Organic Production and Cycling in the Ocean PDF

CHAPTER 3 Organic production and cycling in the ocean Early biologists thought that nothing could live in the deep ocean. Edward Forbes, writ- ing in 1843, considered 550 m to be the limit and even as late as 1948, Hans Pettersson conjectured that 6500 m was as deep as life could exist. We now kno...

CHAPTER 3 Organic production and cycling in the ocean Early biologists thought that nothing could live in the deep ocean. Edward Forbes, writ- ing in 1843, considered 550 m to be the limit and even as late as 1948, Hans Pettersson conjectured that 6500 m was as deep as life could exist. We now know that life is unequivocally present from the surface right down to the deepest ocean depths. This means that a source of energy (food) must be available throughout the ocean, but we also know that light is not. Almost all life is ultimately dependent on the carbon-fixing abilities of photosynthetic organisms and in the ocean, these can only live in the epipe- lagic or sunlit zone. So the many habitats, ecosystems and species described in the fol- lowing chapters of this book, from the surface and seashore down to the deepest hadal zone, could not exist without the productive surface waters. For example, sea cucumbers or holothurians (Holothuroidea) thrive in deep-sea trenches even at depths of more than 7000 m, feeding on detritus that originated from the surface waters above, albeit often through many intermediate organisms. In the ocean, deep-sea hydrothermal vents and ‘cold seep’ communities are exceptions to this dependence on photosynthetic pri- mary producers, deriving energy from chemical sources (Section 7.4.6). 3.1 Primary production in the ocean Seaweeds (macroalgae), seagrasses, algae and especially phytoplankton, are the ocean’s primary producers. These autotrophic organisms carry out photosynthesis, just as plants do on land and manufacture organic compounds from the inorganic constituents of sea- water. This is termed primary production. Gross primary production (GPP) is the total production and net primary production (NPP) is GPP minus losses due to respiration. In terms of the amount of carbon produced per unit area per year, seaweeds and seagrasses are far more productive than phytoplankton. However, seaweeds and sea- grasses are restricted to coastal locations, whereas phytoplankton flourishes in the sur- face waters over vast tracts of ocean. Therefore in terms of ocean productivity, phytoplankton is by far the major player and accounts for over 90% of NPP in the euphotic zone of the ocean. Under favourable conditions phytoplankton is capable of remarkably rapid growth, sometimes producing its own weight of new organic mate- rial within 24 hours, a rate greater than that achievable by land plants. There is also some primary production by bacterial chemosynthesis (see Section 3.1.4). Elements of Marine Ecology r 2022 Elsevier Ltd. DOI: https://doi.org/10.1016/B978-0-08-102826-1.00003-X All rights reserved. 153 154 Elements of Marine Ecology The basic raw materials for photosynthesis are water (H2O) and carbon dioxide (CO2), though various other inorganic ions, principally nitrate and phosphate (nutri- ents) are needed for growth. Chlorophyll-containing organisms use light energy to drive the manufacture of complex organic molecules from these simple substances. This is termed GPP. The chief products are the three major categories of food materi- als, namely carbohydrates, proteins and fats (Steeman Nielsen, 1975). Oxygen, derived from the water, is produced as a byproduct and phytoplankton are calculated to pro- duce around 50% of all the oxygen in the atmosphere. The photosynthetic process is extremely complex and involves a large number of steps but can be summarized by the following very general equation: 6CO2 1 6H2 ð 1 light energyÞ"C6 H12 O6 1 6O2 Some of the organic material manufactured by plants is broken down again by an oxidative reaction, to an inorganic state by the photosynthetic organisms themselves in the course of their respiration. Hence the equation is written as a reversible one. The remainder is referred to as NPP and this is then available for growth and reproduction of the photosynthetic organisms. This is of major importance as the source of food for herbivorous animals. The animal population of the ocean therefore depends, directly or indirectly, upon the NPP (Fig. 3.1). Photosynthesis and primary production in the ocean is a complex topic and readers wanting to explore the processes further, should consult the references listed under Further reading at the end of this chapter. 3.1.1 Food webs and trophic levels Once primary producers have manufactured organic matter, it becomes available for nonproducers to use as food. In the simplest concept of feeding relationships, herbivo- rous animals eat primary producers and convert them into animal tissue. This is termed secondary production and a herbivorous animal, such as copepod grazing on diatoms, is a primary consumer. The herbivores provide food for the first rank of carnivorous animals, that is tertiary production. An arrow worm (chaetognath) eating copepods is therefore a secondary consumer and a small fish eating arrow worms would be a ter- tiary consumer and so on (Fig. 3.1). Each of these successive stages of production of living tissue is a link in a food chain, each link being termed a trophic level (Fig. 3.2). Because many animals take food from several trophic levels, food chains become inter- connected to form intricate food webs. The maximum number of trophic levels varies within different ecosystems and tends to be greatest in the open ocean. However even here the maximum is rarely more than six, due to large energy ‘loss’ (export) at each level, principally through animal metabolism. Much of the food that animals assimilate is broken down by respiration, leaving only a small proportion to form new tissue.  Organic production and cycling in the ocean 155 Light energy Photosynthesis Plant nutrients Gross primary and production by algae, CO2 seagrasses and phytoplankton Herbivores Zooplankton, molluses etc., Secondary production Excretion 1st rank carnivores Respiration Direct Zooplankton, fish etc., Energy transformations regeneration Teritary production and CO2 formation DOM Later carnivores Microbial e.g fish, mammals CO2 loop (see Fig. 3.3) Bacterial decomposition Indirect regeneration of nutrients from dead organic matter Figure 3.1 An outline of the main stages of energy flow and trophic levels (the organic cycle) in the ocean. Orange lines show flow of energy; blue lines show flow of materials. Other losses of organic material between each trophic level result from different causes. For instance, a proportion of the organisms at each trophic level are not eaten by animals, but simply die and decompose by autolysis and bacterial action. Some of the food that animals consume is egested unassimilated. The efficiency of transfer of organic matter from one trophic level to the next varies with the types of organisms, herbivores generally doing rather better than carnivores. In broad terms about 100 g of food are consumed for every 10 g of animal tissue formed, that is a gross conversion efficiency of 10%. Herbivorous zooplankton can sometimes exhibit 156 Elements of Marine Ecology efficiencies of about 30% and certain larval stages do somewhat better, but even after allow- ing for these higher efficiencies, only a small part of the original plant production becomes incorporated into animal tissue. Thus primary production can be regarded as the broad base of a food pyramid, the successive smaller trophic levels being a series of steps towards the apex of final rank carnivores. In terms of human consumption it is more efficient to farm herbivorous or planktivorous fish that lie near the base of the food chain, rather than carniv- orous species near the top (not taking into account the ease or difficulty of rearing different species and the food they are actually fed). In this respect salmon are not as good a choice for farmed fish as, say, Milkfish (Chanos chanos), which feeds on filamentous algae, cyanobac- teria and plankton. Eventually, as a result of respiration and excretion, death and decomposition, organic materials become broken down and returned to the water as simpler sub- stances, which plants can utilize in primary production. In this way, matter is continu- ally cycled from inorganic to organic forms and back to inorganic state. The initial synthesis of organic material involves the intake of energy to the system and this is supplied by sunlight. The transference of organic matter from one trophic level to the next is part of the energy flow of the cycle (Fig. 3.1), energy being continually lost from the system and in due course becoming dissipated as heat. 3.1.2 The microbial loop and dissolved organic matter In the marine ecosystem the simple account of the organic food cycle given in Section 3.1.1 must be extended to take account of the significance of dissolved organic matter (DOM) and especially dissolved organic carbon (DOC) in seawater. DOM is a minor but vital constituent of seawater and is described in Section 2.2.2. More than half of the carbon fixed by autotrophic and chemotrophic organisms is routed through DOM and then processed by heterotrophic microbes (Carlson and Hansell, 2015). As mentioned in Section 2.2.2, an appreciable proportion of the products of Figure 3.2 Simple food chains are rare in the ocean because many animals eat a variety of food taken from different trophic levels. However, where a keystone species is present in an ecosystem, food chains can be particularly short. Antarctic krill (Euphasia superba) is the main food of baleen whales in the Southern Ocean. The krill feeds directly on phytoplankton and small zooplankton. From Shutterstock: Jan Kratochvila (Humpback Whale); I. Noyan Yilmaz (Antarctic Krill); Choksawatdikorn (phytoplankton).  Organic production and cycling in the ocean 157 photosynthesis are released by various means from the cells of primary producers and soon appear in the water as DOM. Some of this material may leach from plant cells, some may be lost during cell division and much may be routed through the feeding, excretion and egestion of animals. Some zooplankton organisms grazing on phyto- plankton, liberate into the water appreciable quantities of DOM from plant cells, by breaking up the frustules prior to ingestion, so-called ‘sloppy feeding’. Although some of this component of primary production may be reabsorbed by phytoplankton, much of it is rapidly taken up by planktonic bacteria. The importance of these bacteria in the organic food cycle of the sea was only realized when their abundance in the water column became clear. Before the development of filters that can retain the smallest bacteria of 0.5 µm or less and of other techniques such as e DNA, the immense contribution made by bacteria and archaea was unappreciated. These bacteria are thought to utilize the greater part of DOM as a nutrient source. By virtue of their small size and correspondingly large surface-to-volume ratio, the bacteria are well adapted to absorb nutrients at low concentrations. Some estimates suggest such direct uptake may account for up to 50% of the total annual production of DOC (Andrews and Williams, 1971). This uptake of DOM results in increased bac- terial production which in turn is grazed by the smallest heterotrophic nanoplankton, mainly single-celled flagellates. These provide food for slightly larger single-celled zoo- plankton, chiefly ciliates, which are then preyed upon by larger metazoan zooplank- ton. The ciliates may be considered as the ‘top predator’ micro-organisms within the microbial food web (Lenz, 2000). In this way, the so-called ‘microbial loop’ (Fig. 3.3) returns a proportion of the energy from primary production released into the water as DOM to the main food-web, as well as particulate organic matter that is too small to be eaten directly by metazoan plankton. The relationships are complex and not yet well understood. The microbial food web includes ultra-small picoplankton and nanoplankton (,5 µm) that are autotrophic and contribute to primary production along with larger phytoplankton. Some micro- organisms not only have photosynthetic pigments, but can also ingest bacteria, thus obtaining energy both by photosynthesis and from bacterial protoplasm. At each stage of the microbial food-chain, animal metabolism returns to the water some DOM as well as inorganic nitrogen and phosphorus compounds, thereby restoring to some extent the supply of major nutrients for photosynthetic organisms. This simplified account illustrates the intricacy of the ‘microbial loop’, which in recent years has become increasingly recognized as a significant part of marine food-webs. 3.1.3 Regeneration and nutrient re-cycling Primary production by autotrophic phytoplankton, algae and marine plants such as seagrasses, requires nutrients, particularly phosphorus and nitrogen. These nutrients are 158 Elements of Marine Ecology CLASSICAL FOOD CHAIN CO2 nutrients Planktivores Herbivores nekton and Piscivores mesa and micro Phytoplankton carnivorous nekton zooplankton zooplankton MICROBIAL LOOP DOC Ciliates Bacteria HNF Figure 3.3 A simplified schematic illustration of the microbial loop (bacteria and micro-organisms) and how it fits in with the basic pelagic grazing food chain (phytoplankton to piscivorous fish). DOC, Dissolved organic carbon; HNF, heterotrophic nanoflagellates. Modified from Lalli and Parsons, 1997 by kind permission of Elsevier Butterworth-Heinemann. re-cycled or regenerated, over and over again through complex processes that degrade organic compounds. Metabolic waste products from marine organisms and their bodies once they die provide these compounds. There is considerable input of dissolved nutrients, especially nitrates and phosphates, from land runoff. This in turn is derived from land organisms and weathering of rocks. Marine animals such as seabirds and pin- nipeds, cycle nutrients between land and sea. Most of the excretory products of marine animals can be directly utilized by pri- mary producers  seagrasses, algae, phytoplankton and other photosynthetic organ- isms. This is ‘direct’ regeneration as the products set free into the water by animal metabolism are used directly. Phosphorus is excreted mainly as phosphate with some soluble organic phosphorus. In most marine animals, nitrogen is excreted mainly as ammonia. The majority of ray-finned fishes (Actinopterygii) excrete part of their waste nitrogen as trimethylamine oxide (see Section 2.2.1). Some animals also excrete amino acids, uric acid or urea. However, whilst these compounds are utilizable directly in varying degrees by photo- synthetic organisms, many of the nutrients are actually regenerated by ‘indirect’ processes involving bacterial and fungal (even in the ocean) activity. Bacteria are an essential part of the organic cycle, necessary for the decomposition of particulate organic matter from fae- cal pellets and the bodies of dead organisms. After death, the tissues of photosynthetic  Organic production and cycling in the ocean 159 organisms and animals become converted by degrees into soluble form. Dissolution may be initiated by autolysis, the tissues being broken down by the dead organisms’ own enzymes, but decomposition is brought about mainly by bacterial action. Bacteria are abundant on the surface of organisms and detritus and are especially numerous in the uppermost layers of bottom deposits. Bacterial metabolism converts solid organic matter into organic solutes and eventually into an inorganic form. Regeneration of phosphorus is mainly to phosphate, although to some extent auto- trophs can also absorb certain dissolved organic phosphorus compounds. Following the death of marine organisms, much of the phosphorus in their tissues returns very quickly to the water as phosphate, indicating that decomposition of organic phosphorus com- pounds is probably largely by autolysis and hydrolysis. Particulate organic phosphorus is acted on by bacteria producing various solutes that can then be taken up or further degraded by bacteria to phosphate. The main pathways of the phosphorus cycle are illustrated in Fig. 3.4. Nitrogenous organic materials are broken down more slowly than phosphorus compounds, mainly by bacterial action. Particulate and dissolved organic nitrogen (DON) are converted by bacteria first to ammonium ions and then further oxidized to nitrite and finally to nitrate. Algae, phytoplankton and other photosynthetic organisms absorb nitrogen mainly as nitrate, but some can also make use of nitrite, ammonium and various simple organic solutes. Some cyanobacteria (e.g. Trichodesmium) and bacte- ria (Azotobacter, Clostridium, Desulfovibrians etc.) are capable of fixing dissolved elemen- tal nitrogen, but this is probably not a major addition to nitrogenous compounds in the sea because of the high energy intake required for this reaction (see also Section 2.2.3). Nitrogen in the atmosphere is fixed by land plants, bacteria and other micro-organisms and enters the sea through land runoff. Some bacteria in anaerobic conditions obtain energy from organic carbon compounds by oxidations involving the reduction of nitrate to elemental nitrogen, that is, nitrogen-freeing. The main path- ways of the very complex nitrogen cycle of the sea are shown in Fig. 3.5. Sulphur-containing compounds are regenerated mainly as sulphate. Bacterial decomposition of organic sulphur commonly yields hydrogen sulphide, which can be oxidized to elemental sulphur (by Beggiatoa) and thence to sulphate (by Thiobacillus). The nitrogen and sulphur cycles are closely interconnected by a variety of bacterial reactions involving both groups of compounds. In the course of these various processes of regeneration and recycling, bacteria themselves grow and multiply and constitute an important component of the food supply. Bacteria therefore perform two major functions in marine food cycles: the breakdown of dead organic matter into soluble forms, mainly inorganic ions, which can be utilized by plants, and the transformation of dead organic matter into bacterial protoplasm which is directly utilizable as food by some animals. 160 Elements of Marine Ecology Land runoff P-compounds in P-compounds in plant tissues animal tissues Consumption by animals es absorption Death Faec Plant P-compounds in bacterial protoplasm Excretion Particulate P-compounds ion Autolysis and po l m ria hydrolysis sit co cte de Ba PO4 ions Dissolved organic Bacterial action P-compounds (DOP) Loss to sediments Figure 3.4 Main pathways of the phosphorus cycle in the ocean. DOP, Dissolved organic phospho- rus; P, phosphorus; PO4, phosphate. Autotrophs: plants, algae, phytoplankton and micro-organisms. There are continuous losses of organic material from the euphotic zone due to sinking and to movements by animals down to deeper levels after feeding. Some of this material may reach the bottom and become lost from the cycle by being perma- nently incorporated in the sediment. The greater part is regenerated in deep layers of water or on the bottom and nutrients therefore accumulate below the euphotic zone. The continuation of production depends upon the restoration of nutrients from the deep to the surface layers by vertical water mixing or upwelling (see Section 2.7.4). 3.1.4 Chemosynthesis Some of the bacteria involved in recycling and regeneration are autotrophic. They function as primary producers of organic compounds by reduction of carbon dioxide  Organic production and cycling in the ocean 161 N-compounds in Consumption by animals N-compounds in autotrophes Leac animal tissues hing and Sin exoc s N-fixing rines due anim tion kin esi ath De als phytoplankton ga al r p nd c Fae sum de ath Con Atmospheric N2 by Dissolved N2 Dead particulate N-compounds in N-compounds bacterial protoplasm Denitrifying bacteria Land drainage sewage, etc. N-fixing bacteria Ba Death cte Autotroph absorption ri actio al Animal excretion n N-compounds in sediments rbtion n NO3 ions tio ila Abso s sim la ia Nitrification by t er bacteria (Nitrobacter) B ac Nitrification by Ammonification by DON, amino acids NO2 ions NH4 ions bacteria (Nitrosomonas) bacteria urea, etc. Figure 3.5 Main pathways of the nitrogen cycle in the ocean. DON, Dissolved organic nitrogen. in chemosynthetic reactions which parallel the photosynthetic processes of plants, but derive energy from inorganic chemical sources rather than from light. For instance, the bacteria Nitrosomonas and Nitrobacter, which oxidize ammonia to nitrite and thence to nitrate, utilize the energy released by these reactions for synthesizing organic mate- rials within their protoplasm. Beggiatoa and Thiobacillus are chemosynthetic autotrophs obtaining energy from oxidation of sulphide and sulphur. Beggiatoa can be seen as a white mat covering the sea-bed where conditions are anoxic, such as under floating fish farm cages. Oxidation of iron to the ferrous and thence the ferric form is another energy source for chemosynthesis. It is now known that primary production by bacterial chemosynthesis contri- butes a significant fraction of the food available at depths remote from the euphotic zone. Deep-sea hydrothermal vent communities (see Section 7.4.6) are entirely dependent for their energy requirements on dissolved hydrogen sulphide and parti- cles of sulphur in the hot vent water. If the vents become inactive, the communi- ties die. Dense clouds of chemosynthetic bacteria form the base of the food pyramid. The hydrothermal vent ecosystem is thus entirely self-contained and does not rely either directly or indirectly on sunlight (Box 3.1). Measurements have also indicated that hydrothermal communities are among the most productive on earth. 162 Elements of Marine Ecology BOX 3.1 Bacterial chemosynthesis. The hot fluids emerging from hydrothermal vents contain large quantities of hydrogen sul- phide. Chemosynthetic bacteria are capable of oxidizing hydrogen sulphide to release the energy required to produce organic matter from carbon dioxide and water (in photosyn- thesis the energy for this comes from sunlight). A number of complex and sequential chemical reactions are involved but the process can be summarized by the following sim- ple equation: H2 S 1 CO2 1 O2 5 CH2 O 1 H2 SO4 Chemosynthetic bacteria can also be found in anaerobic sediments and cold seeps, where hydrocarbon-rich fluids emerge from fissures in the seabed (see Section 7.4.6). 3.2 Measurement of primary production Primary production from phytoplankton in the open ocean can be and has been mea- sured in various different ways, mostly carried out in the laboratory (including aboard ship), using collected samples. These techniques are still important today, but remote sensing using satellite technology now allows large-scale measurements in the field. In situ measurements can also be made using ship-towed devices and to an increasing extent, Autonomous Underwater Vehicles (AUVs). An outline of the main laboratory and in situ methods is given here. All these techniques contain inherent inaccuracies and estimates of production will always be just that  estimates, though current techniques are providing much more reliable data. Production rates are usually expressed as the amount of carbon fixed by photosynthesis in organic compounds, per unit area of surface (open ocean or seabed) or water volume per unit time. For example grams of carbon per square metre per year (g C m22 per year) or grams of carbon per cubic metre per day (g C m23 per day). Estimates of NPP by phytoplankton mostly fall within the range 0.10.5 g C m22 per day with values of more than 1 g C m21 per day in the most productive, upwelling sea areas. Amounts are usually expressed as NPP, which is the GPP, less carbon lost through respiration of the primary producers. Differences in productivity between various ocean regions are discussed in Section 3.5 where comparisons are also made between production on land and in the ocean. 3.2.1 Standing stock The standing stock is a measurement of the total amount of organisms (e.g. phytoplank- ton, or fish) present at the time of measuring, within a unit of either area or volume.  Organic production and cycling in the ocean 163 This can be expressed (measured) in a variety of ways including biomass (wet weight), number of organisms, organic carbon, chlorophyll or adenosine triphosphate (ATP). By measuring changes in biomass, primary production can be estimated. For phytoplankton, a common measure of biomass is chlorophyll a concentration (mg/m3). This does not give a direct indication of the rate of production, because account must be taken of the rate of turnover. If, for example, the phytoplankton or seaweed is being very rapidly eaten, high production may maintain only a small standing stock. On a well-lit coral reef, as much as 15 kg of seaweed can grow on every square metre in a year. However, at any one time, only a few small pieces may be seen, because herbivorous fish and urchins quickly graze the growths down (Shepard, 1983; Sheppard et al., 2009). Alternatively, where the consumption rate is very low and the plants are long lived, a large standing stock is not necessarily the result of a rapid production rate. A large stand- ing stock may itself limit production by reducing the penetration of light through the water and diminishing the supply of nutrients. The size of the standing stock depends upon the balance between the rate of pro- duction of new plant cells and the rate at which they are lost by animal consumption and by sinking below the photosynthetic zone. To determine production rates from standing stock measurements it is therefore necessary to estimate both the rate of change in size of the population and also the rate of loss, the latter being particularly difficult to assess with any certainty. Chlorophyll estimations Remote sensing: Large scale estimates of primary production in the open ocean are now carried out primarily using remote sensing via satellite data. Colour scanners measure ocean radiance  the light radiated back after sunlight hits and penetrates the ocean sur- face. Some of the measured light will also be from bioluminescence generated by marine organisms. The concentration of pigments (mainly chlorophyll) within photosynthetic phytoplankton (primary producers) in the surface layers will affect ocean radiance. Powerful computers using algorithms, are able to carry out the complex calculations needed to convert ocean radiance measurements to an estimate of photosynthetic pig- ment concentration and ultimately estimates of primary production. Maps can then be produced on various scales using colours to indicate the chlorophyll concentration in milligrams of chlorophyll pigment per cubic metre of surface water (Fig. 3.6). Geographical and temporal differences in productivity can be mapped, providing essen- tial data, for example for fisheries management and climate change predictions. Maps and data are available online from NASA Earth Observations. See also Section 2.3.3. Fluorescence: Chlorophyll can also be measured in the field by instruments that detect its fluorescence. Such instruments send out pulses of light at predetermined wavelengths that excite the chlorophyll to fluoresce. Chlorophyll fluorescence sensors can be attached to a multitude of different systems carrying sensors for measuring other 164 Elements of Marine Ecology Figure 3.6 Ocean chlorophyll concentration for the month of April 2020 derived from data mea- sured by MODIS (Moderate Resolution Imaging Spectroradiometer) on NASA’s Aqua Satellite. Courtesy NASA. https://neo.sci.gsfc.nasa.gov/view.php?datasetId=MY1DMM_CHLORA. water parameters, such as Conductivity Temperature Depth sensors, fixed moorings and profilers and to undulators towed from ships, some of which are described in Section 2.3. Fluorescence sensors can also be included in the payload of AUVs a nd remotely operated vehicles (ROVs) (Section 7.5.3). A technique called Fast Repetition Rate Fluorometry is being used with increasing success to measure photosynthetic rates in real time. In coastal waters where phytoplankton blooms are common, data on chlorophyll concentration can also be obtained using a technology known as Light Detection and Ranging. Pulsed lasers stimulate the phytoplankton chlorophyll to fluoresce and sensors detect it. Laboratory estimates: On a small or local scale, chlorophyll can be physically extracted from a unit volume of seawater. The seawater is filtered or centrifuged to collect all the phytoplankton cells. The chlorophyll is then extracted by using a stan- dard volume of organic solvent such as alcohol or acetone. Alternatively the chloro- phyll can be extracted using a super critical fluid, usually carbon dioxide. The intensity of colour in the extract is measured by colourimetry or absorptiometry (absorption of radiation) to determine the concentration of pigment, and the results are expressed as chlorophyll concentration or arbitrary units of plant pigment (UPP). Direct counts The number of phytoplankton cells in a measured volume of seawater can be counted directly. Because nets are not fine enough to filter the smallest phytoplankton, a  Organic production and cycling in the ocean 165 sample is usually obtained by collecting water samples and concentrating the cells by centrifuging or sedimentation. Counts can be made on subsamples using a simple hae- mocytometer, a special microscope slide that holds a known volume of water within counting chambers. More practically, an automatic particle counter, such as an adapted Coulter counter, can be used for counting and recording. This electrical instrument responds to changes in an electrical field as small particles in an electrolyte pass through an aperture. Optical or laser optical plankton counters (Herman et al., 2004) are more often used today. When the number of plant cells in unit volume of water has been determined, the weight of plant protoplasm must be calculated. For this it is necessary to know the size and weight of the plant cells, and to make due allowance for the inorganic content of the cells. See also Section 4.6.3. Zooplankton counts To estimate the rate of loss of plant cells due to grazing by animals, quantitative zoo- plankton samples are needed to determine the number of herbivores present. It is also necessary to measure their feeding rates. If the size of the animal population and its food requirements are known, it is possible also to make a calculation of the primary produc- tion necessary to support this number of animals. Feeding rates of zooplankton can be calculated from measurement of clearance rate of particles or ammonium excretion rates. Carbohydrate estimations It has been shown that the tissues of most zooplankton contain little carbohydrate and the carbohydrate content of material filtered from seawater derives almost entirely from the phytoplankton present. Whilst rarely used today, measurements of carbohy- drate can therefore provide a means of estimating the amount of phytoplankton mate- rial in a sample (Marshall and Orr, 1962). Carbohydrate can be measured by colourimetric determination from measurements of the intensity of brown colouration developed by the action of phenol and concentrated sulphuric acid, or by using anthrone (a tricyclic aromatic ketone). 3.2.2 Adenosine triphosphate measurement A source of inaccuracy in many methods of estimating biomass is the difficulty of dis- tinguishing living from nonliving tissue. In samples containing appreciable amounts of nonliving organic matter there are possibilities of greater accuracy from biomass esti- mates based on measurements of the ATP content, as this is a constituent of all live protoplasm, but is virtually absent from dead cells. The technique measures the amount of light emitted when ATP is added to an appropriate preparation of luciferin and luciferase. Calibrated against known amounts of ATP, the method can measure very small amounts of ATP if photo-multiplier tubes are used. For plankton studies raw samples of seawater are filtered to collect particulate matter, which is then treated 166 Elements of Marine Ecology chemically to extract ATP. This extract can be stored deep-frozen for several months without loss of activity prior to measurement. 3.2.3 Measurement of nutrient uptake Where production is seasonal, estimates of production can be based on measurements of the decrease of nutrients in the water during the growing period. In temperate areas, concentrations of nitrate and phosphate in the surface layers reach a maximum during the winter months when photosynthesis is minimal and convectional mixing is occurring. The concentrations fall during the spring and summer due to the absorption of these nutrients by the phytoplankton. The nitrogen or phosphorus content of the phytoplankton being known, measurements of the reduction of nitrate and phosphate in the water, enable estimates to be made of the quantity of new plant tissue formed. Allowances are necessary for the regeneration of nutrients within the photosynthetic zone by decomposition of tissues, replenishment from deeper water and utilization of other sources of nitrogen, for example nitrite, ammonium or organic nitrogen. Production estimates can also be based on measurements of change of oxygen, carbon dioxide or silicate content of the water. 3.2.4 Measurement of photosynthesis in the laboratory Measurement of the degree of carbon or oxygen flux (movement between systems) in a given unit of time gives an estimate of primary production, provided it can be related to the biomass of the primary producers. In photosynthesis, carbohydrate is formed according to the equation nCO2 þ nH2 O-½H2 COn þ nO2 The rate of photosynthesis may be determined by measuring either the evolution of oxygen or the absorption of carbon dioxide. These are not exactly equal because proteins and fats are also formed, but allowance can be made for this. Oxygen determination There are various methods for measuring oxygen in water samples, but the well- known Winkler chemical titration method remains reliable and accurate. The oxygen produced by photosynthesis and consumed by respiration of phytoplankton, can be measured to give a net production figure. This is not quite as simple as it sounds, because the oxygen measurements must be converted into carbon production and loss. Samples of seawater with their natural plankton populations (including zooplank- ton, as trying to separate these from phytoplankton would damage the latter), are col- lected from several depths within the photosynthetic zone and their oxygen contents measured. Pairs of bottles are then filled from each sample and sealed. The bottles are  Organic production and cycling in the ocean 167 identical except that one of each pair is clear, allowing photosynthesis and respiration, whilst the other is dark so only respiration can take place. The pairs of bottles are next suspended in the sea at the series of depths from which their contents were obtained and left for a measured period. Alternatively, if temperature and illumination at the sampling depths are known, the bottles can be immersed in tanks at corresponding temperatures and provided with artificial illumina- tion at the correct intensity. This is advantageous at sea because the vessel does not need to remain hove-to at each station for the duration of the experiment. With bot- tles in tanks, it is necessary to keep them in sufficient motion to prevent settlement of the plant cells. Whichever method is used, the amount of oxygen in each bottle is measured again after the set time interval. The reduction in oxygen in the dark bottles with respect to the original measurements is due to the respiration of the plant, animal and bacterial cells contained. On the assumption that respiration is not influenced by light, the difference in oxygen content between the light and dark bottles of each pair is regarded as being due to the production of oxygen by photosynthesis. This assump- tion is probably not wholly justified, but the method has been widely used and can give tolerably consistent results. One complication which applies to all experiments in which seawater is enclosed in bottles is the rapidity of bacterial growth in these condi- tions and this may vary with the intensity of illumination. Measurement of carbon dioxide uptake: the 14C method Originally developed in the 1950s by Steemann Nielsen, this remains a standard tech- nique for measuring primary production and can be used both for phytoplankton and macroalgae. This is a method of measuring carbon fixation by using the radioactive isotope of carbon, carbon-14 (14C), as a tracer. The experimental technique is similar to the oxygen determination method described above. Samples of seawater are col- lected from a series of depths and the carbon dioxide content in each is measured. Bottles are filled from these samples and a small, measured quantity of bicarbonate containing 14C (NaH14CO3) is added to each. The bottles are then sealed and sus- pended in the sea at appropriate depths for a measured period or incubated in tanks as described above. When the bottles are hauled in or removed from the tanks, the water is filtered to collect the phytoplankton. The cells are washed and their 14C-content estimated by measurement of the beta-radiation. The total carbon fixation is calculated from the known amounts of 14CO2 and total CO2 originally present in the water, making due allowances for the slight differences in rates of assimilation of 14CO2 and 12CO2. There are several problems in interpreting the results of these measurements associated largely with the difficulties of allowing for losses of the organic products of photosynthesis in solution. This method measures the amount of 14CO2 in the material filtered from the water. However, there is evidence that some of the material formed by primary 168 Elements of Marine Ecology production may pass rapidly into the water in soluble form (see Section 3.1.2) and so would not be measured. The 14C method gives results of the same order as are obtained by oxygen determination and is generally thought to give the most accurate measurements of net primary production in particulate form. However whether the production is truly net or not is uncertain. An advantage over oxygen determination is that measurements refer purely to the phytoplankton as zooplankton does not assimilate the radioisotope. Another source of inaccuracy inherent in all methods of estimating production for the complete photosynthetic zone from discrete water samples is the extremely patchy distribution of phytoplankton which occurs in some conditions (see Section 3.3.4). At times the phytoplankton is concentrated in narrow lines or layers at particular depths, which may easily be missed in taking water samples. 3.3 Factors regulating organic production 3.3.1 Photosynthetic pigments, light and compensation depth As described in Section 3.1, photosynthesis is the process whereby the energy of solar radiation becomes fixed as chemical energy in organic compounds. The ability of plants to absorb and utilize light in photochemical reactions is due to their possession of the green pigment chlorophyll and certain other accessory photosyn- thetic pigments. These are contained in organelles known as chloroplasts, except in cyano- bacteria and other photosynthetic bacteria, where they are diffused in the protoplasm. Chlorophyll occurs in several forms, but only chlorophyll a is common to all photosyn- thetic organisms. Diatoms and dinoflagellates (Sections 4.2.1 and 4.2.2) also contain acces- sory pigments including chlorophyll c and various xanthophyll and carotenoid pigments, which give a golden to brownish appearance to their chloroplasts. The red and brown colours of many seaweeds are also due to accessory pigments and seaweed depth distribu- tions are related to the possession of these pigments. Chlorophyll a is essential for conversion of light energy to chemical energy. This pig- ment is green in colour because it absorbs light in the blue and red parts of the spectrum. The possession of accessory red and yellowish pigments is important in extending the range of wavelengths which can be absorbed and the energy subsequently transferred to chlorophyll a. Different wavelengths of light are absorbed differentially with depth (Section 2.6). Red light is absorbed rapidly by water and consequently long wavelengths at the red end of the spectrum can only be utilized by seaweeds, seagrasses and phyto- plankton in shallow water. Absorption of radiant energy by chlorophyll a is therefore mainly limited to the shorter, blue end of the spectrum (Table 3.1). Compensation depth Photosynthesis is confined to the illuminated surface (epipelagic) zone of the ocean and a useful measure of the extent of this productive layer is the compensation depth. This  Organic production and cycling in the ocean 169 Table 3.1 Range of significant light absorption of chlorophyll a and accessory pigments, used by marine algae (seaweeds and microalgae/phytoplankton). Pigment Light spectrum colour(s) Wavelengths (nm) region Chlorophyll a blue and red 430 and 680 maximal absorptions Chlorophyll b green 400 to 520 Carotenoids b-carotene, green 400 to 520 fucoxanthin Phycoerythrin green 490 to 570 Phycocyanin Green-yellow 550 to 630 Allophycocyanins Orange-red 650 to 670 is defined as the depth at which the rate of production of organic material by photosyn- thesis exactly balances the rate of breakdown of organic material by phytoplankton res- piration, that is, the point at which net photosynthesis becomes zero. The compensation depth obviously varies continually with changes of illumination and must be defined with respect to time and place. In clear water in the tropics, the noon compensation depth may be well below 100 m throughout the year. In high latitudes in summer, the noon compensation depth commonly lies somewhere between 10 and 60 m, reducing to zero during the winter months when virtually no production occurs. Photosynthesis varies in proportion to the light intensity up to a limit at which plants become light-saturated and further increase of illumination produces no further increase of photosynthesis. Exposure to strong light is harmful and depresses photosyn- thesis (photoinhibition), the violet and ultraviolet end of the spectrum having the most unfavourable effects. In bright daylight the illumination at the sea surface seems often to be at or above the saturation level for most of the phytoplankton and mea- surements of photosynthesis in these conditions show that maximum production occurs some distance below the surface, usually somewhere between 5 and 20 m depending upon light intensity and falls off sharply above this level (Fig. 3.7). Correspondingly, the maximum quantity of phytoplankton is seldom found very close to the surface, and except for a few species that seem to thrive in the uppermost few centimetres, the greater part of the phytoplankton can be regarded as ‘shade plants’. By absorbing light the plants themselves reduce light penetration through the water and as the population increases the compensation depth tends to decrease. However phytoplankton is at the mercy of water movements from waves and cur- rents and can be carried down to whatever maximum depth the water is being mixed. This might be the whole water column or to where it becomes stratified and may well be below the compensation depth. Phytoplankton carried below the compensa- tion depth will not contribute to photosynthetic gains, but will continue to respire. So 170 Elements of Marine Ecology Arbitary units of gross primary production or respiration 1 2 3 4 10 Respiration 20 is h es nt sy Depth (m) 30 o to Ph 40 Compensation depth 50 1 2 3 60 Net primary production Figure 3.7 Generalized diagram relating primary production rate to depth in the middle latitudes during bright sunshine. Below the compensation depth there is no net production. phytoplankton production gains and respiration losses are best looked at in terms of the whole water column down to the bottom depth of the mixed layers. The depth at which the whole column daily (24 hours) photosynthetic (carbon) gains are equal to the losses through respiration is termed the critical depth. The distance between com- pensation depth and critical depth depends upon the proportions of the phytoplankton stock above and below the compensation depth. This is determined mainly by vertical water movements. For the standing stock of phytoplankton to increase, its total photosynthesis must exceed its total respiration. This is possible in a stratified water column when the depth of surface wind-mixing is limited by a thermocline and there is very little transport of phytoplankton below the compensation depth. Around the British Isles these are the conditions of spring and summer when the water column is stabilized by thermal strat- ification. There is then an overall gain of organic material within the water column and the critical depth must lie below the sea-bed. But in autumn, once vertical mixing begins to distribute much of the phytoplankton to levels well below the compensation depth, a stage is soon reached where total losses by respiration of photosynthetic  Organic production and cycling in the ocean 171 Arbitary scales of phytoplankton biomass, Arbitary scales of phytoplankton biomass, Temperature (°C) respiration and gross primary production (GPP) Temperature (°C) respiration and gross primary production (GPP) 5 10 15 1 2 3 5 10 15 1 2 3 GP Water mixing P P Compensation depth above GP thermocline Critical depth Discontinuity layer 20 20 Compensation depth 40 40 thermocline ass Mixing througout water column Phytoplankton biomass Phytoplankton biom 60 60 below Temperature 80 80 mixing 100 100 Temperature Water Respiration Respiration 120 120 Depth (m) Depth (m) (A) (B) Figure 3.8 Generalized diagram to illustrate changes in depth distribution of phytoplankton, com- pensation depth and critical depth between (A) late summer and (B) late autumn, in middle lati- tudes. With onset of winter, further decline of illumination causes the compensation and critical depths to ascend further until extinguished at the surface. The biomass of phytoplankton decreases rapidly. organisms are greater than total gains by photosynthesis, the critical depth rises and the standing stock is sharply reduced (Fig. 3.8). In middle and high latitudes, survival of phytoplankton over the winter, when little light energy is available, is effected in several ways. During productive periods the plants build up food reserves, notably as oil droplets, on which they can draw when there is insufficient light for net production. Some species develop resting spores which pass unfavourable periods in a state of dormancy, germinating when conditions become propitious. The dissolved organic matter in seawater provides an energy source which some phytoplankton can utilize if light is inadequate for their needs. 3.3.2 Temperature The rate of photosynthesis increases with rising temperature up to a maximum, but then diminishes sharply with further rise of temperature. Different species are suited to different ranges of temperature and photosynthesis is probably performed as efficiently 172 Elements of Marine Ecology in cold water by the phytoplankton of high latitudes as it is in warmer water by the phytoplankton native to the tropics. Seasonal variations of production rate in temperate latitudes are related to changes of both temperature and illumination. Apart from its direct effect on rate of photosyn- thesis, temperature also influences production indirectly through its effects on move- ment and mixing of the water and hence on the supply of nutrients to the euphotic levels. 3.3.3 Nutrients In addition to dissolved carbon dioxide, which is present in seawater in ample quanti- ties to support the most prolific naturally occurring phytoplankton, seaweed and marine plant growth, there are other substances, the nutrients, which photosynthetic organisms also extract from the water and which are essential for their growth. Many of these are minor constituents of seawater, present only in very low concentration, but their supply exerts a dominant control over production. Nitrate and phosphate are the most important (see Section 2.2.2). Where the quantities of these ions are known, theoretical estimates of the potential productivity of the water generally accord well with observed values. Iron, manganese, zinc and copper are other essential nutrients, silicon is required by diatoms, and molybdenum and cobalt and probably other ele- ments are necessary for some photosynthetic organisms. Organic compounds dissolved in the water (DOM) may be important in some cases (see Section 2.2.2). The absorption of nutrients by the phytoplankton reduces the concentration of these substances in the surface layers and this limits the extent to which the population can increase. A certain amount of the nutrients absorbed by phytoplankton may be regenerated and recycled within the euphotic zone, but over deep water, phytoplank- ton are continually being lost from the surface layers through sinking and by con- sumption by zooplankton, which moves to deeper levels during the daytime. Many of the nutrients absorbed from the surface layers are therefore regenerated in the deeper and darker layers of water where phytoplankton cannot grow. Consequently, nutrients accumulate at deep levels due to the continuous transfer of material from the surface. This loss of nutrients from the productive layer of the sea to deep levels, contrasts with the nutrient cycle of the land surface. In soil the breakdown of organic com- pounds releases nutrients where they are quickly available for reabsorption by plant roots, thereby maintaining the fertility of the land. In the sea the continuance of pri- mary producers growth depends to a great extent upon the rate at which nutrients are restored to the euphotic zone by mixing with the nutrient-rich water from below. The lower overall productivity of the sea compared with the land is largely a conse- quence of the regeneration of nutrients in the sea far below the photic zone, with recycling dependent upon relatively slow processes of water movement. The greater  Organic production and cycling in the ocean 173 productivity of coastal areas compared with deep water is partly a consequence of more rapid recycling of nutrients where the sea bottom is closer to the productive layer. Upwelling and turbulence The vertical mixing processes that bring nutrients back up into the photic zone and so restore fertility to the surface layer of the ocean, are described as upwelling and turbu- lence. The way in which upwelling arises from the meeting or deflection of deep cur- rents, has already been described in Section 2.7.4. Turbulence is a term loosely applied to various complex and irregular movements of the water in which different layers become mixed by vertical eddies. It commonly arises from convection currents, tidal currents, thermal front mixing and possibly from internal waves (Section 2.10.3). Whatever the causes of nutrient replenishment, the result is high concentrations of phytoplankton and zooplankton, which in turn provide a concentrated food source for small pelagic fish. These draw in larger predators including fish, cetaceans and sea- birds. Large aggregations of seabirds wheeling and plunging into the sea are often a good indication of an area of concentrated upwelling (Fig. 3.9). In the Southern Ocean, continuous upwelling ensures that, even during the highly productive period of the Antarctic summer, primary productivity is rarely 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 Figure 3.9 Shoals of small fish feeding on rich plankton in areas of upwelling, attract seabirds, cetaceans and predatory fish, resulting in a ‘feeding frenzy’. In the early days of ocean exploration, sailors used such sights as clues to navigation. From Shutterstock Erin Donalson. 174 Elements of Marine Ecology reduced. Upwelling does not only affect pelagic ecosystems. Boundary upwelling along coastlines can influence intertidal rocky shore communities. The Benguela, California and Peru (Humboldt) currents all bring about major upwelling along the coastlines of SW Africa, California and west Africa respectively (Blanchette et al., 2009). All the major upwelling ecosystems of the world are described in detail in Kampf and Chapman (2016). The effects of turbulence on production depend upon the circumstances. It may promote production by bringing nutrients to the surface, or it may sometimes reduce production by carrying down a considerable part of the phytoplankton population below the compensation depth. Broadly, high production is likely to follow a limited period of turbulence once the water column becomes sufficiently stabilized for the phy- toplankton to flourish in the replenished surface layer, without undue loss by downward water movements. In temperate latitudes these conditions occur at the end of winter. Frontal mixing: Thermal fronts are zones where water masses of different tempera- ture meet, which results in turbulence. Such fronts can show up as swirls and wave disturbances in the water or even mist above it. In temperate areas, during the summer months, blooms of phytoplankton are often associated with such boundary mixing zones. For example at the southern end of the Irish Sea cool, tidally mixed water meets warm, stratified water from the Celtic Sea. Other fronts around the British Isles occur mainly at the western end of the English Channel and across the central North Sea (Pingree et al., 1979). These thermal fronts move irregularly under the influence of tides and wind, mixing the water in complex ways, sometimes characterized by extensive cyclonic eddies which persist for several days. In such transitional areas, strat- ified and unstratified water are closely intermingled in changing, unstable relationships. Over deep water these conditions can favour rapid phytoplankton growth by combin- ing sufficient stratification to prevent excessive loss of phytoplankton below the com- pensation depth, while at the same time effecting sufficient vertical mixing to supply ample nutrients. Convection currents: Turbulent water movements commonly arise from convection currents. When surface water cools, its density increases and convectional mixing com- mences once the density of the surface layers begins to exceed that of underlying water, the surface water sinking and being replaced by less dense water from below. In high latitudes, convectional mixing is virtually continuous because heat is continu- ally being lost from the surface. In temperate latitudes, convectional mixing occurs during the winter months to depths of some 75200 m, but ceases during the sum- mer. The corresponding seasonal changes in production are discussed in Section 3.4. In low latitudes where the surface waters remain warm throughout the year there is little if any convectional mixing and the concentration of nutrients at the surface is generally low, unless vertical mixing is occurring from some other cause, such as wind action on the surface causing upwelling.  Organic production and cycling in the ocean 175 Tidal currents: Turbulent vertical eddies may arise where adjacent layers of water are moving at different speeds, or where currents flow over irregularities on the sea-bed. On the continental shelf, especially where the bottom is uneven, strong tidal currents may cause severe turbulence and keep the water well mixed throughout its depth. Tidal flow in the eastern part of the English Channel and the southern part of the North Sea produces sufficient turbulence to mix almost the full depth of water, pre- venting the development of seasonal thermoclines and helping to maintain the fertility of the area throughout the summer months. Internal waves: A water movement phenomenon known as internal waves (see Section 2.10.3) may also contribute to turbulent vertical mixing and thus nutrient replenishment under certain circumstances. Internal waves might cause vertical mixing where they impinge upon the continental slope, their motion here becoming trans- lated in a manner comparable with that of waves breaking on the shore, carrying deep water up the continental slope, much as surface waves run up a sloping beach. In this way, oceanic deep layers rich in nutrients may sometimes spill over the continental edge, mixing with and increasing the fertility of shelf water. Animal vectors of nutrients As described above, nutrients are cycled between surface and deep waters by vertical water movements created through various means. However on a much smaller, but nevertheless important scale, nutrients can be brought up from the depths by animal vectors. Sperm Whales (Physeter macrocephalus) hunt and feed on large squid that live at bathypelagic depths. However they often defaecate when resting or breathing at the sur- face. Although very difficult to ascertain, the same may be true of other deep-diving cetaceans and other marine mammals. Southern Elephant Seals (Mirounga leonina) can dive to at least 2000 m in search of food and might also release nutrients at the surface in the form of faeces. The death of marine mammals out at sea over deep water, results in the movement of nutrients in the opposite direction, since their bodies will eventually sink down to the seabed and be broken down and consumed. 3.3.4 Grazing rates Although the interactions between plant and animal populations are difficult to eluci- date, the grazing rate of the herbivorous zooplankton is certainly one of the factors which regulates the size of the standing stock of phytoplankton and therefore influences the production rate. The quantity of epipelagic zooplankton generally correlates more closely with the quantity of nutrients in the surface layer than with the size of stock of phytoplankton, indicating how greatly grazing reduces phytoplankton numbers in fertile water. In the long term, the primary productivity of an area must determine the size of the animal population it supports, but in the short term there are often wide, and some- times rapid, changes in both numbers and composition of populations, due to a variety 176 Elements of Marine Ecology of causes. Interactions between species often involve a time lag and there is consequently a tendency for numbers to fluctuate about mean levels. Although some natural popula- tions show homoeostatic mechanisms which control reproduction within limits which do not exhaust the food resources of their environment, there is obviously a general trend for animal numbers to increase as long as there is sufficient food, until consump- tion diminishes the food supply. Food shortage may then cause a decline in the feeding population, and eventually the reduction in food consumption may allow the food sup- ply again to increase and these oscillations may involve many links of the food web. If the inorganic environment were to remain uniform, then the system might in due course settle to a steady state, but in nature the physical conditions fluctuate and the equilibrium is forever being disturbed. A dominant cause of short-term fluctuations in the plankton of middle and high latitudes is seasonal variation of climate which influences both the production rate and the sequence of species which predominate. These changes are discussed later (see Section 3.4), but in the present connection it should be noted that the sharp reduction in numbers of diatoms which follows their period of rapid multiplication in the spring, occurs before nitrate and phosphate are fully exhausted, but coincides with the growth in quantity of zooplankton. There can be little doubt that the increasing rate of graz- ing is one cause of the decline of the standing stock of diatoms. 3.3.5 Patchiness of plankton A striking and salient feature of the distribution of marine plankton is its unevenness, with localized patches in nearby areas differing in both quantity and composition. This was evident even to plankton researchers as far back as the 1930s, who noticed that plankton tows in closely adjacent sites at the same depth, produced significant differ- ences in species and quantity. The scale of this patchiness varies from tens of kilo- metres to millimetres and smaller. Even the uneven distribution of primary productivity around entire ocean basins could be considered patchiness (see Fig. 3.12). Experimental studies and statistical analysis of plankton counts in the 1960s confirmed that phytoplankton patchiness was a real phenomenon on a scale from a metre or so to many hundreds of metres. Patchiness results from of a variety of factors, but the exact causes are extremely difficult to elucidate and separate. Physical, chemical and biological factors are all certainly involved. Physical movements of the water, especially turbulence resulting from water temperature differences, can move and concentrate plankton. Biological factors include the ability of zooplankton (and some phytoplank- ton) to move from one place to another, albeit on a small scale and so find and influ- ence phytoplankton patches. Phytoplankton itself can also ‘move’ by growing. If nutrient and light conditions are right, then some species can divide rapidly and form ‘blooms’, expanding the original ‘patch’ into new areas.  Organic production and cycling in the ocean 177 The effects of some water movements, leading to overall patchiness of plankton, can be seen fairly easily. Positively buoyant organisms will tend to become aggregated along lines of convergence, or in the centre of swirls, while negatively buoyant forms can be brought together in upwelling zones beneath divergences. Upward-swimming organisms may form patches above the course of cascade currents (see Section 3.5.3). Wind action sometimes sets the uppermost few metres of water in lines of spiral motion, forming so-called Langmuir vortices, with zones of convergence and diver- gence between adjacent vortices. This pattern of water movement must cause quite localized patches of organisms, which differ in buoyancy or speed and direction of swimming. Any localized turbulence or vertical mixing which affects temperature, salinity or fertility must obviously influence distribution, and may sometimes result in small-scale blooms of phytoplankton. One aspect of plankton patchiness that has often been reported, is the inverse relation- ship of quantities of phytoplankton and zooplankton. Where phytoplankton is especially plentiful, herbivorous zooplankton are sometimes few in number and where herbivores abound, the phytoplankton may be sparse. This appearance of an inverse relationship may be due simply to the different reproductive rates of phytoplankton and zooplankton and the effects of grazing on the size of the standing stock. In favourable conditions phyto- plankton can multiply rapidly and produce a dense stock. Zooplankton populations increase more slowly, but as the number of herbivores rises, the phytoplankton will be increasingly grazed and the stock correspondingly diminished. It may therefore be impossi- ble for any abundance of phytoplankton and zooplankton to coexist for any length of time in natural conditions, because of the rapidity with which phytoplankton can be removed from the water by herbivorous animals. In the 1950s another explanation for an inverse phytoplanktonzooplankton rela- tionship was put forward which involved the concept of ‘animal exclusion’. According to this hypothesis, animals avoid water rich in phytoplankton because the plants have some effect on the quality of the water which animals find unpleasant, perhaps due to secretion of external metabolites by the plants. Small zooplankton could avoid this water by controlling their depth so as to remain at deeper levels until the relative movement of the different layers of water carries them to areas where the surface water is less objectionable. Pelagic fish are also known to avoid water containing cer- tain phytoplankton species, such as Phaeocystis (see Section 4.2.3). This species forms blooms during its colonial gelatinous phase and this can make can make the water slimy and unpleasant. Bainbridge (1953) devised ingenious laboratory experiments enabling observations of zooplankton behaviour in the presence of various concentrations and species of phytoplankton. However he concluded ultimately that ‘exclusion’ is of quite restricted occurrence in natural conditions, although it may operate during intense blooms of some toxic dinoflagellates. It seems that, unsurprisingly and in general, natural 178 Elements of Marine Ecology concentrations of diatoms and other phytoplankton, are likely to be attractive to graz- ing zooplankton. The patchiness of plankton is still a highly topical subject and is of great importance to understanding the dynamics of planktonic food webs. In addition to the physical environment, grazing by zooplankton certainly affects the patchiness of phytoplankton. Differences in multiplication rates of phytoplankton and zooplankton may have seesaw effects on the relative abundance of grazers and their food. Differences in the behaviour of species making vertical migrations, results in different organisms concentrating at various levels at various times (see Section 2.6.3). Attractive or repellent effects of one species on another, influencing direction of movement or the extent of vertical migrations, may cause the appearance or disappearance of certain species in particular places. Swarming behaviour, mainly associated with breeding, may account for localized patches of adults and subsequently of eggs and larvae. The distribution of meroplankton must obviously reflect any patchiness of distribution of the benthos, which relates to differences in the nature of the sea bottom. Whatever its various causes, there is no doubt that the tendency of plankton to occur in patches rather than an even distribution, has important implications with regard to feeding. Animals feed more economically where food is abundant than where it is scarce. By concentrating in and around patches of best food supply, they have the double advantage of efficient feeding, while allowing the recovery of depleted food stocks in other areas. If food were more evenly distributed, its concen- tration might sometimes be below the starvation threshold. 3.4 Ocean seasons Seasonal variations in temperature, illumination and availability of nutrients in the sur- face layers of the ocean impose a pronounced seasonal cycle in production and com- position of the plankton between winter and summer, particularly in temperate latitudes (Fig. 3.10). Both geographical and year-to-year patterns of fluctuation have their origins within the dynamics of the seasonal cycle. For example, continuous plankton recorder studies have shown that the copepod Centropages hamatus in the North Sea is most abundant in the south and in coastal areas and the seasonal cycle in the west is about a month later than in the south and east. This pattern can be related to hydrographic features (Colebrook et al., 1991). 3.4.1 Seasonal features of middle latitudes In middle latitudes (temperate and cold temperate) the four seasons of winter, spring, summer and autumn, so familiar on land, are also evident in the ocean.  Organic production and cycling in the ocean 179 Winter Spring Summer Autumn Winter (A) Solar radiation at sea surface Temperature of surface water Temperature of water at 70 m Convectional Seasonal Convectional mixing thermocline mixing (B) Concentration of inorganic nutrients in photosynthetic zone Concentration of DOM in surface layers Standing stock of (C) diatoms Standing stock of dinoflagellates Standing stock of zooplankton Winter Spring Summer Autumn Winter Figure 3.10 Diagram illustrating seasonal changes of (A) temperature, (B) nutrients and (C) phyto- plankton and zooplankton in the surface layers of temperate seas. Winter During winter the surface of the sea loses heat to the atmosphere and consequently the surface water becomes progressively colder as the season advances. Convectional and wind mixing extends deep into the water column, bringing nitrates, phosphates and other inorganic nutrients to the surface. By late winter the surface water reaches its annual minimum temperature and its annual maximum of inorganic nutrients. Short day-length and the low angle of the sun results in poor or absent illumination 180 Elements of Marine Ecology within the water. The quantities of both phytoplankton and zooplankton are minimal, except at the end of winter when many animals start their spawning, thus timing their reproductive period so that their larvae have the advantage of the rapidly increasing food supplies that are shortly to follow in spring. In neritic (shallow coastal) areas from late autumn through to the end of winter the water column is often virtually fully mixed throughout its entire depth, surface and bottom temperatures being almost the same. Beyond the continental edge, convectional mixing in winter usually extends to between 100 and 200 m, depending on the temperature of the deeper levels. Spring In spring, increasing insolation (solar radiation) causes the surface water temperature to rise, the water column gradually becomes stabilized by thermal stratification, illumina- tion increases and the critical depth becomes lower than the zone of wind mixing. The concentration of nutrients in the surface layer is initially high, but begins to decrease sharply due to rapid absorption by the phytoplankton, which now begins to multiply very quickly in this favourable combination of temperature, light, nutrient supply and stable water column. The rate of primary production soon becomes very high and there is an enormous increase in the quantity of phytoplankton, especially diatoms, which soon reach their greatest abundance for the year (the spring diatom peak). The zooplankton undergoes a more gradual increase, but during late winter and early spring it becomes augmented by the spawning of innumerable marine ani- mals, contributing great numbers of eggs and larvae, which by late spring have devel- oped to more advanced larval or juvenile stages. As the zooplankton increases in amount, the quantity of phytoplankton declines rapidly. Summer During summer the surface water is (relatively) warm and well illuminated. The con- centration of inorganic nutrients at the surface is now low because they have been taken up by the phytoplankton. There is little replenishment from deeper water, because vertical mixing is restricted by a sharp thermocline. Dinoflagellates are at their highest numbers, but the phytoplankton as a whole has declined in amount and pri- mary production is reduced due to grazing by zooplankton and shortage of inorganic nutrients. Diatoms are often quite scarce at this time. During midsummer the numbers and production of phytoplankton are often greatest within the discontinuity layer, usually at some 1520 m, where nutrients are to some extent available from the dee- per mixed layers. The zooplankton, mainly holoplankton, now reaches its greatest amount for the year, and after that diminishes. The concentration of DOM (Section 2.2.2) is usually highest during the summer.  Organic production and cycling in the ocean 181 Autumn During this season the surface water cools and illumination declines. The deeper layers are still getting slightly warmer, until eventually the thermocline breaks and convec- tional mixing is re-established. This leads to rapid replenishment of nutrients in the surface layer and a consequent increase in primary production, both diatoms and dino- flagellates becoming more numerous. This autumn increase of phytoplankton is always smaller than the spring peak. It is often followed by a slight increase in zooplankton, but these increases are short-lived. Vertical mixing disperses much of the phytoplank- ton below the critical depth and the size of stock falls quickly. As temperature and illumination decrease further, the quantities of both phytoplankton and zooplankton gradually reduce to their winter levels, and their overwintering stages appear. 3.4.2 Ocean seasons in high and low latitudes The sequence of four ocean seasons described above is a feature of middle latitudes where the temperature of the surface water undergoes the greatest seasonal change. In high latitudes the surface water temperature does not vary much with season. Here, within the Arctic Ocean and Southern Ocean, illumination is the dominant factor reg- ulating productivity. Although there may be a short transitional spring and autumn, only two main ocean seasons are apparent, a long winter period of poor or absent illu- mination and virtually no primary production, followed by a shorter summer period of very high production when the light becomes sufficiently good to enable the phy- toplankton to grow. The summer productive period lasts only a few weeks, but during part of this time daylight may be continuous throughout the 24-hour period, the length of daylight depending on latitude. This makes possible a very rapid growth of a large quantity of phytoplankton and this abundance of food allows a great increase in zooplankton. Because the rich food supply lasts only a short time, the developmental stages of zooplankton at high latitudes must be passed through rapidly. After that, illu- mination declines and primary production eventually falls to near zero. The phyto- plankton virtually disappears, though some of it overwinters locked within sea ice in various forms such as resistant spores (Box 3.2). When released as the ice melts at the approach to summer, these provide a ‘starter pack’ for phytoplankton blooms. The zooplankton population decreases to a much lower level during winter. Thus there is a single short season of rapid growth, soon followed by decline. In low tropical latitudes, conditions are mostly those of continual summer. The surface water is consistently warm and well illuminated, but there may be some limita- tion of production by shortage of nutrients, there being little vertical mixing across a strongly developed thermocline. However, production continues throughout the year and extends to a greater depth than in high latitudes, and the rate of turnover is proba- bly rapid. The result in some tropical areas is a total annual production some 510 182 Elements of Marine Ecology BOX 3.2 Ice algae. Planktonic phytoplankton is not the only source of primary production in the Arctic and Antarctic. Some algae and cyanobacteria can actually live within the lower layers of sea ice, where it is riddled with ‘brine channels’ and on the irregular, rough underside. Pockets of salty brine become trapped within the ice as it forms but eventually drain away leaving a network of small channels. The algae can be seen as a green or brown coloured bands within and on the bottom of the ice. They provide a larder for zooplankton, including krill and are important primary producers in some areas and at some times (Lisotte, 2001). Arctic ice algae can secrete polysaccharides that may prevent themselves from freezing, as well as maintaining the brine channels in which they live (Krembs et al., 2011). sea ice snow algae sea brine channels ice brinicles magnified area to show brine channels 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. times greater than in temperate seas (Wickstead, 1968). Generally the rate of produc- tion in warm seas remains fairly uniform, but there are parts where seasonal changes of wind, for example the monsoons, cause variations of water circulation and seasonal improvements in nutrient supply, which are quickly followed by periods of increased production. Except for a few areas, seasonal peaks in warm seas seldom exceed a ten- fold increase of production, whereas fluctuations are sometimes as great as fiftyfold in temperate waters. 3.4.3 Seasonal changes in plankton around the British Isles Seasonal changes in phytoplankton and so organic production, are the driver behind seasonal changes further up the planktonic and higher food chain. Many benthic and nektonic  Organic production and cycling in the ocean 183 animals time the release of their planktonic eggs to coincide with the provision of an abun- dant food supply for their subsequent larval stages, provided by the spring bloom of phyto- plankton. In previous editions a detailed account was given of seasonal changes in plankton species and abundance around the British Isles. This was based on published data from plankton sampling, especially the Continuous Plankton Recorder (CPR) survey in the North Atlantic, including the North Sea (see Section 4.6.2). Many papers and data on this subject have been (and are) published in the Journal of the Marine Biological Association UK and the information in previous editions was based on such material from the 1930s through to the 1960s (the first edition of this book was published in 1968). Major changes in phytoplankton and zooplankton populations and communities in the North Atlantic, have taken place over the past few decades to the present (2020s), including changes in sea- sonality. Therefore only some general seasonal features of plankton around the British Isles are described here. Whilst these changes are undoubtedly a result of climate changes, Edwards et al. (2013) estimate that this is about 50:50 between natural climate variability and forced anthropogenic warming. This is discussed further in the section on warming oceans in Chapter 9, Human Impacts 2: Problems, Mitigation and Conservation (Section 9.2.5). The detailed plankton data collected by the CPR over more than 60 years is vital in detecting such changes. Winter (Novem