish are oceanic mesopelagic species that live in the intermediate layer of the deep seas. They normally live at depths of between 656 and 3,281 ft (200 and 1,000 m) in the photic (epipelagic) layer, between the level where 1% of the incident light penetrates and the greatest depth light reaches. They are usually distributed beyond the slopes around every continent and island. These areas account for about 22.5% of the total surface area of our planet's oceans.
Many species perform daily vertical migrations, rising to the surface in the afternoon to eat in the zooplankton-rich waters. Some even arrive in the surface layer during the night. When the sun comes out, they descend back to their usual depths. They are so abundant that they form most of the deep scattering layer, an echo that appears in deep soundings and moves vertically between sunrise and sunset. Their eggs and larvae form part of the meroplankton and are the highest biomass of any type of vertebrate in the oceanic plankton. They form an unexploited reserve of millions of tons.
This group of fish, the largest portion of the biomass of the mesopelagic zone, is made up of about 700 species in the entire world. Their relatively large eyes allow them to see in the twilight conditions of the mesopelagic layer, and many have tubular eyes to concentrate light. Their jaws can open very widely, and catch prey and eat pieces of dead animals or even entire corpses of their own size. They possess numerous photophores on the ventral surface, said to confuse predators that hunt them from below against the scarce light that penetrates from the surface of the sea.
There have been limited efforts to catch these fish, especially in South Africa. Most are processed for fishmeal and oils, but they contain so much oil that these products are difficult to extract using conventional procedures, because they clog the machinery. The direct consumption of some of the larger species has had an unenthusiastic reception, mainly because some have high concentration of waxes and esters in their flesh. Their exploitation is difficult because of their small size (most species are between 2-4 in [5-10 cm]) and the fact they are very dispersed (one individual per 1,308 cubic yards [1,000 cubic meters]), quite unlike the clupeids, which form very compact masses that are profitable to exploit.
Mesopelagic fish basically eat zooplankton and in turn form the main food of many larger species, such as tuna, mackerel, squid, pinnipeds, and cetaceans, especially some rorqual whales and many dolphins.
Mesopelagic fish form part of the trophic chain, actively transporting energy towards the bottom. As opposed to the passive sinking of corpses and waste products, mostly consumed in the layer where they originate or in the layer immediately below, this form of transference is based on the daily migration of organisms from deeper layers to the surface to feed. Here they are, in turn, food for organisms of the underlying layer, and those of lower layers, and so on. The original conception of a photic zone producing surplus biomass that slowly sinks and is consumed by different organisms is difficult to reconcile with the dynamic recycling of nutrients within each level of the long water column of the deep oceans.
The Scomberesocidae, such as the skipper (Scomberesox saurus) and other similar species, are pelagic fish 8-14 in (20-35 cm) long when adult. Their abundance makes them an important link in the trophic chain and they connect the zooplankton's secondary production to larger fish, especially tuna, and many birds. Although they do not reach the volumes of the two groups discussed above, their importance lies in the fact that they live close to the surface and far from the coast. There are scomberesocids in the Pacific and the Atlantic.
On the Pacific coast of the United States calculations suggest a biomass of almost 500,000 tons. Japan has been one of the main countries fishing these species and recently catches have reached 250,000 tons. The scombereosocids belong to the order Beloniformes that also includes other pelagic species, such as halfbeaks (Hemirhamphidae) and flying fish (Exocoetidae), relatively important in coastal tropical waters.
In the Antarctic Ocean there are two species of small fish that occupy an equivalent trophic level: Pleurogramma antarcticum and Notolepis coatsi. Both are relatively abundant, consume zooplankton and are eaten by larger animals. The first is eaten by penguins and seals, and the second by rorquals.
Some pelagic microcrustaceans exist at this trophic level of phytoplankton and zooplankton consumers. Euphausia superba, Antarctic krill, is usually considered as a component of the zooplankton and is not discussed here. However, some galatheids such as the Chilean crayfish (Munida gregaria) of Chile and New Zealand, or the Mexican shrimp (Pleu-roncodes planipes), are very abundant and of great importance in the trophic chain in some areas.
During the first years of their lives, these small reddish crabs, (which in Chile are called langostinos, or crayfish) have a pelagic phase and later become benthic. During their pelagic phase they form extraordinarily abundant concentrations and, on occasions, they even get beached in large quantities. They eat both zooplankton and phytoplankton, and so are similar to the clupeids, inasmuch as they do not channel productivity towards higher trophic levels. The Chilean crayfish has been caught commercially in Chile, processed to obtain the relatively small tails, and then exported at a good price.
Mexican shrimp are a favorite food of the tuna during the part of their annual migration when they penetrate the California Current, when they may even form 85% of the tuna's food. They are also among the few organisms grey whales (Eschrichtius robustus) eat during their stay in the warm-temperate waters in the coastal areas of the Baja California where their young are born during the winter season.
Medium-sized fish form the least defined category of the entire trophic chain found in the pelagic environment. Some are only slightly larger than small fish and their food includes zooplankton, microplankton, and the juvenile stages of other fish and squid. The most abundant genera of medium-sized fish belong to the scombrid family (Scombridae), the mackerel (Scomber) and the Spanish mackerel (Scomberomorus), or to the carangid family (Carangidae), such as the saurel (Trachurus) and jacks or kingfish (Seriola).
Some important genera that do not belong to these two families are Mallotus of the osmerid family (Salmonidae) and Micromesistius, including the blue whiting (M. poutassou), a member of the gadid family (Gadidae). Micromesistius, exceptionally for a member of the normally benthic gadiforms (Gadiformes), is mainly pelagic but tends to form extensive layers rather than dense masses. The capelin (Mallotus villosus) is a mainly arctic gadid found to the north of the polar front, off the coasts of Canada and Norway, and in the Barents Sea. It is fished in the north and the southeast of the Atlantic. The catch of each of these genera has exceeded 100,000 tons a year, a figure that demonstrates their abundance. Many other genera of these two families are also present in the pelagic environment, especially on the continental platforms of tropical seas.
Another important family in this category is the Sphyraenidae, represented by the barracudas (Sphyraena), medium-sized predators that basically eat small fish and squid.
The bathypelagic (between 1,640 ft [500 m], the lowest level with light reaches, and 9,842 ft [3,000 m]) and abyssal (down to 6 mi [10 km]) subdivisions form most of the pelagic environment. The ecosystem of these deep seas is almost totally heterotrophic, dominated by catabolism, and allochthonous, in the sense that the energy necessary for its existence has to come from somewhere else.
In addition to the absence of light, most of the water is cold and the seasonal variations in temperature are almost imperceptible. The physical and chemical characteristics of the water correspond to the high latitudes where they formed. Water from the circumpolar areas takes a long time to flow along the seafloor to the equator. The deep water of the Atlantic, for example, is probably 200 to 300 years old, while that of the Pacific is definitely 1,000 years old. Variations in the environment of the deep ocean make sense only on a geological time-scale.
Just as upwellings on the surface are very important because they bring nutrient-rich water up to the photic zone, turbidity currents appear to be the most relevant phenomena in the deep sea. Immense cascades carry sediments down to the poor seafloor, bearing organic remains and covering part of the deep fauna.
It has been shown that the abundance of organisms diminishes with depth in a way that is exponential (but not regular). There is a clear tendency for organisms to be less dense as depth increases, probably to increase metabolic efficiency and conserve energy, as it reduces their need to maintain themselves floating at a specific level. The deeper the fish lives, the greater its water content in comparison with proteins, carbohydrates, lipids, and skeleton.
Bathypelagic fish show the most profound modifications found in fish living at any depth. They have large jaws and teeth, and many possess barbels to attract prey. Deep-sea devils (Ceratiidae), for example, have a photophore-bearing "lure" appendage above their usually very small eyes. Many females seem to emit pheromones to attract males that have a highly developed sense of smell. This helps the different sexes to find each other in a world without light. Sexual dimorphism is common and can be extreme; the males of Ceratias are much smaller than the females, and when they locate a female they attach themselves and gradually degenerate until they are little more than a small sac with reproductive organs. Bathypelagic fish undergo even more profound changes than the benthopelagic fish, which are much more related to the seafloor. These fish, such as the ghostfish (Chimaeridae), the ratfish, and other Macrouridae and some rays look much more familiar.
Squid and cuttlefish
Cephalopods, especially the squids (Loligo, Todarodes, Abralia, Illex, etc.) and the cuttlefish (Sepia) are a very important component of pelagic ecosystems, although only a minimal part of their population is exploited by human beings. Nearly all the squid catch comes from waters less than 656 ft (200 m) deep, a very small part of the oceans. Larger squid live at greater depths.
The abundance of larger species of squid (Architeuthis), has been estimated partially on the analysis of remains (especially of the mandibles) found in the stomachs of sperm whales. It has been calculated that these large mammals alone consume 100 million tons of squid a year, in other words, more than the total caught by humans throughout the world. In the Antarctic, where predation of squid by cetaceans has been studied, it has been calculated that squid consumption by sperm whales represents about 35% of the total consumed by all predators.
Pelagic squid mainly eat small fish although they may also consume some crustaceans, including copepods and galatheids, as well as pteropod mollusks and other squids. Squids' food conversion (ecological efficiency) is among the highest known: About 50% of the fresh weight consumed is incorporated into the organism.
The subclass Scombridae includes medium- and large-sized fish, active predators at high trophic levels. These include tuna (Thunnus), bonito (Sarda), Luvarus, mackerel (Scomber), the cutlassfish (Trichiurus), marlins or spearfish (Tetrapterus), and swordfish (Xiphias). All of them are adapted to permanent movement and speed; the sailfish (Istiophorus platypterus) has been timed at more than 68 mi/h (110 km/h). They are the most hydrodynamic of all fish; their fins fold into a special groove, and their eyes form a smooth surface flush with the rest of the head. They cannot stop swimming for two reasons. The first is that they depend on the oxygen transported in the water flowing permanently through their open mouth, as they have lost most of the mechanisms used by other fish to pump water through their gills. The second reason is that if they do not swim, they sink, because they are denser than water, partly because they lack a swim bladder.
This permanent movement requires a considerable expenditure of energy; some species consume up to 25% of their body weight every day. Their intense metabolism generates a large quantity of heat, meaning that they, and tuna in particular, are warm-blooded animals. They possess unique physiological mechanisms to dissipate the excess heat, including an intricate network of fine blood vessels called the rete mirabilis. As efficient predators they have very sensitive hearing, sensitive chemical detectors, and a stereoscopic vision so they can measure distances. They are also very prolific; the females release 100,000 eggs per kilo of body weight; so a 110 lb (50 kg) female produces about 5,000,000 small eggs. Starting from an egg just one millimeter in diameter, the tuna (Thunnus thynnus) increases a thousand million times in weight to reach its adult weight of more than 1,542 lb (700 kg). The black marlin (Makaira ampla) may reach more than 2,863 lb (1,300 kg); it is without doubt the largest bony fish in the seas. They are remarkably migratory; the albacore (Thunnus alalunga) migrates from the coast of California to Japan, about 5,282 mi (8,500 km), and even greater distances have been recorded for other species of the same group.
Other large fish include the dolphinfish or "mahi-mahi" (Coryphaena) and the sea cock (Nematistius), well-known but comparatively scarce. One particularly important group in the pelagic environment, especially in the open ocean, is the sharks; without a doubt they are among the most important predators of the entire ocean.
4.3 Allochthonous pelagic consumers
Fish and crustaceans are truly marine animals. Marine food chains also include typically continental animals, such as carnivorous birds, reptiles, and mammals specialized in exploiting fish stocks. These groups show a wide range of strategies--ranging from coastal fishing (seagulls) to capturing prey on the high seas (petrels), and from life on the land with incursions into the sea (sea otters) to permanent adaptation to marine conditions (cetaceans).
Marine turtles belong to two different families: the Dermochelidae (leatherbacks), with one genus (Dermochelys), and the Cheloniidae, with four genera (Chelonia, Caretta, Lepidochelys, Eretmochelys). The leatherback turtle (Dermochelys coriacea), one of the largest reptiles in existence, belongs to the Dermochelidae. The adults are easily recognized by their coriaceous (leathery), scaleless carapaces (shells). This species has the widest distribution of the marine turtles and lives in colder water than the others. In autumn and winter they move in very large groups. The main beaches where they nest are on the western coast of Mexico (80,000 nests a year), in Guyana (10,000-15,000), in Costa Rica (5,000), and in Trinidad and Tobago (1,000). The coasts of Malaysia also used to be important, but the number of nesting areas has now fallen greatly. On other tropical coasts the number of nests is much lower. The other family, the Cheloniidae, includes important species, like the loggerhead turtle (Caretta caretta), green turtle (Chelonia mydas), Pacific ridley (Lepidochelys olivacea), Kemp's ridley (L. kempi), flatback turtle (Chelonia depressa), and the famous hawksbill turtle (Eretmochelys imbricata), which used to be exploited for its carapace. It is the most tropical of the marine turtles and is distributed in the coastal Atlantic and the Indo-Pacific, and breeds in the spring and summer.
Marine mammals include the largest consumers found on the entire planet, not just the oceans, and the largest organisms known to have existed. The large majority of marine mammals are found in the circumpolar regions, or the temperate areas of high productivity caused by upwelling or the mixing of waters. In any case, it is obvious that these organisms have developed in a special way in those areas where there is a wealth of food available. One group of mammals, the pinnipeds (walruses and sealions), uses the pelagic environment in the same way as birds; they eat there, but escape its more dangerous aspects by reproducing on land.
Not all marine mammals eat mainly pelagic organisms. On the contrary, many of them preferentially consume species from the seafloor. This is the case in some seals (for example Erignathus), walruses (Odobenus), some dolphins, the narwhal (Monodon), and even a whale, the grey whale (Eschrichtius). In general terms, because of the large area of continental platform in this region, many of the marine mammals in the Arctic eat organisms from the ocean bottom. In the Antarctic, most species depend almost entirely on the pelagic environment for their food supply, as there is almost no shallow seafloor. (see volume 9).
Dolphins are active consumers of pelagic organisms, especially small fish and squid. There are many species of dolphin distributed throughout almost all the oceans, although they are considerably more abundant in zones of high productivity. The largest organisms of all, the whales (of the family Balaenidae), have shortened the food chain by eating basically zooplankton and, in some cases, small pelagic organisms.
The Antarctic Ocean and the Arctic Sea are their most important feeding areas during the summer. The Antarctic, to be precise, has four times more whales than the entire northern hemisphere. Its main attraction is the enormous abundance of zooplankton and micronekton, which grows extraordinarily quickly and forms enormous, dense patches.
The whales that feed in the pelagic environment have two methods of feeding. The first is characteristic of the whales with flippers (family Balaenopteridae), and consists of gulping a huge quantity of water (up to 78.5 cubic yards [60 cubic meters]), and filtering it through the baleen plates that retain the zooplankton. The other is characteristic of the right and bowhead whales (family Balaenidae), and consists of swimming close to the surface with their mouths open and baleens closed, like a net. Both methods require abundant prey to compensate for their energetic cost and to leave enough surplus for normal metabolic expenditure and for growth and blubber accumulation.
Seabirds are very important predators of the pelagic environment. In some places, guano deposited by seabirds on coastal islands has been used as a fertilizer and used to be collected in large quantities, especially near upwellings like the Humboldt Current and the Benguela Current.
Many species of bird--such as gulls, cormorants, pelicans and penguins--feed basically in the pelagic environment. Although many eat benthic organisms such as crabs and mollusks, in terms of food volume there is no doubt that small pelagic animals are their main food source. In fact, one major effect of the "El Nino" (heating of the Pacific of equatorial origin) is the widespread mortality of marine birds, as the schools of Peruvian anchoveta, their main prey, move to lower depths than normal and are not accessible to the birds.
The degree of adaptation to the pelagic environment is reflected in the feeding methods of each group of birds. The range of variation is very wide. There are species that belong to clearly terrestrial taxonomic groups, for example, the osprey (Pandion haliaetus), is a bird of prey that obtains its prey flying low over the surface of the water. There are other species, such as frigatebirds (Fregata), fully identified with marine environments, which do not submerge or swim and obtain their prey by seizing it from other birds that capture it directly. Gulls (Larus) and pelicans (Pelicanus) obtain their food while swimming on the surface or penetrating a short distance into the water; only those species that usually swim close to the surface are within their reach. Gulls not only consume fish but also considerable quantities of benthic organisms. Cormorants (Phalacroco-rax) and gannets (Sula) show greater adaptation and can dive to great depths to hunt their prey. Even so, there is no doubt that pelicans (Pelecanus) show the greatest adaptation to marine diving.
The world distribution of guano deposits shows that upwellings support the largest biomass of birds that eat fish and nest on land. However, it is in the Antarctic, where there are many penguins, that seabirds' participation in the trophic chains of the pelagic environment is most obvious (and this is why they are treated in volume 9).
The biomass of the seven species of penguins that live in the Antarctic has been calculated to be about 500,000 tons, while the other seabirds are only about 50,000 tons. The penguins' consumption of small fish, krill, and squid has been calculated to be about 30 million tons a year, more than a third of the total world fisheries' catch.
23 The marine environment is the largest of all the Earth's environments. Although it cannot be inhabited by people, its food resources have been known and used since antiquity. This Roman mosaic at the National Archeological Museum in Naples, Italy, clearly shows the range of seafood on Roman tables 2,000 years ago.
[Photo: Museo Archeologico Nazionale di Napoli / Scala]
24 The relationship be-tween the size and speed of planktonic organisms, depending on the viscosity of the water. The speed attained, multiplied by a linear dimension characteristic of each species, and divided by the index of viscosity of the water, is equivalent to the Reynolds number, a parameter that allows comparison of different hydrodynamic behavior by individuals depending on the water regime (laminar, turbulent, etc.). The triangles correspond to specific cases.
[Drawing: Jordi Corbera, bas-ed on Margalef, 1982]
25 Plankton nets have been essential for obtaining samples since the first studies of marine plankton. The pictures shows two being cast from an oceanographic vessel.
[Photo: Joan Biosca]
26 The Sargasso Sea lies at the center of the Atlantic Ocean between the Azores and the Bahamas, and is surrounded by currents isolating it from the rest of the ocean. It is one of the world's bluest and most transparent seas, the result of its low nutrient levels. Virtually the only external nutrients it receives come from the eddies that split off from the meanders of the Gulf Stream. The false-color satellite images use a color scale from red to violet to indicate decreasing presence of chlorophyll and nutrients. The dark patches to the east are areas where the satellite sensor did not capture images, due to clouds or other reasons.
[Photos: courtesy of the Global Change Data Center, NASA Goddard Space Flight Center]
27 Sargasso (Sargassum) floating in the Bermuda Sea. Unlike other phaeophytes and most macroalgae, sargasso does not live anchored on a substrate but instead floats freely on the high sea. Its many air bladders give it the buoyancy that makes this ecological strategy possible.
[Photo: Peter Parks / Oxford Scientific Films / Firo Foto]
28 Secchi's disc, perhaps the simplest and most classic of all the devices used in oceanography. It was introduced in the middle of the 19th century by the Jesuit astronomer Angelo Secchi (1818-1878), director of the Pontifical Observatory. It is used to measure the transparency of the water and consists of a weighted white disk 12 in (30 cm) in diameter hung horizontally at the end of a rope. At the depth where the Secchi disc can no longer be seen, the photosynthetically active radiation is about 18% of that found at the surface, and at a depth 2.7 times greater, this has decreased to, at most, 1%. The consistent sensitivity of the human eye is surprising, as estimations by different observers of the disappearance of Secchi disks in the same water coincide nearly exactly. This is almost independent of the diameter of the disk, as long as the disk occupies a large enough angle of vision at depths close to disappearance.
[Photo: Jordi Camp]
29 A bloom of the cyano-bacteria Trichodesmium erythraeum off Ribloon Reef, on the Great Barrier Reef, Australia. This is the only genus of cyanobacteria that forms blooms like this, which are much more common in other groups of phytoplankton.
[Photo: D. Parer & E. Parer-Cook / Auscape International]
30 Dinophytes, like other marine protoctists, have always fascinated microscopists. Since the first drawing by the Danish microscopist Otto F. Muller, many scientist have become artists in their attempts to represent their many forms and varied behavior. These drawings dating from 1915-1917 are the work of the American zoologists Charles A. Kofoid and Olive Swezy, and the artist Anna L. Hamilton. These two plates are from their large monograph The free-living unarmored Dinoflagellata. The dinophytes represented are: Cochlodinium miniatum (107), C. volutum (108), Gyrodinium herbaceum (109), Gymnodinium submarinum (110), Amphidinium dentatum (111), Gyrodinium virgatum (112), Cochlodinium scintillans (113), Pavillardia tentaculifera (114), Cochlodinium convolutum (115), Gyrodinium rubricaudatum (116), G. corallinum (117), Erythropsis hispida (127), E. scarlatina (128), E. cornuta (129), E. extrudens (130), E. minor (131), E. labrum (132), E. pavillardii (133) and E. richardii (134). Note the range of colors and forms shown by the chromatophores (mostly pigments with no photosynthetic role), the light-sensitive eyes of the genus Erythropsis, and the extensible tentacles of the species of this genus and of Pavallardia tentaculifera.
[Photo: Jordi Vidal]
31 Not all dinophytes are photosynthetic organisms contributing to the primary productions of the water they live in. Many freshwater and marine species show heterotrophic lifestyles, which are more complex and varied in the sea environment. Some, such as Protoperidinium conicum, can extend and withdraw a veil-like pseudopodium (pallium) that envelops other cells, usually diatoms, which then undergo extracellular digestion. Others, such as Paulsenella chaetoceratis issue pseudopodia that penetrate and suck the cytoplasm of their prey, digesting it intracellularly (mizocytosis). Although it is a freshwater species, Gymnodinium aeruginosum does the same, but it uses its pseudopia to acquire its prey's chloroplasts which its keeps alive and functional, while digesting the rest of the prey's cytoplasm. The case of Peridinium balticum is quite different, as it houses a small intracellular symbiont that provides the food it could not otherwise synthesize. There are also dinophytes that limit themselves to phagocytosis of other organisms, and some that are intracellular parasites and eat the cytoplasm surrounding them.
[Drawing: Jordi Corbera, from several sources]
32 Dinophytes are among the most common organisms in the phytoplankton. Ceratium is one of the most diversified genera, with both freshwater and marine species. The image to the left shows Ceratium ranipes, one of the most spectacular warm-water species, because of its two branched appendages. Noctilucas (Noctiluca), on the right, are larger than dinophytes, reaching 0.08 in (2 mm) in diameter, and their size and bioluminescence make them visible to the naked eye.
[Photo: Claude Carre]
33 Drawings of some cryptophytes. They are all small, especially Plagioselmis prolonga, and vary greatly in color because of the range of pigments they may possess. The pairs of drawings represent the same cell from different angles.
[Drawing: Jordi Corbera, from data by Hill]
34 Chrysochromulina is a genus of prymnesiophyte known as "killer algae," although it is not known how they cause the fish mortality they are blamed for. In May and June 1988 a sudden bloom of C. polypepis affected a large area of the Denmark Strait and the Oresund and the southern coast of Norway, causing great alarm and some fish mortality. This was due to obstruction of the fish's gills and local oxygen depletion in some bays by the decomposition of masses of beached algae and mucilage, rather than by any identifiable toxin. The drawing on the left shows a different species of Chrysochromulina that is slightly larger than C. polylepis, a species that occasionally produces similar patches in the Mediter-ranean.
[Drawing: Ramon Margalef and Editronica]
35 The unusual appearance of many diatom frustules, with their regularly-arranged clefts and pores, has made them a favorite for research by microscopists. Many people have made collections of preparations of diatom frustules, and they have been used as tests of the quality of optical microscopes, or as a sort of microscopic yardstick. The images show the complete frustule of a species of Thalassiosira in connective view (top), an external valve view of T. eccentrica (middle), and an internal valve view of an organism of the genus Asteromphalus (bottom).
[Photo: Maximino Delgado and Jose Manuel Fortuno]
36 Some diatoms live in association with ciliates. This allows them to remain in suspension without settling and also guarantees regular renewal of the surrounding water, thus increasing their assimilation. It is not clear what benefit the ciliate obtains from the association, but it may obtain a more regular supply of bacteria--those growing on the diatom or its appendages. Alternatively, the size and shape of the association may prevent the ciliate from being eaten by zooplankton predators. The photo shows an example of the association between Tintinnus inquilinus and the diatom Chaetoceros tetrastichon.
[Photo: Claude Carre]
37 Some silicoflagellates can only live within a limited temperature range. There is a close correspondence between water temperature and the distribution of the two major groups of silicoflagellates (those with four sides, included in the genus Dictyocha, and the six-sided ones, in the genus Diste-phanus). Distephanus types are generally found in waters below 59[degrees]F (15[degrees]C), while those of Dictyocha cannot live below 50[degrees]F (10[degrees]C). The transition between the two forms may be sudden, as in the Sea of Japan, or they may coexist in areas with water temperatures within their respective limits, as happens in the south-western Atlantic.
[Drawing: Jordi Corbera, bas-ed on data from Lipps]
38 Biogeographic types of phytoplankton and their areas of distribution. The geographical distribution of phytoplankton species is still not well enough known to make generalizations other than a provisional simplification that allows a convenient ordering of the available data. That given here is based on a division of the oceans into five great domains: cold northern waters, temperate northern waters, warm waters, temperate southern waters, and cold southern waters. These domains allow division into twelve biogeographical areas to include all known species of marine phytoplankton. The approximate percentage of each type is shown.
[Drawing: Editronica, based on data provided by the author]
39 Plankton diversity in the Mediterranean and the Caribbean is among the highest in the world, and is probably only exceeded by some points of the Pacific Ocean. These graphs show two comparisons between plankton samples from the two areas, one in the north-west Mediterranean and the other in the southeast Caribbean (1963 and 1965). The upper graph shows the distribution of the two sets of samples grouped by cell volume. In the Caribbean, smaller cells predominate and there are relatively fewer larger ones. The lower graph arranges phytoplankton species in decreasing order of total numbers of individuals. Only the 200 most abundant species in each set were included. Abundance is expressed on a logarithmic scale (left). The values found are very similar in both cases, with the Mediterranean showing a slight advantage.
[Drawing: Editronica, based on data provided by the author]
40 Factors affecting plankton distribution. The left-hand diagram shows the relationship between fluctuations in environmental conditions and the presence of toxic dinoflagellates (Gymnodinium catenatum and Protogonyaulax affinis) in the Vigo estuary (Spain) in autumn, 1985. The water in a relatively resting state (low index of upwelling) coincides with a high surface temperature and the development of toxic dinoflagellates. The appearance of the coastal upwelling introduces cold water and brings the "sea purge" to an end. The right-hand diagrams shows the relationship among chlorophyll, nutrients, and light. The observations made in the English Channel in July 1976 show the tendency to reach, sooner or later, nutrient depletion where there is a lot of light. The lower diagrams show more detailed sections of the Baltic Sea, where chlorophyll peaks cluster around the maximum temperature gradient.
[Drawing: Jordi Corbera, based on S. Fraga, Derenbach, and Pingree]
41 14C levels in the dissolved organic carbon oxidisable by ultraviolet radiation in samples from the north of the central Pacific (31[degrees]N, 159[degrees]W) and from the Sargasso Sea in the Atlantic (31[degrees]50'N, 63[degrees]30'W). The 14C values are indicative of the age of the dissolved organic carbon, given that the concentration (in parts per thousand) diminishes with depth. As the graph clearly shows, the deeper the samples are taken, the older the organic material is. From this we can conclude that in the deep waters of the Pacific there is more dissolved organic matter than in the Atlantic, which confirms the Atlantic's relative youth. Note that at 3,281 ft (1,000 m) there is a change in the vertical scale.
[Drawing: Editronica, from several sources]
42 Rapid phytoplankton blooms occur for no apparent reason in different points of the ocean, such as this bloom of the cyanobacterial genus Oscillatoria in the Pacific, off the eastern coast of Australia. They are only possible because there is always a reserve of biodiversity in the plankton, including a wide range of organisms in a more or less quiescent state, but ready to make use of improved growing conditions.
[Photo: L. Newman & A. Flowers / Auscape International]
43 The concentration of phosphorus in seawater decisively affects its fertility. Although on a global scale the phosphorus content of the oceans is considerable (an average of 2.3-2.5 micromoles phosphorus per liter), its concentration in surface water is negligible, as almost all that arrives is immediately used by organisms. Only in certain upwelling areas does a little phosphorus from deep waters and nutrient-rich sediments enrich the surface, and even in these areas it is mainly concentrated in deep water. This is shown by superimposing the values for available phosphorus on those for chlorophyll on this section along the parallel 26[degrees]S near Luderitz, Namibia, in the upwelling off southwestern Africa during the southern summer. As in other upwellings, the amount of unconsumed and non-dispersed production determines the accumulation of organic matter and phosphorites in the sediments below, as shown in the maps. The graph, corresponding to samples taken from Septem-ber 19-21, 1985, also shows the areas dominated by different species or genera of diatoms with different behavior with respect to nutrients. Thalassiosira multiplies rapidly (chlorophyll peaks) and is eaten by copepods. At the other extreme, the similar Planktoniella, multiplies more slowly and has a sort of "skirt" making it hard to digest; it is more frequent on the open seas where the intensity of upwelling decreases.
[Drawing: Jordi Corbera, from data provided by the author]
44 Vertical distribution of trypton (seston that is not plankton) in average dry weight, in the oceanic waters off western and northwestern Australia, according to observations by A. Hagmeier (summer 1961), on a logarithmic scale. The suspended material consists of non-living particles, about which there is very little information, as well as live plankton.
[Drawing: Editronica, based on several sources]
45 The marine laboratory at Rosgo (Roscoff) at the beginning of the 20th century. This marine laboratory on the Brittany coast of the English Channel was the first of those created by Henry Lacaze-Duthiers (1821-1901) as coastal extensions to his zoology laboratory at the Sorbonne. Although its founder was most interested in marine invertebrates, since its beginnings the Roscoff laboratory has contributed to many aspects of marine biology, especially the plankton of the Channel and the neighboring Atlantic.
[Photo: Station Biologique de Roscoff]
46 Arctic and Antarctic waters are characterized by spectacular phytoplankton blooms during their summers, as shown by these false color satellite images (warm tones indicate high photosynthetic activity). Phy-toplankton blooms are due to the availability of light, which is limited or absent during the winter. Note the difference between the Arctic and the Antarctic (left and right respectively) as the Arctic is surrounded by land, while the Antarctic is a sea surrounding a continent.
[Photos: courtesy of the Global Change Data Center, NASA Goddard Space Flight Center]
47 Model of the formation of eddies and grids of descending water surrounding small eddies of rising deep water in the northern hemisphere. The force of the wind generates horizontal movements that, when compounded by the Earth's rotation, give rise to alternating eddies in opposite directions. Anticyclonic eddies (clockwise in northern hemisphere and anticlockwise in the south) tend to stratify lighter water at their center and to expand until they fuse laterally with others. Cyclonic eddies (in the opposite directions) suck up deep water in their center, bringing nutrient-rich water to the illuminated surface, and thus show greater fertility, but they tend to become narrower and maintain themselves separated from the grid structure created by the anticyclonic eddies.
[Drawing: Jordi Corbera, using data provided by the author]
48 The strong absorption of light by water is even apparent in transparent water, as shown here in the center of the Pacific, close to the Hawaiian islands. A jellyfish Cephea cephea is moving against a blue background clearly showing the transparency of the nutrient-poor water. This absorption of light is one of the most rigorously conditioning factors of phytoplankton, which progressively loses its source of energy as it settles until it reaches a depth where it is insufficient for photosynthesis.
[Photo: David B. Fleetham / Natural Science Photos]
49 Comparison of production and presence of silicon dioxide on the surface of sediments in the Pacific and Indian Oceans, and a generalized model of the accumulation of sediments on the seafloor. The production of silicon oxides by phytoplankton (mainly by diatoms and to a lesser extent by silicoflagellates and radiolarians, which are more common in tropical waters) is expressed in grams of silicon per square meter per year, while that of amorphous silicon (opal) as a percentage of dry weight of carbonate-free sediment. The maximum values for concentrations of amorphous silicon in sediment are found between the Antarctic convergence and the Antarctic divergence, but slightly displaced from the zones of maximum production. Relative production maxima are found that can be related to areas of upwelling and divergence in these oceans and that are also reflected in the sediments of the equatorial band of the eastern Pacific. In a generalized model of oceanic sedimentation, siliceous muds would tend to accumulate in areas of upwelling of the eastern shores of the ocean and under the equatorial divergences, while in the centers of the hemi-oceans red clays, poor in organic materials, would accumulate, reflecting their scarce productivity.
[Drawing: Editronica, based on data from Lisitzin]
50 The struggle against settling out of the sunlit zone is a priority for phytoplankton organisms. Those that develop the most successful strategies, such as the large extensions that increase the buoyancy of the diatom Chaetoceros, are usually the species responsible for plankton blooms when conditions allow.
[Photo: Claude Carre / Jacana]
51 Representation of the main characteristics of the phytoplankton (plankton "mandalas") using different descriptors. The first uses as descriptors turbulence and presence of nutrients. The upper right box corresponds to the beginning of succession, while the lower left box corresponds to its end. The start typically shows considerable turbulence and persistence of nutrients in the sunlit layers (as well as being dominated by opportunistic species with high rates of reproduction). The end of succession is characterized by low turbulence and nutrient depletion (and is dominated by specialized, persistent species with low rates of reproduction). The bottom right box would correspond to very turbulent spring waters in a Nordic or Antarctic sea, almost without nutrients and organisms (the Gran-Braarud effect). The upper left box shows the situation in bays or other stratified waters near the coasts where the surface water receives additional nutrients, often of continental origin: In these situations swimming dinoflagellates (often toxic) bloom and accumulate, causing "red tides." The same diagram can be rotated by 45[degrees] (clockwise) to change the coordinates that become, respectively, the quotient of nutrients divided by turbulence and the product of nutrients multiplied by turbulence, which now correspond to stratification and productivity, respectively. The axis of succession (and of change in dominant reproductive strategies) now runs from right to left.
[Diagram: Jordi Corbera, using data provided by the author]
52 A colony of polyps, in the form of a planktonic medusa, of Porpita porpita. This is the most common form of the species, and is an asexual phase. This colony consists of a central polyp specialized in feeding (the gastrozooid), above which there is a circular floater. Around the gastrozooid there are polyps specialized in reproduction (gonozooids), and between them at the type of the umbel, are circles of polyps specialized in defense (dactylozooids), arm-ed with many cnidoblasts borne in small spheres that may completely cover the specimen. Their color is due to the presence of symbiotic zooxanthellae that nourish the polyps. The medusa phase is the shortest and smallest phase in the life cycle of this species. It is only 2 mm wide, while the polyp colony can reach a diameter of 10 mm.
[Photo: Peter Parks / Norbert Wu Photography]
53 The biological cycle of many zooplankton species is very complicated. The copepod Acartia clausi from the Atlantic coast of the Americas is an example. The drawing shows the different stages of its life cycle, its length, percentage survival, and the number of individuals that survive each stage out of the total that hatched initially. The complete cycle may last up to 14 days, but the cycle of the population as a whole is longer, as the adult females have a life expectancy of five days. While they are in the plankton, if enough food is available, the females can lay eggs several times. In the species A. tonsa, when food concentration is 100 g of carbon per liter, 46% of its energy goes into growth, 33% into reproduction, and the other 21% is lost by excretion. If food is increased 4-fold, feeding increases 3.5-fold, and the energy invested in reproduction is doubled. But if food is increased 9-fold, assimilation increases only a little, and reproductive effort hardly increases.
[Drawing: Jordi Corbera, from several sources]
54 The dispersal and distribution of many zooplankton organisms are intimately linked to the dynamics of water masses. An example of this phenomenon is the dispersal of the larvae of the anchovy Engraulis capensis in the southeast Atlantic. The adults lay their eggs near Cape Agulhas, where the water column is mixed and not very productive. The eggs hatch within a few days, forming lecithotrophic larvae (ones that feed on their yolk) that are able to feed within a week. After a month, they are 20 mm long, and when they 60-70 mm they are juveniles. The larvae drift to the north in a strong current that bears them more than 149 mi (240 km) to a highly productive upwelling above Cape Colombine, thus ensuring an abundant food supply. The adults return to the region of Cape Agulhas the following southern spring or summer to spawn.
[Drawing: Jordi Corbera, from several sources]
55 Phases in the development of the medusa Pelagia noctiluca, which forms large masses, or swarms. They do this, among other reasons, so that their eggs can form new medusae directly and do not have to pass through a benthic polyp stage like other species. The ciliated, elongated, free-swimming larva (planula larva of P. noctiluca) has a darker end where the mouth forms (upper left). A few days later, the larva flattens and forms the rough fissured rim (upper center and right) that will make it a true medusa. Next, it becomes a new larval form, the ephyra, the first indication that it will form a large swarm, and it is often found in large quantities in samples of plankton (center right). The larvae take three months to complete development to the adult medusa, during which time they remain in the same water mass and so they, too, can form dense populations that may drift to the coast on surface currents.
[Photos: Claude Carre (upper and center) and Sophie de Wilde / Jacana (bottom)]
56 Shrimp larvae are a good example of what plankton organisms have to do to avoid sinking. Many species develop a range of morphological structures, such as body projections and filamentous appendages, which give them a neutral buoyancy and, as a result, they do not have to expend energy to move and avoid sinking in the water column.
[Photo: Peter Parks / Norbert Wu Photography]
57 Planktonic pteropods (sea butterflies), such as this individual of the genus Creseis, may be herbivorous or carnivorous. The shells of herbivorous pteropods are very thin and almost transparent. The herbivores browse on phytoplankton or filter it from a large volume of water, which they draw to their mouth by the constant movement of the cephalo-bucal prolongations that emerge from their shells.
[Photo: Peter Parks / NHPA]
58 Sexual phase of the anthomedusan Neoturris pileata, showing the red gonads adhered to its stomach. Like most other anthomedusans, it has a benthic polyp phase whose life is much shorter than the adult's. The tentacles around the umbrella of this widely distributed species of anthomedusa may reach three times the length of the body, which is about 1 or 2 in (3 or 4 cm). This species is carnivorous, catching small prey such as copepods.
[Photo: Claude Carre]
59 Euchaeta marina is a widely distributed copepod of tropical, subtropical and temperate waters, where it forms dense populations in the top 328 ft (100 m). It can migrate strongly and avoids the surface water during the hours of light. It is also clearly seasonally distributed with peaks of abundance in spring and winter, but it disappears almost completely from the plankton during the summer.
[Photo: Claude Carre]
60 Calanus finmarchicus is one of the largest calanoid copepods, with adults up to 4 mm long. It is very abundant in the North Atlantic, where it forms dense swarms close to the coasts. The life expectancy of an adult female is two and a half months, although the population generated at the beginning of summer lives for seven months, until the onset of winter. The males remain in the plankton for a shorter period than the females. Like other species of zooplankton, C. finmarchicus performs ontogenetically distinct migrations. The females clearly migrate to the surface at night, while the males stay a few meters below it. The nauplius and smaller copepodid larvae do not perform vertical migrations.
[Photo: Robert Arnold / Planet Earth Pictures]
61 Many benthic organisms have a pelagic larval stage, lasting from a few days to several months. The echinoderms, such as Amphiura filiformis, have several larval stages, one of which, the ophiopluteus, is very abundant in the coastal plankton for a few weeks. The different larvae undergo a process of morphological transformation until they reach a stage similar to that of the adult, when recruitment takes place. Larval mortality is very high and up to 95% of each brood is lost.
[Photo: Claude Carre]
62 Chaetognaths are planktonic organisms that are very common at certain periods of the year.They are highly seasonal. The species of the genus Sagitta form dense populations in the meso-and epipelagic waters at varying times of the year, while at other times they may be almost absent. It is not clear if their eggs are present in a latent state, or if there are so few individuals that they are not captured by plankton nets. Chaetognaths are carnivorous animals and frequently, cannibals.
[Photo: Peter Parks / NHPA]
63 Ostracods are among the smallest organisms of the zooplankton. They are especially abundant in mid-latitude surface waters and can be caught in neustonic nets. Although there are many benthic species, the planktonic species are more diverse and show wide horizontal and vertical ranges. They are active filter-feeders that can form dense populations at certain times of the year, when they play an important role in coastal planktonic communities.
[Photo: Claude Carre]
64 Nanomia bijuga is a colony of siphonophores consisting of polyps with differing morphology and functions.
The colony can reach 7 ft (2 m) in length, although the nectophores are at most 3 mm long. The upper part of the colony consists of buoyant nectophores, underneath the pneumatophore responsible for the colony's vertical orientation and buoyancy. The cluster of nectophores responsible for buoyancy produces a long stolon on which the other polyps are located. The most visible polyps are the gastrozooids (responsible for feeding), the gonozooids (reproductive), and the tentacles, which are specialized and highly retractile polyps. The colony captures its prey by extending its long tentacles in a volume of water greater than 5 cubic yards (4 cubic meters), forming a type of very fine net that is invisible to the occasional passing prey that adhere to it.
[Photo: Claude Carre]
65 Interspecific associations are much more common in the zooplankton than might be expected of organisms that live in a dilute environment like a body of water. One example of an association exists between medusae (like the Antarctic species Scarcia princeps, shown in the photo) and hyperiid amphipods. The association generally starts as commensalism, with the amphipod eating part of the medusa's prey, and it may turn into parasitism, because the amphipod eats the medusa if other prey is not available. This type of association often starts with the implantation of eggs in the medusa's mesogloea by an adult female amphipod. When the embryos hatch, their larval development takes place within the medusa, which they feed upon. The senescence of the host means that once they are adults the amphipods have to find another host to settle on and to lay their eggs on.
[Photo: Norbert Wu / Still Photography]
66 The underside (ventral) of pelagic fish is often lighter in color than the upper side (dorsal), as shown by this stingray (Dasyatis americana). This combination, together with the reflections and hues of the water itself, make the fish less visible from above (against the dark ocean depths) and from below (against the light).
[Photo: Norbert Wu / Still Photography]
67 Predation is intense in the pelagic environment, and is practiced by members of most animal groups. The photo shows a sparid fish caught by a coelenterate and about to be ingested.
[Photo: Peter Parks / Norbert Wu Still Photography]
68 The migrations of some species of pelagic fish. In one way or another, most pelagic fish migrate large distances. The term oceanodromous is used for species that migrate within the oceans. Diadromous refers to fish that migrate between fresh and salt waters. The map shows the migration routes of four oceanodromous fish: the herring (Clupea arengus), the cod (Gadus morhua), the tuna (Thunnus thynnus) and the skipjack tuna (Euthynnus pelamis). It also shows two groups of diadromous fish: the eels and the salmons. Both European eels (Anguilla anguilla) and American eels (A. rostrata) are catadromous, reproducing in the sea and feeding and growing in freshwater. Both the Atlantic salmon (Salmo) and the Pacific salmon (Oncorhynchus) are anadromous--feeding and growing in the sea and reproduce in freshwater.
[Drawing: Editronica, from several sources]
69 Annual production cy-cles in different oceanic regions. Annual cycles of primary and secondary production are more seasonal at polar latitudes. At high Arctic or Antarctic latitudes there is a single peak of primary production in the summer, followed by a peak of secondary production, also in the summer but slightly out of phase. At mid-latitudes there are two peaks of primary production (the most important is in the spring, the autumn one is secondary) and one peak in the summer of secondary production by herbivores. At equatorial latitudes there are no seasonal peaks, only slight oscillations within the tendency of primary producers (algae) and herbivores to maintain uniform production throughout the year.
[Drawing: Editronica, based on data from Cushing, 1959]
70 Mass of engraulids (Anchoa) in the Pacific, near the Galapagos Islands. One of the engraulids' most remarkable characteristics is that they live in large schools that move as a single unit, and this makes their exploitation especially attractive to humans. However, their populations may vary greatly in very short periods, and this is favored by their excessive exploitation in some of the places where they are most abundant, such as the coasts of Peru and northern Chile.
[Photo: D. Parer & E. Parer-Cook / Auscape International]
71 Simplified diagram of food webs in the Antarctic Ocean, probably one of the most complex seas, with the longest food chains in the entire pelagic environment. To make it simpler, some details are not included: Some cephalopods eat small fish and are thus tertiary consumers, seals and birds export some of their production from the marine environment, and the great skua (Stercorarius skua) migrates from pole to pole, leaving the southern hemisphere to breed.
[Diagram: Editronica, from various sources]
72 Clupeids, like engrau-lids, form very large schools. Both can eat phytoplankton thanks to their cellulase-producing intestinal bacterial symbionts. This allows clupeids, like this shoal of herrings (Clupea harengus), to grow fast and reach high levels of biomass that are food for larger predators, including humans.
[Photo: Norbert Wu Photography]
73 Carangids (saurels, jacks, trevally, and similar) are middle-sized pelagic fish, although some are almost the same size and show the same gregarious behavior as small phytoplankton-eating fish. Carangids do not eat phytoplankton, but feed on zooplankton and the juvenile forms of other fish or marine organisms. The photo shows a school in the Turks and Caicos Islands, in the Antilles.
[Photo: Yves Lefevre / Bios / Still Pictures]
74 Typical circular school of barracudas (Sphyraena), a large (up to 7 ft [2 m]) predatory fish with ferocious teeth, frequent in all tropical seas. The juveniles in particular form large groups that swim in circles. They do not form groups as large as some smaller fish.
[Photo: Norbert Wu Photo-graphy]
75 Cephalopods are voracious predators and also the favorite prey of some large fish, especially the predatory cetaceans. They vary greatly in size, from squid and cuttlefish a few centimeters long, such as this Indonesian coral shield squid (Sepioteuthis lessoniana), to the 49 ft (15 m) long giant deep sea squid, the favorite food of the sperm whale (see insert, "Whale food," page 98).
[Photo: David B. Fleetham / Natural Science Photos]
76 Bonitos (Sarda) are powerful swimmers that migrate long distances. The scombrids have an unusual physiology and are the only warm-blooded fish.
[Photo: Juan Carlos Calvin]
77 Marine mammals are present throughout the Earth's seas. They have adapted their physiology to the marine environment. The right whale (Eubalena glacialis, above) prefers to live in warm waters and approaches the coast to reproduce; they usually feed by swimming close to the surface with their mouth open, filtering with their baleen plates. Dolphins, such as the pan-tropical species Stenella longirostris (below) are among the most abundant marine mammals, especially in highly productive areas. They eat small- and medium-sized fish and cephalopods.
[Photo: Doug Allen / Oxford Scientific Films / Firo Foto & R. Seitre / Bios / Still Pictures]
78 Migratory routes of some marine birds. Although all marine birds nest on land and many remain within a relatively restricted territory, others migrate over thousands of kilometers, from their nesting sites to their overwintering areas. The Arctic tern (Sterna paradisaea), the shearwaters (Puffinus), and the skuas (Stercorarius) migrate almost from pole to pole. Others, such as Wilson's petrel (Oceanites oceanicus), only migrate from the temperate areas of one hemisphere to those of the other. Other migratory birds, such as the wandering albatross (Diomedea exulans) and the giant petrel (Macronectes giganteus), take advantage of the dominant winds to move across the southern oceans, following the parallels. Gannets (Sula) and brent geese (Branta bernicla) move along the latitudes within a single hemisphere, while the Cape gannet (Sula capensis) never crosses the equator.
[Drawing: Editronica, based on several sources]
79 Cormorants (Phalacro-corax) and other diving birds actively exploit the marine environment, especially up-wellings. They remove some nutrients from the sea, and these accumulate on the cliffs and coastal islands where the birds nest and reproduce, such as this island in the Channel Islands National Park, California.
[Photos: Frans Lanting / Bruce Coleman Limited]
80 Turtles of the world. The adult loggerhead turtle (Caretta caretta) measures between 38 and 45 in (96 and 114 cm) and lives in the tropical zones of all the oceans, feeding on mollusks and crabs. The Pacific green turtle (Chelonia agassizii) lives off the coast of Mexico, Peru and Galapagos Islands; it eats algae and the adults measure 28-36 in (71-91 cm). Not all zoologists separate the green turtles into two species. The flatback turtle (Chelonia depressa) lives off the north of Australia and eats holothurians and other invertebrates, and can reach 35 in (90 cm) in length. The leatherback turtle (Dermo-chelys coriacea) reproduces in the tropics but can also be found in temperate and even subarctic waters; it eats medusae and attains the largest size of any marine reptile, 60-70 in (152-178 cm). The Kemp's ridley (Lepidochelys kempi) is found in the Gulf of Mexico and the north Atlantic; it eats crabs and mollusks and reaches 23-26 in (58-66 cm). The hawksbill turtle (Eretmochelys imbricata), whose carapace (shell) is of great decorative value, lives in tropical oceans close to coral or rocky reefs and measures from 11-14 in (28-36 cm). The green turtle (Chelonia mydas), lives in all the tropical oceans, except the east Pacific; it eats algae and marine plants and measures 35-43 in (90-110 cm). The Pacific Ridley (Lepi-dochelys olivacea) lives in the tropical oceans, mainly the east Pacific, the Indian, and the south Atlantic; it eats crustaceans, fish eggs, and vegetation. It may reach a length of 23-26 in (58-66 cm).
[Drawing: Anna Maria Ferrer]
* The classification used in this work is based on the division of living beings into five kingdoms (see volume 1, p. 75), proposed by Robert H. Whittaker in 1959, according to which most phytoplankton organisms are protoctists, and not members of the plant kingdom (although the term suggests they are plants). The term phytoplankton is still a valid designation for planktonic primary producers in spite of the taxonomic inexactitude implied by its etymological meaning of "plant plankton." The same is true for zooplankton, or "animal plankton," which also includes many protoctists.
** The 1989 Handbook of Protoctists, by L. Margulis, J.O. Corlyss, M. Melkonian, and D.J. Chapman, considers the Dinoflagellata or Dinomastigota as an independent phylum of protoctists.
*** The 1989 Handbook of Protoctists, by L. Margulis, J.O. Corlyss, M. Melkonian, and D.J. Chapman includes the prasinophytes within the chlorophytes, and considers them to be the phylogenetic origin of the chlorophytes.
**** The 1989 Handbook of Protoctists, by L. Margulis, J.O. Corlyss, M. Melkonian, and D.J. Chapman considers the haptophytes or prymnesiophytes, and diatoms or Bacillariophyta as two independent types of protoctists, and includes the silicoflagellates as a class within the Chrysophyta (also considered as a separate phylum), called the Dictyochophyceae.
***** The 1989 Handbook of Protoctists, by L. Margulis, J.O. Corlyss, M. Melkonian, and D.J. Chapman includes the prasinophytes within the chlorophytes, and considers them to be the phylogenetic origin of the chlorophytes.
****** This work considers the Euglenida as a separate phylum of protoctists.
******* This work considers the Raphidophyta as a separate phylum of protoctists, although some authors consider it a class of Chlorophyta.
******** Zooplankton species exist that are carnivorous and thus secondary consumers, but this term is reserved for the larger marine predators (large crustaceans, fish, etc.).
|Printer friendly Cite/link Email Feedback|
|Publication:||Encyclopedia of the Biosphere|
|Date:||Oct 1, 2000|
|Previous Article:||Ghost crabs and fishes in trees.|
|Next Article:||Microscopic jewelery.|