Open Water Lifestyles: Marine Plankton PDF

CHAPTER 4 Open water lifestyles: marine plankton The word ‘plankton’ is derived from a Greek word meaning errant, which itself refers to travelling or wandering. So planktonic organisms are those that live their lives sus- pended in the water column, drifting at the mercy of tides and currents. Ma...

CHAPTER 4 Open water lifestyles: marine plankton The word ‘plankton’ is derived from a Greek word meaning errant, which itself refers to travelling or wandering. So planktonic organisms are those that live their lives sus- pended in the water column, drifting at the mercy of tides and currents. Many can swim but not powerfully enough to go against the flow. Most are microscopic in size though some reach a few centimetres in length. Larger swimming animals, living in open water, such as many fish, are termed nekton and are the subject of the next chapter. The photosynthetic organisms of the plankton are the phytoplankton and the ani- mals the zooplankton, whilst bacteria and other prokaryotes are the bacterioplankton and viruses the virioplankton. Almost all marine phyla have permanent or temporary representatives in the plankton. Early naturalists were enthralled by these tiny animals and plants and wrote some fascinating and now classic accounts of their observations (Fraser, 1962; Hardy, 1956). Specialist photography can now reveal plankton in all its intricate glory and there are both specialist (e.g., Larik and Westheide, 2011; Kraberg et al., 2010) and popular (e.g., Kirby, 2010; Sardet, 2015) books portraying them. This huge subject can be only introduced in this chapter. The phytoplankton is responsible for most of the primary production in the ocean (see Chapter 3). There would be virtually no life in the ocean without the photosynthe- sis carried out by these microscopic plants, plant-like chromists and cyanobacteria. On land the energy-fixing plants dominate the landscape in the form of grasses, shrubs and trees. In contrast the phytoplankton is only visible to us as a cloudiness or discolouration of the water, when reproduction is rapid and a ‘bloom’ occurs. Feeding on the phyto- plankton or on each other are the animals of the zooplankton. The distinction between phytoplankton and zooplankton is not absolute because some planktonic organisms, such as some dinoflagellates, are both autotrophic and heterotrophic, that is, can both manufacture their own food through photosynthesis and ingest or absorb food. Some planktonic organisms can only float passively, unable to swim at all. Others are quite active swimmers, but are so small that swimming does not move them far, compared to the distance they are carried by the water. The swimming movements serve chiefly to keep them afloat, alter their level, obtain food, avoid capture, find a mate or set up water currents for respiration. Although the majority of planktonic organisms are small, mainly of microscopic size, a few are quite large. For example, the tentacles of Portuguese Man-of-War (Physalia) sometimes extend 15 m or more Elements of Marine Ecology r 2022 Elsevier Ltd. DOI: https://doi.org/10.1016/B978-0-08-102826-1.00005-3 All rights reserved. 193 194 Elements of Marine Ecology through the water and there are jellyfish (Scyphomedusae) in which the bell (main body) grows to over 2 m in diameter. Most ‘jellyfish’ are considered to be plankton because they can only swim weakly, but others such as some box jellyfish (Cubozoa) blur the line because they swim strongly. Nonfloating microorganisms such as forami- niferans are sometimes lumped in with plankton, but as they live on and in the seabed, then ecologically speaking, they are not really plankton. 4.1 Ecological definitions Plankton can be divided into different components on the basis of both size and habi- tat. Size categories have been used for many years but are actually of rather limited value on their own. Habitat and ways of life categories have more practical applica- tions. In terms of ways of life, organisms whose entire lifespan is planktonic are termed holoplankton or permanent plankton. In contrast, organisms which spend only part of their lifespan in the plankton, usually the early stages, are termed meroplankton or temporary plankton. For benthic (bottom-living) organisms, particularly sessile species fixed to the seabed, the planktonic larval stages, including spores, eggs or larvae, pro- vide an essential means of dispersal. Holoplankton is perhaps a more reliable source of food for animals than the often seasonal meroplankton, though both are important. Plankton is generally thought of as living in the surface layers (epiplankton or epi- pelagic plankton) and indeed the top 200 m is where the majority is found. However, some plankton is present at all levels and so can also be described as mesopelagic, bathypelagic and abyssopelagic depending on the depth zones (Fig. 1.9) they inhabit. 4.1.1 Surface living plankton As well as plankton living in the water column there are also animals that live at the very surface of the ocean, exposed to rain, wind and wave action. Some of these, such as certain sea snakes, are obviously perfectly able to swim strongly even if they do like to drift and so are counted as part of the nekton. Others have no such abilities and are carried around by wind, waves and currents. These surface organisms are known col- lectively as neuston and pleuston. Technically pleuston are planktonic animals that have some means of floating partially submerged, with part of their body above and part below the surface. This includes hydrozoans such as By-the-wind Sailor (Velella velella), Portuguese Man-of-war (Physalia) and Blue Buttons (Porpita). Some of these attract other holoplanktonic pleuston such as Violet Sea Snails (Janthina). These preda- tory molluscs float by producing a mucous bubble raft and feed on Velella and Physalia. Neuston float on the surface tension and include coastal sea skaters (Halobates) (again nekton rather than plankton) as well as surface scum containing planktonic bac- teria and other microorganisms.  Open water lifestyles: marine plankton 195 4.1.2 Size definitions Size definitions of plankton have changed and evolved since they were first proposed in the 1890s, particularly with the development of finer gauge nets and measurement technology. The most widely accepted system is that of Sieburth et al. (1978). The main size designations are shown in Table 4.1 but for more detail, the full classification and explanations are conveniently accessible in the ICES Zooplankton Methodology Manual (Harris et al., 2000). The smaller size categories, femtoplanton, picoplankton and nanoplankton are sometimes called water bottle plankton because they can only be sampled effectively by using specialised nets or water bottles (Section 4.6.1), rather than conventional plankton nets. 4.2 Marine phytoplankton Marine phytoplankton comprises a wide variety of planktonic organisms that are able to photosynthesize. These include microalgae (Kingdom Plantae) and chromists (Kingdom Chromista) most of which are unicellular and microscopic, as well as cya- nobacteria (Kingdom Bacteria). Some of these organisms can both photosynthesize and feed in a heterotrophic manner, catching prey or absorbing nutrients directly from the water. The predominant phytoplankton varies in different parts of the ocean, with diatoms (Bacillariophyceae) often prevalent in temperate and cold waters at high lati- tudes, both in terms of numbers and species. Diatoms are often more numerous in coastal areas than in oceanic areas and rely on a supply of silica to construct their cell walls. Dinoflagellates (Dinoflagellata) and prymnesiophytes (Prymnesiophyceae) are also important contributors to the phytoplankton. Table 4.1 Size classification of plankton. Size Size range Examples designation Femtoplankton 0.02 0.2 µm Viruses Picoplankton 0.2 2 µm Bacteria, cyanobacteria Nanoplankton 2 20 µm Small flagellates, small diatoms, coccoliths Microplankton 20 200 µm Diatoms, dinoflagellates, rotifers, ciliates Mesoplankton 0.2 20 mm Copepods, chaetognaths, appendicularians, small hydromedusae Macroplankton 2 20 cm Ctenophores, scyphomedusae, siphonophores, salps Megaplankton 20 200 cm Large jellyfish and siphonophores, salp chains Names of categories and sizes follow Sieburth et al. (1978). 196 Elements of Marine Ecology Whilst phytoplankton are mainly responsible for productivity in the ocean, macroalgae (seaweeds), seagrasses and mangroves are important producers in shallow coastal areas. However, some macroalgae are effectively planktonic, living unattached on the water sur- face. The best known is floating Sargassum seaweed (S. natans and S. fluitans) found in the Sargasso Sea region of the North Atlantic and in the Gulf of Mexico. Within very shel- tered sea lochs on the Scottish coast, in areas where the salinity is reduced, there occurs a floating and proliferating form of the common littoral fucoid seaweed, Ascophyllum nodo- sum (A. nodosum ecad mackayi). However, this and other similar seaweeds around the world are not generally regarded as phytoplankton because they derive from the fragmen- tation of benthic plants growing on the sea bottom in shallow water. 4.2.1 Diatoms The majority of diatoms are unicellular, uninucleate plants with a size range of about 15 to 400 µm in maximum dimension, although some smaller and a few considerably larger forms exist. They are currently classified in the kingdom Chromista and the phylum Ochrophyta. The largest known diatom is a tropical species, Ethmodiscus rex, up to 2 mm in diameter. The diatom cell, known as a frustule, has a cell wall of unusual com- position and structure. It is impregnated with siliceous material giving a glassy quality and consists of two parts, the valves. At its simplest, for example, in Coscinodiscus, the cell wall is like a transparent pillbox (Fig. 4.1), the larger valve or epitheca overlapping the smaller hypotheca much as the lid of a pillbox overlaps the base. The valves are often very elaborately ornamented with an intricate sculpturing of min- ute depressions, perforations or tiny raised points which are sometimes arranged in a great variety of beautiful symmetrical patterns. In some, such as Chaetoceros and Biddulphia, the cell wall has larger projections forming spines, bristles and knobs. Ornamentation increases the surface area and also strengthens the cell wall, which in the majority of planktonic dia- toms is very thin. In some species, growth occurs by elongation of the valves at their mar- gins forming a number of intercalary bands, for example, Guinardia. Internal thickenings of these bands may form septa which partially divide the interior of the frustule. The cytoplasm usually lines the cell wall and contains numerous small, brown chromatophores. There is a large central vacuole containing a cell sap. The nucleus with an enclosing film of cytoplasm is often suspended within the vacuole, supported by cytoplasmic threads extending from the peripheral layer. In planktonic diatoms the cell sap is probably lighter than seawater and may confer some buoyancy to support the heavier protoplasm and cell wall. In many diatoms the cytoplasm is not confined to the interior of the frustule, but exudes through small perforations to cover the sur- face or form long thin threads, and these may join the cells together in chains. Planktonic diatoms come in a considerable variety of shape, each in its way well adapted to provide a large surface/volume ratio which improves their photosynthetic  Open water lifestyles: marine plankton 197 nucles epitheca ‘lid’ of the frustule cytoplasmic strands chromatophore lipid vacuoles hypotheca ‘box’ of the frusule Figure 4.1 Diagram of a hypothetical pillbox-shaped diatom. From Dipper, F.A., 2016. The Marine World: A Natural History of Ocean Life. Princeton University Press (Wild Nature Press), 544pp. Courtesy Marc Dando and Wild Nature Press. efficiency. However, most can be described as either centric, meaning radially sym- metrical, or pennate, meaning elongate and bilaterally symmetrical. The latter are much more common than the former. Not all can be recognized as easily falling into one or the other of these categories, but looking at general shape, diatoms can be grouped into four broad categories as follows and examples of these are illustrated in Fig. 4.2: 1. Pillbox shapes (centric)—Usually circular and radially symmetrical when seen in top or bottom view, for example, Coscinodiscus, Hyalodiscus. Sometimes they are connected by protoplasmic strands to form chains, for example, Thalassiosira. 2. Rod or needle shapes (raphide)—The division between the two valves is at right angles to the long axis of the cell in some species, for example, Rhizosolenia and these are often joined end to end to form straight chains. In others the division runs lengthways, for example, Thalassiothrix, Asterionella and these may be joined to form star-like clusters or irregular zig-zag strands. 3. Filamentous shapes—Cells joined end to end by the valve surfaces to form stiff, cylindrical chains such as in Guinardia or flexible ribbons as in Fragilaria. 4. Branched shapes—Cells bearing various large spines or other projections and some- times united into chains by contact between spines, for example, Chaetoceros, or by sticky secretions, for example, Biddulphia. Figure 4.2 Some common diatom genera. (A) Skeletonema; (B) Coscinodiscus; (C) Chaetoceros; (D) Rhizolenia; (E) Thalassiothrix; (F) Biddulphia. From Shutterstock: Rattiya Thongdumhyu (A), (E), and (F); Elif Bayraktar (B); Apichan Thongkrajang (C) and (D).  Open water lifestyles: marine plankton 199 In addition to the planktonic forms there are numerous benthic species of diatom occurring on the shore or in shallow water. These often grow on the surface of sedi- ments, particularly in sheltered areas such as sea lochs. Here they form a clearly visible, thin brown layer. On rocks and stones, they may form a slimy covering. Some project above the surface of the substratum on short stalks. Diatoms are also commonly found attached to the surface of other plants or animals. Benthic diatoms usually have appre- ciably thicker and heavier cell walls than the planktonic species. Certain benthic spe- cies living on and in sediments have some powers of motility and can glide along in a characteristic fashion that is limited by their rigid cell wall. Movement in response to light is important both for placing the diatom in the best position for photosynthesis, but also to help minimise predation and maximise nutrient uptake (Kohn, 2001). The usual method of reproduction in diatoms is by simple asexual division, each individual splitting into two. Under favourable conditions (warmth, light and nutri- ents) this may occur three or four times a day, so that rapid increase in numbers is pos- sible. If one individual divided three times a day for 10 days that would be over a billion individuals (though of course not all would survive that long). The protoplast enlarges and the nucleus and cytoplasm divide. The two valves become gradually sepa- rated, the daughter cells each retaining one valve of the parent cell. The retained valve becomes the epitheca of each daughter cell and a new hypotheca is secreted, the mar- gin of which fits inside the old valve. The new cell formed within the parent epitheca is therefore the same size as the parent cell, but the cell formed inside the original hypotheca is smaller. Because of this, it is a peculiarity of diatoms that the average size of the individuals in a population tends to decrease as division continues (Fig. 4.3). This process of size reduction does not go on indefinitely. Eventually the valves of the smaller individuals separate, the protoplasm flows out and the valves are shed. The naked protoplasm, enlarges and grows new, larger valves. In some species when the offspring reach about a third of the original size, then sexual reproduction can occur if environmental conditions are right. The diatoms then divide by meiosis (rather than asexual mitosis) to produce haploid gametes, discarding the hard frustule along the way. Gametes are motile sperm and large eggs in ‘centric’ diatoms and the eggs are fertilised in the normal way. In ‘pennate’ diatoms the gametes are all similar and amoeba-like and two fuse together. Resulting zygotes grow and produce a new full-size frustule. In some diatoms, zygotes can delay growth and instead form resistant spores (aux- ospores) to carry them through unfavourable periods, for example, during the winter months in neritic water when the temperature falls and salinity may fluctuate appreci- ably. Probably many resistant spores sink to the bottom and are lost, but in shallow water some may be brought to the surface again later by wave action, currents and turbulence and then germinate. In high latitudes, diatom spores become enclosed in sea ice during the winter months and germinate the following year when the ice 200 Elements of Marine Ecology Figure 4.3 Diagram showing the reduction in size of diatoms following asexual cell division. This is relatively easy to visualize in centric diatoms but more difficult with other shapes. melts. There are other more complex variations on gamete and auxospore formation in some diatom groups. When planktonic diatoms die, fragments of their valves sink down to the sea bed. In some areas, notably beneath the Southern Ocean and the northern part of the North Pacific, this accumulation of diatomaceous material gives rise to a siliceous ooze (see Section 1.3.2). 4.2.2 Dinoflagellates Dinoflagellates are unicellular organisms with a size range similar to diatoms, but with a larger proportion of very small forms that escape through the mesh of fine plankton nets (nanoplankton). They are mainly marine occurring in both oceanic and neritic water and are currently (2020) classified in the Kingdom Chromista, the Phylum Myxozoa and the Infraphylum Dinoflagellata. They come in a wide range of ornate shapes but have a similar basic design. Each is equipped with two flagella and the arrangement of these is characteristic of the group. Typically the cell is divided into anterior and posterior parts by a superficial encircling groove termed the girdle or cingulum, in which lies a transverse flagellum wrapped around the cell (Fig. 4.4). Immediately behind the origin of the transverse flagellum, a whip-like longitudinal flagellum arises in a groove known as the sulcus and projects behind the cell. The longitudinal flagellum performs vigorous flicking  Open water lifestyles: marine plankton 201 Pellicle epicone transverse flagellum girdle hypocone longitudinal flagellum sulcus Figure 4.4 Akashiwo sanguinea (previously Gymnodinium sanguineum), a simple nonthecate dino- flagellate. From Dipper, F.A., 2016. The Marine World: A Natural History of Ocean Life. Princeton University Press (Wild Nature Press), 544pp. Courtesy Marc Dando and Wild Nature Press. movements and the transverse flagellum vibrates gently, the combined effects driving the organism forwards along a spinning, spiral path. There are numerous variations along this basic theme. For example, Amphisolenia has a thin, rod-like shape whilst Polykrikos has several nuclei and a series of girdles and sulci, usually eight, each provided with transverse and longitudinal flagella. A variety of dinoflagellates are illustrated in Fig. 4.5 and dinoflagellates from the British Isles are described in Dodge (1982, 1985). ‘Naked’ or nonthecate dinoflagellates have no tough cell wall and the cytoplasm is covered only by a thin pellicle. Thecate species are covered with a strong wall of interlocking cellulose plates beneath the pellicle. In some species these plates are elabo- rated into spines, wings, or parachute-like extensions, and these are especially complex in some of the warm water forms, perhaps assisting flotation. In terms of habitat and geography, dinoflagellates are most numerous in the warmer parts of the ocean, where they sometimes outnumber diatoms, but are also found in cold areas. Around the coasts of the British Isles they are scarce in the winter months and reach their greatest abundance in the midsummer period, when the low concentration of nutrients seems to have less effect in limiting their growth than it 202 Elements of Marine Ecology Ceratium horridum Ceratium fusus Protoperidinium depressum Dinophysis acuminata Polyknkos kofoidii Noctiluca scintillans Figure 4.5 A variety of dinoflagellates from the NE Atlantic. From Dipper, F.A., 2016. The Marine World: A Natural History of Ocean Life. Princeton University Press (Wild Nature Press), 544 pp. Courtesy Marc Dando and Wild Nature Press. does on diatoms. Although mainly marine, dinoflagellates also occur in fresh and brackish water and are sometimes abundant in estuaries. Some are found in sand in the interstitial water between the particles. There are also many parasitic dinoflagellates infecting a variety of planktonic organisms, including radiolarians, copepods, ptero- pods, larvaceans and fish eggs. Reproduction is by asexual fission but is not as rapid as in diatoms. In thecate dinoflagellates the process is somewhat similar to fission in diatoms, each daughter cell retaining part of the old cell wall and secreting the other part, but the old and new cell plates do not overlap and there is consequently no size reduction as occurs in dia- toms. The daughter cells do not always separate completely and repeated divisions then form a chain. Resistant spores may be produced during adverse periods. Dinoflagellates as a group are important primary producers as many of them can photosynthesise. Thecate dinoflagellates in particular rely on photosynthesis as they are  Open water lifestyles: marine plankton 203 constrained by their tough cell wall and so cannot capture prey in the manner of some nonthecate species. Many of the latter are heterotrophic, feeding in an animal-like way using a variety of cytoplasmic extensions to capture their prey, including other dinoflagellates, diatoms, microflagellates and bacteria. Protoperidinium species, for exam- ple, engulf and digest their prey by surrounding it with a cytoplasmic sheet called the pallium. Noctiluca (see Fig. 4.5) is large enough to devour copepod larvae as well as much smaller diatoms and other plankton. Some heterotrophic species can also photo- synthesise, bridging the gap between primary producers and consumers. Colourless thecate dinoflagellates can neither photosynthesise nor capture prey and are presum- ably saprophytes, feeding off decaying material. Dinoflagellates are responsible for some amazing light shows including the spar- kling, phosphorescent wakes sometimes left by boats or people in the water on a warm, still night. Noctiluca is an example which sometimes occurs in swarms around the British Isles and produces myriads of tiny flashes of light when stimulated by agita- tion of the water. This can be seen to dramatic effect when scuba diving. Various spe- cies of Peridinium flash spontaneously in undisturbed water. Highly pigmented photosynthetic dinoflagellates can be so numerous under certain conditions, that they colour the water with green, red or yellow tints and are one of the prime causes of so-called ‘red tides’ (Section 4.2.6). 4.2.3 Prymnesiophytes (Coccolithophorids) The prymnesiophytes or coccolithophores as they are commonly known, (Fig. 4.6) are tiny, unicellular organisms that fall into the nanoplankton size range, mostly some 5 20 µm in diameter. They are currently (2020) classified in the kingdom Chromista and the phylum Haptophyta. In spite of their minute size, they form an extremely important component of the phytoplankton and can occur in incredible numbers. Most are approximately spherical and are characterized by tiny calcareous plates which cover their outer surface. The plates, known as coccoliths, are usually extremely finely and elaborately sculptured. At their simplest, they are oval discs, but in some species, the plates form long projections from the surface of the cell, often of bizarre design. Inside each individual are two (or sometimes only one) plastids which contain the photosynthetic pigments. However, as is so often the case with chromists, some nutrition can also be gained by ingestion, in this case tiny organic particles. A unique flagellum-like structure called a haptonema extends out from the cell wall in most (but not all) species and is thought to be the means by which food is gathered. They have complex life histories usually involving several morphologically different phases. Normal diploid individuals divide asexually, but there can also be a motile haploid phase with lighter uncalcified coccoliths and a pair of flagella for swimming. Haploid individuals act essentially like gametes. 204 Elements of Marine Ecology Figure 4.6 A scanning electron micrograph of Emiliania huxleyi, a well-studied prymnesiophyte. Alison R. Taylor (University of North Carolina Wilmington Microscopy Facility. Creative Commons Attribution 2.5 Generic license https://creativecommons.org/licenses/by/2.5/deed.en). From https://en. wikipedia.org/wiki/Emiliania_huxleyi#/media/File:Emiliania_huxleyi_coccolithophore_(PLoS).png. BOX 4.1 Nanoplankton. In spite of their small size, prymnesiophytes and other nanoplankton (,20 µm in diameter) are an extremely important part of the phytoplankton. The quantity of living material in the water in this form sometimes exceeds that present as diatoms and dinoflagellates (though the smallest of the two latter can also be considered nanoplankton). The nanoplankton is now thought to make a major contribution to primary production and is especially important as the chief food for many heterotrophic plankton species and zooplankton larvae. Modern analytical techniques have demonstrated that the shallow waters (epipelagic zones) of many temperate and tropical seas are dominated by nanoplankton, both in terms of numbers of individuals and amount of photosynthesis. In the tropics, nanoplankton may account for more than 80% of photosynthetic activity in open ocean waters. In coastal (neritic) waters, nanoplankton play a less important role. Prymnesiophytes are widely distributed and can sometimes be so numerous near the surface that they turn it a milky white colour (Box 4.1). Such blooms can be visi- ble from aircraft and even from space. When they die, the calcareous coccolith plates sink down through the water column and are a conspicuous component of the deep- sea sediment in some areas (see Section 1.3.2). They are also the main component of the chalk that makes up many coastal cliffs, including the famous ‘White Cliffs of Dover’ along the south coast of England.  Open water lifestyles: marine plankton 205 Prymnesiophytes have occasionally been found in surprisingly large quantities far below the photosynthetic zone, sometimes very numerous between 200 and 400 m and even in considerable abundance at depths of 1000 4000 m. These deepwater populations must rely on heterotrophic feeding and probably absorption of dissolved organic matter (Section 7.3.5). In some areas they may be an important source of food for some of the animals at deep levels. Phaeocystis (Fig. 4.7) is an unusual and well-known prymnesiophyte which has a normal free-living motile phase and a clumped, colonial phase. In the latter, dividing individuals remain held together by a thick polysaccharide mucilage coating, the whole colony surrounded by a protective membrane. These gelatinous clumps can reach at least a centimetre in diameter. In good conditions massive blooms can form, to the extent of giving the water a slimy consistency. Phaeocystis is abundant in north temperate inshore waters in spring and summer and fishermen call such blooms ‘weedy water’. Unsurprisingly fish such as herring seem to avoid this water, which can clog up their gills and catches can be poor when Phaeocystis occurs in quantity on the fishing grounds. A Phaeocystis patch over 100 miles in extent was recorded from the North Sea in 1927. The slime can also clog up aquaculture and fishing nets. Following a summer bloom, the gelatinous material breaks down in the water and when waves stir the water up, a foam is produced that can cover shores in thick swathes. This often leads people to think there has been a pollution incident. In a way there has, because Phaeocystis produces DMSP, a precursor of DMS which is released into the atmosphere. The structure and ecology of this foam-producing organism are described in Hamm (2000) and a review of the taxonomy (and much background information) in Medlin and Zingone (2007). Figure 4.7 (A) Cropped light microscope photograph of the colonial phase of Phaeocystis globosa in a culture; (B) Sea foam can form when Phaeocystis blooms die off and the resulting dissolved organic matter (DOM) is whipped up by waves. (A) Maggibrisbin on Wikimedia https://creativecom- mons.org/licenses/by-sa/4.0/deed.en. (B) Courtesy Professor David John. 206 Elements of Marine Ecology 4.2.4 True plant plankton Many species of microalgae belonging to the true plants (kingdom Plantae) are repre- sented in the phytoplankton. These are green algae in the phylum (or division) Chlorophyta, which also contains the green macroalgae (green seaweeds) and are abundant in freshwater as well as in the ocean. Most are unicellular, motile flagellates or at least have a motile phase. There are also many colonial species. Their morphology is very varied and their classification is complex and in need of constant revision. Halosphaera (Fig. 4.8) is one of the largest and belongs to the class Pyramimonadophyceae. It consists of a single spherical cell with a tough elastic wall and sometimes reaches nearly 1 mm in diameter. There is a large central vacuole in which a single nucleus is usually suspended, but fully grown cells may contain as many as eight nuclei. In the peripheral cytoplasm are numerous small, yellowish-green chromatophores giving the cell a vivid colour. Asexual reproduction involving repeated division of the nucleus and cytoplasm leads to the libera- tion of numerous four-flagellate spores called swarmers. These can also divide but ulti- mately lose their flagella and develop into a large, nonmotile individual. Sexual reproduction has not been recorded. Halosphaera is found throughout the North Atlantic but is commonest in tropical areas. It is sometimes carried into British waters in great numbers by the North Atlantic Drift and is often abundant in the northern North Sea in autumn. (A) (B) swarmers chloroplasts Figure 4.8 Halosphaera minor (A) mature phase; (B) motile, flagellated phase. From Dipper, F.A., 2016. The Marine World: A Natural History of Ocean Life. Princeton University Press (Wild Nature Press), 544 pp. Courtesy Marc Dando and Wild Nature Press.  Open water lifestyles: marine plankton 207 4.2.5 Bacterial plankton (ultraplankton) Although the number of bacteria in seawater varies greatly with time and place, in coastal waters they sometimes contribute a significant part to the total biomass of the plankton. Bacterioplankton are often associated with floating organic debris known as ‘marine snow’ (Section 7.3.4). Bacteria and other microorganisms play a very important role in marine eco- systems, functioning as decomposers, saprophytes and pathogens, regenerating nutrients, pro- ducing dissolved gases and exocrine compounds, some of which may be essential for the normal growth of other organisms. They are a major source of food for ‘protozoa’ and filter-feeding animals. At hydrothermal vents, (Section 7.4.6) chemosynthetic bacteria and archaea flourish and form the basis of the extraordinary ecosystems found there. Cyanobacteria are photosynthetic bacteria that are generally (though not univer- sally) classified as a phylum within the bacterial kingdom. Many species are free-living and form part of the phytoplankton, where they contribute to primary productivity. They are also found as symbionts within the tissues or various other organisms (see Section 4.2.8) including corals. They are still sometimes referred to as blue-green algae. Cyanobacteria come in a very wide range of forms from small individual rods to long, branching filaments. As well as chlorophyll a, they contain other photosynthetic pigments the phycobilins and together these give them their blue-green colour. However, some also contain phycoerythrins, which impart an orange-red colour. Under certain conditions cyanobacteria form extensive blooms (Box 4.2). With increasing eutrophication of enclosed fresh and brackish water areas, such as estuaries and reservoirs, such blooms are now causing amenity problems. Toxins released by the algae can cause rashes and illness in bathers and other water users. 4.2.6 Plankton blooms and ‘red tides’ Various species of phytoplankton are capable of extremely rapid asexual division and can form extensive blooms particularly prymnesiophytes (Section 4.2.3) and dinoflagellates (Section 4.2.2). This happens particularly when an excess of nutrients is present and the BOX 4.2 Indirect red tides. Under certain weather regimes, dust generated from the deserts of Africa is blown across the Atlantic and into the Gulf of Mexico. The dust is rich in iron and can stimulate the growth and division of some phytoplankton. Cyanobacteria, such as species of Trichodesmium, which fix atmospheric nitrogen, and are normally present in relatively low numbers, proliferate. When they die, the nitrogen is released along with phosphorus and iron and these nutrients in turn stimulate blooms of Karenia brevis. As the bloom dies off, these release large amounts of poisonous brevetoxin. 208 Elements of Marine Ecology sea is very calm. Blooms commonly occur in coastal areas near nutrient-rich discharges such as sewer, industrial and land drainage outlets, but also in areas of natural enrichment. The water is often discoloured hence the name ‘red tide’, though not all ‘red tides’ are red. Such blooms can be beneficial by providing an abundant food source for zooplank- ton. However, some blooms can be extremely detrimental to other marine organisms. Certain species of dinoflagellates contain highly toxic substances which are released as they die or when they are eaten and commonly cause extensive fish kills. Fish farms are often cited in sheltered, enclosed areas such as sea lochs and if a poisonous bloom develops nearby or is swept into the vicinity, many thousands of fish can be killed. Fish are not the only victims and various invertebrates and algae may also suffer. In the USA, common places for red tides to occur are the Gulf of Mexico, in Californian waters and in the Gulf of Maine. In the Gulf of Mexico, tons of dead fish are periodically washed up along the Florida coastline. The fish are killed as they swim through blooms of the dinoflagellate Karenia brevis, rupturing the algae which release neurotoxins onto the gills of the fish (Anderson, 1994). Sea birds, marine mammals and humans can also be poisoned indirectly when they eat filter-feeding shellfish that have accumulated the toxins. The shellfish themselves are not usu- ally affected by the toxins. In the summer of 1968, cases of food poisoning in humans in the United Kingdom were traced to a dinoflagellate infection of mussels on the Northumberland coast, which also caused the death of seabirds, sand eels and flounders. In 1987 a large num- ber of humpback whales died in Cape Cod Bay (United States). It was eventually shown that toxins from a dinoflagellate Alexandrium tamarense had killed the whales via their food web (Anderson, 1994). In the same month many fishermen, visitors and residents along the North Carolina coast, who had eaten local shellfish, became ill with a variety of symptoms. In Canada, people who had eaten mussels from Prince Edward Island also became ill. This was traced to a toxin from a diatom, Pseudonitzschia pungens. Other examples of toxic dinofla- gellates include Alexandrium catenella and Exuviella baltica. Red tides are a global and to a certain extent a natural, phenomenon and can occur, for example, in localized areas of upwelling (Section 4.2.7). However, their extent and frequency appear to be increasing along with warmer surface ocean tem- peratures and increasing nutrient enrichment from land runoff and river drainage. 4.2.7 Upwelling The growth of phytoplankton and subsequently of zooplankton is at least partially con- trolled by the availability of nutrients in the water column. Nutrients in the open ocean can be in short supply, but surface waters in certain areas are enriched by upwelling. In such areas water is pulled up from deeper levels, bringing nutrients with it, which replen- ish supplies and encourage continued phytoplankton growth. Upwelling has several differ- ent mechanisms resulting from various oceanographic processes.  Open water lifestyles: marine plankton 209 Prevailing wind Land Surface layers set in motion by wind Continental Deep layers upwelling to slope replace surface water Figure 4.9 Coastal upwelling resulting from persistent wind action at the surface. Coastal upwelling is generated by offshore winds, which set the surface water in motion and cause water from deeper levels to be drawn up to the surface (Fig. 4.9). Perhaps the best-known occurrence is along the west coast of South America (Peru and Chile), but sig- nificant coastal upwelling also occurs along the west coasts of North America, Africa (Mauritania and Namibia), Arabia and Australia. The upwelling water in these areas is drawn up from about 100 to 200 m, into the coastal currents, including the Canaries Current, Benguela Current, Peru Current, California Current and West Australia Current. In the Southern Ocean, continuous upwelling resulting from violent storms ensures that, even during the highly productive period of the Antarctic summer, phy- toplankton growth is probably never limited by shortage of nutrients. In the Arctic, where upwelling is less, there is some depletion of surface nutrients during the summer months and production is correspondingly reduced. Equatorial upwelling is a much wider phenomenon, occurring in a wide band along the equator through the Pacific, Atlantic and Indian Oceans. This is caused by divergences between the equatorial currents and countercurrents, that is areas where adjacent surface currents move in opposite directions. Equatorial upwelling is impor- tant in maintaining the productivity of tropical waters. Upwelling also occurs at more localized divergences and along the flanks of seamounts, where deep currents are deflected upwards as they encounter these underwater mountains. This is one reason why these areas are so rich in marine life. 4.2.8 Symbiotic ‘phytoplankton’ A number of photosynthetic microorganisms form symbiotic partnerships with various marine invertebrates (Fig. 4.10). These do not really count as phytoplankton since they are not free-living, but are mentioned here because they are of fundamental importance in marine ecology. Perhaps the best known photosymbiotic partnership is 210 Elements of Marine Ecology Figure 4.10 The flatworm Symsagittifera roscoffensis has a photosymbiotic relationship with the microalga Tetraselmis convolutae, with which its body is packed. The worms mass together in shal- low, sunlit intertidal pools, where their contained algae can photosynthesize, but disappear beneath the sand if danger threatens. Courtesy Peter Barfield. the relationship between certain photosynthetic dinoflagellates, known as zooxanthel- lae, with stony, hermatypic (reef-forming) corals. Without zooxanthellae living within their bodies and providing them with an energy source in the form of photosynthetic products, the corals cannot survive for long. Coral bleaching, where the symbionts are lost due to stresses such as ocean warming, are currently threatening many coral reefs (see Section 9.2.5). Other coral reef ecosystem cnidarians and invertebrates, including soft corals (Octocorallia), jellyfish and giant clams (Tridacna spp.) also harbour zooxan- thellae. Zooxanthellae are described further in Section 7.4.3. Lichens are an example of a dual organism consisting of a fungus together with a microalga or cyanobacterium. The association is such that neither partner can live on its own in the wild and if each of the partners is cultured in the laboratory then they look nothing like the living lichen. The thallus (lichen body) is about 80% fungus and 20% alga or cyanobacterium. The association allows lichens to live in extremely inhospitable environments, such as high up on rocky seashores, on mountain tops, trees, houses and even gravestones. The fungus is provided with energy-rich carbohy- drates produced by its photosynthetic partner. The latter, although captive forever, can thrive in habitats that would normally be much too dry. This is an over-simplification, but there is no doubt that the two partners, each from different kingdoms of life, thrive together. A further example is the use of symbiotic, bioluminescent bacteria by deep-sea fishes, maintained in photophores for a variety of uses including defence and commu- nication (see Section 2.6.4 Bioluminescence).  Open water lifestyles: marine plankton 211 4.3 Marine zooplankton The zooplankton includes a very wide variety of animals but can be divided into two major ecological groups, according to whether they are permanently part of the plank- ton or just temporary residents. Permanent residents are known as holoplankton and include small animals such as copepods (Copepoda), arrow worms (Chaetognatha) and comb jellies (Ctenophora). They spend their whole life, from egg to adult, as part of the plankton. Animals that spend only part of their life cycle in the plankton are called meroplankton. The meroplankton includes eggs and larvae of benthic, sessile (fixed) animals such as sponges, anemones and hydroids and of mobile bottom-living animals such as gastropod molluscs, crustaceans such as crabs (Fig. 4.11) and lobsters and a vari- ety of ‘worms’. It also includes eggs and larvae of fish, cephalopods and other nektonic (swimming) animals and spores of seaweeds. Matching up meroplanktonic larvae to the appropriate adult form is a difficult and time-consuming process. There are many planktonic larvae for which the adult form remains unknown and vice versa. Every animal phylum present in the ocean is represented in the plankton, either as holo- plankton or as meroplankton. Some phyla such as arrow worms (Chaetognatha) and comb jellies (Ctenophora) are exclusively holoplanktonic, whilst most phyla include both holoplanktonic and meroplanktonic species, plus often some that have no plank- tonic phase at all. The zooplankton includes both herbivores and carnivores. The herbivores feed on phytoplankton and are often referred to as ‘grazers’ because their position in the food chains of the sea is comparable with that of herbivorous grazing animals on land. These animals have efficient filtration mechanisms for sieving microscopic phytoplankton, dis- persed in large volumes of water. The planktonic herbivores are mainly crustaceans Figure 4.11 Pisidia longicornis (A) Zoea larva; the hugely elongated rostral spine of porcelain crab (Porcellanidae) zoea helps deter would-be predators. (B) This adult is carrying eggs and when they are ready to hatch, they will be released to become part of the plankton. (A) Courtesy David Fenwick (Aphotomarine); (B) Courtesy Paula Lightfoot. 212 Elements of Marine Ecology (copepods, euphausids, cladocerans, mysids), certain gastropod molluscs known as sea butterflies (Pteropoda, Euthecosomata) and the pelagic tunicates. Planktonic carnivores include medusae, ctenophores, chaetognaths, polychaetes, hyperiid amphipods and the other group of pelagic gastropods with no shells, known as sea angels (Pteropoda, Gymnosomata). Feeding habits can differ between quite closely related forms; for example, although the majority of copepods feed chiefly on phytoplankton, some are carnivorous, particularly those that live at deep levels and some common copepods are omnivorous. The euphausids are also predominantly her- bivores, but there are carnivorous and omnivorous species. Some animals are highly specialized in their food requirements, for example, the sea angel Clione limacina appar- ently feeds only on another species of shelled pteropod, Limacina. In many cases, food requirements change with age. The majority of invertebrate larvae at first rely mainly upon phytoplankton for their food but become omnivorous or carnivorous later. Many fish larvae are at first omnivorous but later take only animal food. It is beyond the scope of this book to describe the complete range of zooplankton organisms. Some excellent general accounts are available and several are listed under Further Reading at the end of this chapter. In this section the most prominent and ecologically important groups of holoplanktonic animals are described briefly. 4.3.1 Crustaceans (Arthropoda: Crustacea) Crustaceans are the most conspicuous and abundant element of the permanent zoo- plankton, commonly amounting numerically to at least 70% of the total. In addition to holoplanktonic forms, great numbers of larvae are contributed to the meroplankton by benthic crustaceans. Larvae of crabs, barnacles and lobsters are very different in form from the adults and often have striking adaptations of shape that prevent them from sinking. The predominant group of holoplanktonic crustaceans is the Copepoda and cope- pods are a key link in the ocean food chain. Whilst only a few millimetres long at the most, they are present in incredible numbers and are represented by many thousand species. There are more than 1200 species around the British Isles, of which Calanus, Acartia, Centropages, Temora, Oithona, Pseudocalanus and Paracalanus are especially com- mon (Fig. 4.12). Another abundant group of planktonic Crustacea is the Euphausiacea. The best known of these is a large species, Euphausia superba (Fig. 4.12), which occurs in enor- mous numbers in the Southern Ocean south of the Antarctic Convergence. It consti- tutes the ‘krill’ upon which the giant baleen whales of the Antarctic feed, including the blue whale (Balaena musculus). E. superba is a keystone species in the ecology of Antarctic waters. In the north-east Atlantic, species of Nyctiphanes, Meganyctiphanes and Thysanoessa are common.  Open water lifestyles: marine plankton 213 cephalothorax antenna compound eye cephalothorax abdominals segments antennule telson throax eye abdomen antenna genital segment gills thoracopods egg sac (filter legs) 5 bifurcate pleopods (swimming legs) furca or caudal ramus (A) (B) Figure 4.12 Examples of important holoplanktonic crustacean groups: (A) A typical calanoid cope- pod, the most common type of holoplanktonic copepod; (B) Antarctic krill (E. superba), the predom- inant euphausiid shrimp in the Southern Ocean. From Dipper, F.A., 2016. The Marine World: A Natural History of Ocean Life. Princeton University Press (Wild Nature Press), 544 pp. Courtesy Marc Dando and Wild Nature Press. Figure 4.13 Examples of other holoplanktonic crustaceans: (A) Cladoceran Evadne nordmanni, with four juveniles within the body. This species is common in spring and summer around the British Isles; (B) The hyperiid amphipod Hyperia galba is a hitch hiker, here riding on a Moon Jellyfish (Aurelia aurita). Courtesy David Fenwick (Aphotomarine). Other less predominant crustacean groups that are sometimes numerous are the so- called water fleas (Cladocera), seed shrimps (Ostracoda) and amphipods (Amphipoda) (Fig. 4.13). Mysids or opossum shrimps (Mysidacea) mostly live close to the bottom but are sometimes found in coastal plankton, especially in estuarine regions. 4.3.2 Arrow worms (Chaetognatha) Arrow worms or chaetognaths constitute a common and widespread phylum of holo- plankton and are found in most plankton samples. Around the British Isles there are several species of Sagitta and Eukrohnia hamata that occasionally enter the North Sea 214 Elements of Marine Ecology from the Arctic. Worldwide there are around 130 described species. They are an important group of planktonic predators, shaped like a miniature torpedo and capable of catching and eating copepods, larval fish and even other arrow worms. They are a vital link in many food chains and are eaten in large numbers by pelagic fish such as herring. Chaetognaths are of special interest as ‘indicator species’ (see Section 2.7.7) and can be used to track the movement of water bodies, for example, tongues of warm water that periodically extend up the west coast of the British Isles. 4.3.3 Cnidarians and ctenophores (Cnidaria and Ctenophora) Some groups of cnidarians are truly holoplanktonic, for example, the hydrozoan Trachymedusae and Siphonophora. However, most hydrozoan medusae are set free by benthic hydroids and so form part of the meroplankton. Similarly, pelagic true jel- lyfish (Scyphozoa), such as the ubiquitous moon jellyfish A. aurita, might appear to spend their whole life cycle in the plankton, but in fact most have an inconspicuous benthic stage the scyphistoma, although this stage is omitted in some, for example, Pelagia. In contrast comb jellies (phylum Ctenophora) are holoplanktonic predators of widespread distribution. Pleurobrachia and Beroe are common genera found around the British Isles. The movements of their rows of comb-like cilia result in waves of col- ourful iridescence, making them amongst the most attractive of all zooplankton (Fig. 4.14B). 4.3.4 Polychaete worms (Annelida: Polychaeta) Several families of polychaete worms include holoplanktonic species, the most con- spicuous being the family Tomopteridae. The genus Tomopteris occurs throughout the world’s oceans. However, the majority of planktonic annelids are the various larval stages of benthic annelids and so are classified as meroplankton. Some benthic annelid worms also have an adult pelagic phase, usually associated with mass spawning. A well-known example is Palola, a genus of polychaetes found in shallow tropical waters, of which the best known is P. viridis from the south Pacific. For just the few days of the full moon in October and November, the egg and sperm-filled hind ends of these normally benthic worms, break off and join the surface plankton. Known as epitokes, they are considered a delicacy by Polynesian islanders. 4.3.5 Molluscs (Mollusca) A numerous and widespread group of holoplanktonic molluscs is the Pteropoda, small heterobranch gastropods. These are of two types, the tiny thecosomatous forms which have a very lightly built shell, for example, Limacina and the larger gymnosomatous forms which have no shell, for example, the sea butterfly Clione. The latter is large  Open water lifestyles: marine plankton 215 Figure 4.14 Examples of predatory holoplanktonic zooplankton found in the North Atlantic. (A) Stauridiosarsia gemmifera (Hydrozoa: Anthoathecata); (B) Pleurobrachia pileus (Ctenophora); (C) Doliolum sp. (Tunicata: Thaliacea); (D) Oikopleura (Vexillaria) dioica (Tunicata: Appendicularia). Courtesy David Fenwick (Aphotomarine). enough to be seen regularly by divers. Various other pelagic gastropods occur in warm oceans, for example, Carinaria, Pterotrachea and Janthina. These have light, fragile shells to assist floatation. As already mentioned in Section 4.1.1 Janthina, the Violet Sea Snail, is holopelagic, drifting at the surface of the sea by means of a float of mucus mixed with air bubbles. It feeds on the pelagic cnidarians, Porpita and Velella. Benthic molluscs produce innumerable meroplanktonic larvae. 4.3.6 Tunicates (Tunicata) Most tunicates are bottom-living sea squirts (Ascidiacea) and spend their lives attached to the seabed, but there are two planktonic classes: the Thaliacea comprising salps, dolioids and pyrosomes (e.g., Doliolum, Salpa, Pyrosoma) and the Appendicularia, previ- ously known as Larvacea (e.g., Fritillaria, Oikopleura) (Fig. 4.14D and Box 4.3). Appendicularians secrete a separate ‘house’ around themselves and through which they drive a current of water by wriggling their ‘tail’. This helps to concentrate food 216 Elements of Marine Ecology BOX 4.3 Neotony. Tunicates have a characteristic larval stage that resembles a bent tadpole in shape, with a trunk containing the body organs and a muscular tail. Larval tunicates have a notochord that runs the length of the body and this is what places the tunicates in the phylum Chordata, along with ourselves and all vertebrate animals. In vertebrates the notochord is replaced by a vertebral column as the animal develops. Appendicularians retain the larval features of a notochord and tadpole shape as adults, a condition termed neotony. Neotonous animals reach maturity whilst retaining various larval characteristics. Perhaps the best-known example is the axolotl, a type of salamander (Amphibia) which never loses its external larval gills. Appendicularians probably evolved through neotony from the tadpole larva of an ancestral, ascidian-like animal that lived attached to the seabed. particles for filtration through the pharynx and allows for collection of the smallest plankton, the nanoplankton and ultraplankton. Whilst appendicularians are tiny, these exceptionally abundant animals are an important link between the smallest plankton and the larger metazoans. They are eaten directly by larval fish, for example, European Plaice (Pleuronectes platessa). Both thaliaceans and appendicularians are a common component of the zooplank- ton in all oceans. Thaliaceans around the British Isles are mainly associated with the influx of warmer water from the south and west and on occasion, swarms of large salps are reported by divers off the west coast of Scotland, their rubbery bodies filling the surface layers. 4.3.7 Deepwater zooplankton Plankton is often thought of as living only in relatively shallow water down to a few hundred metres depth. Phytoplankton is, of course, restricted to this sunlit epipelagic zone and here too are large populations of herbivorous zooplankton grazing on these rich pastures. A large proportion of herbivorous zooplankton species undertake diel vertical migrations as described in Section 2.6.3, descending to deeper depths during the day to escape their predators. Predatory zooplankton have no such light require- ments and whilst the abundance of small but active hunters, such as chaetognaths and ctenophores, is greatest in the upper layers, many predatory zooplankton species hunt through the inky blackness of the mesopelagic and bathypelagic. These include coro- nate jellyfish such as Atolla and Periphylla, comb jellies and siphonophores. The larvae of many benthic species also form part of deepwater plankton populations. Gelatinous zooplankton, particularly medusae, are often common in the benthic boundary layer (BBL) along with an increased abundance of other plankton, compared to the abyssal water column above. The BBL is the water that lies just above the  Open water lifestyles: marine plankton 217 Table 4.2 Pelagic species recorded from hadal zones. Clade (group) Species Depth range of samples Ostracoda Archiconchoecilla maculata 9500 m Ostracoda Paraconchoecia vitjazi 9500 m Copepoda 20 species 6000 8500 m Mysidacea Boreomysis incisa 6000 7000 m Mysidacea Dactylamblyops tenella 6600 m Scyphozoa Stephanoscyphus spp. 6180 7000 m Scyphozoa Ulmaridae sp. 7847 8662 m Hydrozoa, Trachymedusae Pectis profundicola 6800 8700 m The species in this table were collated from Jamieson (2015), who himself collated records of hadal zone species (benthic and pelagic) from many disparate references and reports. seabed and which is therefore likely to be enriched in terms of nutrients. Smith et al. (2020) recorded large numbers of Benthocodon pedunculata in this zone in the abyssal Northeast Pacific, over a period of 3 years, using an autonomous time-lapse camera system. This benthopelagic, hydrozoan trachmedusa and other gelatinous zooplankton have been similarly observed in large numbers in the BBL elsewhere. They surmised that such concentrations must play an important ecological role in the BBL food web. Information about plankton from the abyssal and particularly deep trench hadal zones is necessarily limited by the difficulties inherent in sampling, especially in a quantitative way. This makes it difficult to assess the ecological role of these planktonic animals at these depths. Jamieson (2015) collated all known records and gives details of recorded hadal species, both planktonic and benthic (Table 4.2). Planktonic calanoid copepods (Calanoida), ostracods, mysids and medusae have all been collected from the hadal pelagic zone, albeit often in small numbers. Medusae, both hydrozoan and scyphozoan, are also present but are rare at these depths. 4.4 Planktonic food webs Primary production in the ocean results mainly from the photosynthetic activities of the phytoplankton and has already been discussed in Chapter 3 (Section 3.1), along with ocean food webs and trophic levels. Whilst plankton is the basis of almost all food chains/food webs in the ocean, it is so diverse in species, size and behaviour that there is a complex web of feeding opportunities just within the plankton itself. This is particularly obvious in the open ocean environment, where there may be several tro- phic levels preceding the level at which nektonic animals come into the picture. The reality in the open ocean (and other ecosystems) is one of a complex food web, where there are multiple interactions between multiple species. Some species can easily be assigned to a particular trophic level; an Orca (Orcinus orca) is undoubtedly a top 218 Elements of Marine Ecology predator and seemingly remote from the plankton being discussed here. However, the even larger Whale Shark (Rhincodon typus) feeds directly on plankton and may suck in an entire food chain, from phytoplankton through copepods up to small fish with each mouthful, though the smaller plankton will not all be retained by the gill rakers. The number of trophic levels within the food web of an ecosystem varies in differ- ent pelagic habitats and this is mainly as a result of the type and size of phytoplankton that prevails. If the predominant phytoplankton is of a size that can be eaten directly by zooplankton, then there may be fewer trophic levels. Diatoms and dinoflagellates often predominate in the phytoplankton in the water over productive continental shelves. These are large enough (microphytoplankton) to be eaten directly by cope- pods (mesozooplankton), which themselves can be eaten directly by planktivorous fish such as herring and these in turn by predatory fish eaters such as sharks. This example has four trophic levels, only two of which are planktonic. In particularly productive parts of the ocean such as regions of upwelling, there may be only one trophic level made up of phytoplankton. Large chain-forming diatoms are common in these areas and can be utilized directly by small fish such as anchovy, in turn eaten by large preda- tory fish such as tuna, making a short ‘chain’ of three trophic levels. A similar example from the Southern Ocean is shown in Fig. 3.2. Out in the less productive open ocean, there is a smaller variety and abundance of phytoplankton and much of it is in the tiny nanoplankton range (e.g., photosynthetic flagellates). This is too small to be eaten directly by copepods and must first be con- sumed by larger microzooplankton such as protozoans. Open ocean ecosystems there- fore often have up to six trophic levels. 4.5 Surface living and floating communities and species Neuston and pleuston (Section 4.1.1) are surface-living planktonic animals that tend to lead an individual existence, though some such as By-the-wind Sailor (Velella) may occur in huge numbers, pushed together by wind and waves. In contrast are entire floating communities of organisms that form on a temporary or permanent basis. The whole community lives a drifting ‘planktonic’ existence, but the individual species may be essentially benthic or nektonic. Almost anything that floats on the ocean sur- face for some time, such as large logs, will attract marine organisms to settle or take up temporary residence (Fig. 4.15). In areas that are not too far from the coast, seaweed and other algal spores often settle first, along with a variety of sessile animals such as hydroids. Large and relatively stable objects make an excellent resting place for sea- birds, whose droppings provide nutrients, thus encouraging algal growth. Once this undergrowth is in place, conditions may be such that the larvae of various mobile species settle out from the plankton.  Open water lifestyles: marine plankton 219 Figure 4.15 Stalked or goose barnacles (Lepas sp.) have settled and grown on this bottle whilst it was floating off the South Australian coast. Barnacles are often the first colonisers of floating objects. The cap on the bottle has proved a better attachment surface than the slippery glass sides. Many species will settle opportunistically but some are also specialists and various crustaceans especially are found only in such mobile habitats. Stalked goose barnacles, particularly species of Lepas, settle almost invariably on drifting objects, often far out to sea. Their larvae colonise logs, lost fishing buoys and other large drifting objects, either in ones and twos or sometimes hundreds. Columbus Crab (Planes minutus) larvae settle exclusively on floating objects and whilst this is usually flotsam and jetsam, some also associate with slow-swimming marine turtles. Whilst adults can swim, they only make short excursions, staying near the safety of their floating homes. Two species of floating pelagic Sargassum seaweed form the scaffold for a much more complex and long-term floating community. Sargassum natans and to a lesser extent S. fluitans form floating masses far out in the North Central Atlantic Ocean and especially in the Sargasso Sea, to the south and east of Bermuda. The seaweed accu- mulates and is corralled there by a huge ocean current eddy that forms part of the North Atlantic gyre. The seaweed provides a home for a wide variety of other species, some of which live only within this habitat, (Fig. 4.16) whilst others are benthic spe- cies that settle opportunistically on the seaweed. A complex mix of the seaweed along with various cnidarians, molluscs, worms, hydroids, bryozoans and other invertebrates provides food and shelter for open water fish, especially juveniles. Even seabirds are attracted and use dense rafts of the seaweed as resting and foraging places. The extent and diversity of this floating ecosystem vary from year to year depend- ing partly on weather and variations in water currents. Dense rafts many hundreds of metres across, elongated wind-blown strips and small patches are all common. Satellite imagery has shown that Sargassum also grows and develops within the Gulf of Mexico 220 Elements of Marine Ecology Figure 4.16 The well-camouflaged Sargassum frogfish (Histrio histrio) is endemic to rafts of floating Sargassum. Other endemics include species of anemone, crab, shrimp, amphipod and seaslug. From Shutterstock Ethan Daniels. in spring and is carried out into the Atlantic by currents in the summer, eventually reaching north east of the Bahamas by about February the next year (Gower and King, 2008). The extent of this external input of seaweed into the Sargasso Sea area each year is not yet clear but seems to be substantial and the Gulf of Mexico may be acting as a nursery for the seaweed. Sargassum species are notorious for spreading via vegetative fragmentation and in the calm and warm conditions of the Sargasso Sea, the seaweed can grow quickly. For S. natans and S. fluitans this is their only method of reproduction as they do not appear to reproduce sexually. However, the water in this area is relatively nutrient poor so an annual input from outside the area would maintain the community. The lifetime of an individual Sargassum is probably only around a year. Pelagic Sargassum is not confined to the Sargasso Sea area, but that is where floating rafts are best developed. S. natans is washed up on beaches as far apart as Canada, Europe and Brazil. Masses are also found off the coast of Nigeria in the Gulf of Guinea, where they sometimes cause problems with net fisheries. 4.6 Sampling and observing plankton Samples of plankton are traditionally collected by plankton nets and this is still very much the case today. However, plankton can also be collected using other methods such as water bottles and pumps (Section 2.3.2). Microscopic identification of plank- ton in the laboratory remains a vital part of plankton research but is time-consuming and requires taxonomic expertise. Many planktonic organisms are very sensitive to temperature and to keep a sample alive for any length of time, it must be kept at an even temperature as close as possible to that of the water from which it was filtered. Plankton samples can also be preserved using standard chemicals such as neutralized  Open water lifestyles: marine plankton 221 formalin. Rapid molecular methods for determining taxa present in collected samples have been developed in recent years, but these still need to be backed up by using tra- ditional identification methods. Samples collected for DNA analysis require specialist preservation methods. Plankton is not evenly distributed either horizontally or vertically and ‘patchiness’ is the norm, resulting from environmental variables, including temporal variation. Therefore a variety of methods are often needed to overcome this and to ensure that a sufficiently large water volume is sampled to ensure that abundance estimates are statistically reliable. Detailed methodologies and equipment for sampling, preserving, counting and viewing zooplankton, as well as much more information are given in Harris et al. (2000). A comprehensive account (and excellent photographs) of plankton nets and other plankton sampling systems as well as counting and viewing systems in use from the early days, through to the 21st century current state, is given in Wiebe and Benfield (2003). There were and are many ingenious designs and modifications. Identifying the plankton in a sample to species level is difficult and requires specialist knowledge and access to a comprehensive library of taxonomic keys and literature. However, there is now a wide variety of books and online sites that cover various groups in different oceans, seas or local coastal waters. Many of these are regional pho- tographic guides to the commonest species, especially of the larger zooplankton. 4.6.1 Plankton nets There are many different designs of plankton net and they come in various mesh sizes aimed at catching particular size classes of plankton, whilst avoiding unnecessary clog- ging. Plankton nets can be towed behind a slowly moving vessel or lowered from a stationary vessel and hauled vertically. Simple nets can even be operated by hand from pontoons, in rock pools or along the shoreline. Most consist essentially of a long cone-shaped net, with the mouth held open by a strong hoop to which the tow rope is attached by three bridles (Fig. 4.17). Size varies but a 25 100 cm diameter mouth is Figure 4.17 A simple plankton net in operation. Courtesy David Fenwick (Aphotomarine). 222 Elements of Marine Ecology commonly used. The narrow end of the net is firmly connected to a small metal or plastic container in which the filtered material becomes concentrated. After hauling, the net can be held vertically and hosed or washed with seawater to wash any material left on the mesh into the collecting container. In order to filter efficiently, plankton nets must be towed quite slowly, usually no faster than about 1 1.5 knots. Fine mesh presents high resistance to the flow of water through it and if towed too fast, the net sets up so much turbulence in the water that material is deflected away from the mouth. Many designs of plankton net have a reducing cone over the mouth which cuts down the volume of water entering the net to give more effective filtering. The original design of such nets was developed in the 1920s by Christian Hensen, a German researcher. Nets need to be constructed from materials and in ways that result in even meshes that do not deform under the strain of towing. Coarse mesh is more effective than fine mesh for catching the larger plankton, because it offers less resistance and allows a faster flow of water through the net and does not clog so easily. For collecting organisms over a wide range of sizes several grades of net are often used together. For collecting macro- plankton such as euphausiid shrimps, larger nets known as young fish trawls are some- times used, having a mesh of about 1 mm and an aperture of 1 2 m diameter. Neuston nets are similar to plankton nets but designed to skim the surface when being towed along, and so catch surface-living plankton. Frames are buoyant and vary in shape but are often rectangular in order to cover more surface area. These nets are also used to sample for floating microplastics (Section 9.1.6). Closing and opening closing nets When studying the vertical distribution and migration of plankton, it is necessary to have samples of plankton from particular levels. To avoid contamination of the sam- ples by organisms entering the net while it is being lowered or raised, there must be some method of opening and closing the net at the required depth. The simplest method of closure is to encircle the mouth of the net with a noose which can be drawn tight, as in the Nansen closing net (Fig. 4.18). This net is lowered vertically to the bottom of the zone to be sampled, not filtering on descent and is then drawn up through the sampling depths. A messenger sliding down the tow rope then releases the bridles from the tow rope, causing the throttle to draw tight and close the mouth of the net, which can then be hauled to the surface without further filtering. Nets that can be both opened and closed under water are used mostly for horizon- tal and oblique tows. The net is kept closed whilst being lowered to the required depth, is then opened for the tow, and closed immediately afterwards. There are many different net types of varying efficiency. They can be opened and closed by messengers, electric, sonic, time or pressure releasing mechanisms. A simple system  Open water lifestyles: marine plankton 223 Tow rope Messenger-operated release detaches bridles, transferring weight of net to throttle rope Bridle Throttle rope Canvas sleeve and throttle to close net Coarse mesh net Fine mesh net Receiver Weight Figure 4.18 The Nansen closing net. This simple net is rarely used today in unmodified form and has a tendency for part of the catch to escape on closure. involving two messenger-operated throttles is shown in diagrammatic form in Fig. 4.19. The net is lowered with the mouth closed by a noose. The first messenger releases this noose and the mouth of the net opens. After towing, a second messenger releases the bridles and another noose closes the mouth before the net is hauled up. Other nets have messenger-operated valves which open and close the mouth. Large systems may have several nets mounted on a frame that can be opened and closed at different depths before hauling. 224 Elements of Marine Ecology (A) (B) (C) Figure 4.19 A simple opening and closing plankton net operated by throttles of the type used widely in the early 20th century. (A) The net is lowered with the first throttle closed. (B) The first messenger frees the first throttle and the net opens. (C) The second messenger releases bridles and the strain is taken by the second throttle, closing the net before hauling. Nanoplankton and ultraplankton The smallest plankton, such as bacteria and microflagellates, escape through the meshes of ordinary nets. Very fine mesh can be manufactured using modern materials, but if too fine, the water will not pass through easily. So the sampling of nanoplankton and ultraplankton is usually done by collecting samples of seawater in sterile bottles or by pumping and then concentrating the organisms by allowing them to settle, by centrifuging or by fine filtration. 4.6.2 High speed and continuous plankton samplers As already stated, standard plankton nets must be towed slowly to be effective. They are therefore normally only operated from research boats and ships that can go where they want to and at their chosen speed. The scope of plankton studies can be extended by using equipment that can be towed behind commercial vessels, such as container ships, proceeding on their normal routes (Box 4.4). For this, high-speed plankton samplers are needed that can operate effectively at the speeds at which these ships normally sail, that can be easily deployed and that do not interfere with the functioning of the ship. High-speed samplers are of course also used by research vessels.  Open water lifestyles: marine plankton 225 BOX 4.4 Continuous plankton recorder survey. The CPR, currently operated by the Marine Biological Association (MBA) of the United Kingdom, marked 60 years of continuous plankton recording, using standardized methods of collection and analysis, in the North Atlantic in 2018. The survey actually started in 1931 but methodologies differed until standardization in 1958. The first continuous plankton recorder instrument was invented by Sir Alister Hardy in the 1920s. CPR instruments provide a contin- uous record of the plankton collected over long-distance hauls. The current models used by the MBA can operate successfully up to around 25 knots and are towed by a large number of volunteer merchant ships on various routes across the North Atlantic. Instead of being col- lected into a ‘cod end’ container, the plankton is filtered by continuously moving bands of filter silk, wound through the apparatus, powered by a propeller. The silk is wound onto a take-up spool in a formalin reservoir, where the plankton is preserved undisturbed. Preloaded cassettes containing rollers with the filtering silk make it easy to load and unload and also allow for really long tows over several thousand nautical miles. Electronic sensors for depth, salinity and temperature provide associated information. Back in the MBA labora- tory, the collecting silk can be divided up into lengths representing 10 nautical mile tows and the plankton identified and counted using standard procedures. The survey is on-going and continues to provide a means of mapping plankton populations and pin-pointing changes. This is of particular interest in terms of possible changes resulting from ocean warming. A total of more than 6.5 million nautical miles has now been towed. Similar CPR surveys are now conducted by many other countries throughout the world’s oceans and in 2011 a Global Alliance of Continuous Plankton Recorder Surveys (GACS) was set up. A continuous plankton recorder ready to deploy. Copyright Marine Biological Association, UK. For high-speed sampling the net area must be very large in relation to the aperture to reduce the high back pressure developed when a fine-mesh net is towed rapidly through water. Various designs and sizes have been developed and modified over the years, but all involve either a casing or a framework to hold and protect the net and a conical nosecone. Water enters a small opening at the front, filters through the 226 Elements of Marine Ecology enclosed plankton net and leaves through a rear aperture. A mechanical or electronic flow meter enables the volume of water filtered to be calculated. High-speed samplers are often used to sample at deep depths and usually also incorporate CDT’s (see Section 2.3). They are also better at sampling larger or more mobile organisms such as fish larvae and eggs. 4.6.3 Quantitative plankton studies Quantitative plankton studies aim to estimate numbers, density or weights of organisms beneath unit area of sea surface or in unit volume of water. An approximation of the volume of water passing through a plankton net can be calculated from πr2d, r being the radius of net aperture and d the distance of the tow. Positional instruments (GPS) can help determine the tow distance with reasonable accuracy. However, a net does not filter all the water in its path and the filtering rate reduces as material collects on the mesh and the resistance of the net increases. A more accurate measure of the filtered volume can be obtained using mechanical or electronic flow meters, which can record the volume entering the net, or leaving in the case of enclosed high-speed samplers. The patchiness of plankton also needs to be taken into account when designing a sam- pling programme. The more samples that can be taken at different stations spread over the area of investigation, the better. Nets also vary in their ability to retain plankton, some of which can be displaced from the path of the net by turbulence small organisms may escape through the meshes and the larger active forms may avoid capture by swimming. Another method of collecting plankton is the plankton pump. These are particu- larly useful in shallow water and to sample at specific locations. Water is simply drawn up a hose and pumped through nets or filters to trap the plankton. Simple pumps sam- pling shallow depths can be operated from small boats. Large ships can operate sub- mersible electric pumps capable of raising many litres of water a minute from depths down to about 100 m. This method allows an accurate measure of the volume of water filtered and from which depth and also allows chemical analysis of the actual water from which the plankton is filtered. After filtering, the water can be centrifuged or otherwise sampled for the smallest organisms that escape through nets. Despite these advantages the method has some drawbacks. Large organisms are prone to damage as they pass through the pump, the stronger-swimming zooplankton may escape being sucked into the hose and there are difficulties in the use of pumps to obtain samples from deep levels. For most purposes quantitative investigations are done on plankton samples which have been filtered from a known volume of water, the method depending on the type of study. Sometimes an estimate is wanted of the gross quantity of plankton of all types. A rough volume estimate can be made very simply by allowing the sample to settle in a measuring cylinder and reading the volume directly from the scale.  Open water lifestyles: marine plankton 227 Measurements of displacement volume are probably rather more accurate, and esti- mates can also be made by weighing, either as a rough wet weight, or better, by dry- ing to constant weight. Plankton counting Numbers of planktonic organisms can be counted by electronic instruments towed from ships. These count the number of small organisms present in the water which flows through the instrument. The apparatus is essentially a tube containing electrodes connected to circuitry which records the change of impedance when objects pass between the electrodes. This enables an estimate to be made of both number and size of organisms. In the laboratory detailed investigations might require direct counting from col- lected samples. Large organisms are usually few in number and can be individually picked out and counted. Smaller organisms may be so numerous that the sample must be subsampled to reduce them to a number and volume that it is practicable to count. The subsample can be spread out in a flat glass dish and examined, with a microscope if necessary, against a squared background or using a plankton counting chamber. For very small organisms present in large numbers, the haemocytometer used by physiolo- gists for counting blood cells can be used for plankton counting, or a Coulter particle counter can be adapted for this purpose. See also Section 3.2.1 (Standing stock measurements). 4.6.4 Plankton collection by divers and underwater vehicles Gelatinous plankton such as scyphozoans and salps are easily damaged by nets and in shallow water are best captured by divers using wide-mouthed containers. Planktonic foraminifera have also been collected in this way. ‘Blue-water diving’ over deep water carries certain risks, including disorientation where there are no reference points to indicate up and down. A diving platform and tethers are often employed for safety. Blue-water diving has also contributed much useful information on the behaviour and mode of life of these animals (Madin et al., 2013). Deepwater gelatinous plankton can be collected from submersibles and ROVs (see Section 7.5.3) using robotic arms. However, unless they can be placed directly into pressure-proof containers, specimens may suffer damage on returning to the surface. ROVs can also be used to carry out video profiles through the water column, allow- ing large plankton such as jellyfish to be identified and counted. Autonomous underwater vehicles (AUVs) are increasingly being used to collect environmental information in the ocean but can also be adapted to take water samples simultaneously for plankton analysis. AUVs fitted with large ‘gulper’ water bottles that draw in water rapidly using a piston suction method, can collect multiple, large vol- ume samples at specific locations. On-board computer software can direct when 228 Elements of Marine Ecology samples are taken, based on environmental data, such as chlorophyll levels. The vehi- cles can cover much larger areas than using traditional nets and sample patches of plankton found under specific physical conditions. These physical processes can then be linked to plankton distribution and diversity (Harvey et al., 2012). Further reading Castellani, C., Edwards, M., Boxshall, G.A., 2017. Marine Plankton: A Practical Guide to Ecology, Methodology and Taxonomy. Oxford University Press, 694pp. Gershwin, L.-A., 2016. Jellyfish: A Natural History. Ivy Press, United Kingdom. Lenz, J., 2000. Introduction. In: Harris, R.P., Wiebe, P.H., Lenz, J., Skjoldal, H.R., Huntley, M. (Eds.), ICES Zooplankton Methodology Manual. Academic Press, London (Excellent introduction with plates showing all zooplankton groups). Munn, C., 2011. Chapter 4 Marine bacteria. In: Marine Microbiology: Ecology and Applications, 2nd (ed.) Garland Science, USA and UK, 364pp. Newell, G.E., Newell, R.C., 2006. Marine Plankton. A Practical Guide. Pisces Conservation, 223pp. Facsimile paperback edition of the original 1979 book. Suthers, I.M., Rissik, D., Richardson, A.J. (Eds.), 2019. Plankton: A Guide to Their Ecology and Monitoring for Water Quality. Second ed. CRC Press, 236pp. Thomas, C.R. (Ed.), 1993. Marine Phytoplankton. A Guide to Naked Flagellates and Coccolithophorids. Academic Press, London. Winter, A., Siesser, W.G., 1994. Coccolithophores. Cambridge University Press. Resources Journal of Plankton Research. Oxford Academic. The website of ‘Diatoms Online’ a project of the Natural History Museum, London to make their dia- tom collection accessible to the public and researchers. ,http://www.diatoms.myspecies.info..