There are environmental factors other than light, CO2 and temperature that can have a major influence on the total amount of photosynthesis that takes place (i.e. on primary production in the ecosystem) by their effects on the amount of plant biomass present. Since our concern here is mainly with factors that influence photosynthesis directly we shall touch on these indirect factors only briefly.
Inorganic nutrition - particularly the concentrations of the key elements phosphorus and nitrogen - is the most important indirect factor. The average composition of marine phytoplankton is characterized by the Redfield ratio, 106C:16N:1P, originally determined by the marine chemist, Alfred Redfield in the 1930s. If the nutrient concentration is low, then although the existing phytoplankton may be photosynthesizing at a higher rate per unit biomass, they cannot increase their biomass and so the rate of photosynthesis per unit volume or area remains low. When nutrient levels increase, due to agricultural run-off or sewage input in inland waters, or an increase in river outflow in coastal waters caused by increased rainfall, or the commencement of a seasonal upwelling off the west coast of a continental landmass, or a breakdown of stratification in the sea or a lake in the autumn bringing up fresh nutrients from below the thermocline, then the phytoplankton population and therefore total photosynthesis both increase as well. In the sea, rainfall can be a significant, but episodic, source of nitrogen, both in oligotrophic regions of the ocean1027 and in coastal waters.143
When the phytoplankton population has depleted the level of any essential nutrient, then photosynthetic biomass ceases to increase. In the case of nitrogen depletion, however, certain filamentous species of blue-green algae are not prevented from continued growth since they have the ability to fix molecular nitrogen. This ability is present in common bloom-forming genera such as Anabaena and Aphanizomenon in inland water bodies. In the sea, where nitrogen is usually the limiting mineral nutrient, the unicellular cyanobacterium Synechococcus, a major component of the picoplankton throughout the oceans, cannot fix nitrogen,1442 but the large colonial filamentous cyanobacterium, Trichodesmium, which is often the major component of the phytoplankton in tropical ocean waters, does fix nitrogen. Carpenter and Romans (1991) have concluded that in the tropical North Atlantic Ocean Trichodesmium is the most important primary producer, and that its nitrogen fixation contributes about 30 mg of nitrogen per m2 per day, a value exceeding the estimated upward flux of nitrate from below the thermocline.
In ocean waters, as nutrient availability and total phytoplankton biomass increase, so the contribution of the smaller phytoplankton species decreases as the larger phytoplankton come to dominate. The relative importance of picophytoplankton (cells <2 mm) is greatest in warm oligotrophic waters.9 From measurements along a north-south transect (48° N to 8° S) in the central Pacific Ocean, Suzuki et al. (1995) found that the prochlorophyte, Prochlorococcus marinus (0.6-0.8 mm in diameter), although universally present, was most abundant in oceanic environments with higher temperature (15-30°C) and lower nutrient concentrations. The larger surface area to volume ratio of small cells gives them a competitive advantage over large cells where nutrient concentrations are low.
In freshwater lakes, phosphorus is most commonly the limiting mineral nutrient for phytoplankton growth and primary production. Enrichment of inland waters with phosphate from incompletely treated urban wastes, and from fertilizer run-off has, over many decades, led to the phenomenon of eutrophication, the excessive growth of phytoplankton and epiphytes, with a variety of undesirable consequences, such as development of toxic blue-green algal blooms, elimination of desirable macrophytes and anaero-biosis due to breakdown of the excessive organic matter leading to fish kills. For many, but not all, lakes in the developed world, steps have been taken in recent years to reduce external phosphorus loading, and Jeppesen et al. (2005) report an analysis of long-term data from 35 case studies of lakes in Europe and the USA, of the process of re-oligotrophication of these water bodies. The lowering of in-lake phosphorus concentration was accompanied by reductions in chlorophyll a concentration and increased water clarity (Secchi depth). Declines in phytoplankton biomass were accompanied by changes in community structure, chrysophytes and dino-phytes increasing at the expense of cyanobacteria in deep lakes; diatoms, cryptophytes and chrysophytes becoming more dominant in shallow lakes. Macrophyte abundance increased in some, but not all, lakes.
Anthropogenic eutrophication in coastal waters due to excessive input of nutrients is now a world-wide problem,22,500 giving rise to harmful algal blooms, loss of seagrass meadows, overgrowth of coral by algae, depletion of deep-water oxygen with consequent loss of benthic fauna and damage to fisheries. To address the problem of eutrophication, the phenomenon must be clearly defined, and linked with appropriate assessment and monitoring systems. As a definition of eutrophication, Andersen et al. (2006) propose 'the enrichment of water by nutrients, especially nitrogen and/or phosphorus and organic matter, causing an increased growth of algae and higher forms of plant life to produce an unacceptable deviation in structure, function and stability of organisms present in the water and to the quality of the water concerned, compared to reference conditions'. They go on to propose that measurements of primary production, being a sensitive and accurate indicator of eutrophication, should be mandatory when monitoring and assessing the ecological status of coastal waters. Smith (2007) suggests that the most sensitive and reliable primary productivity parameter to use when evaluating the eutrophication status of coastal marine ecosystems is the light-saturated maximum volumetric rate of photosynthesis (mg C m-3 day-1) observed in a standard vertical productivity profile. The volumetric expression of primary productivity appears to track changes in nutrient loading and algal biomass more predictably and sensitively than changes in areal (integrated) primary productivity.
For the diatoms, with their external skeleton (frustule) made of silica, silicon is an essential element. Depletion of silica can bring diatom blooms to an end in fresh water.1120 Leblanc et al. (2005) present evidence that the low contribution of diatoms to the spring bloom in the northeast Atlantic is due to the limited availability of silicon. In diatom-dominated ocean ecosystems, silicate is not recycled as quickly as is cellular nitrogen and is thus lost to deep water at a higher rate as diatom cells and diatomaceous faecal pellets sink down through the thermocline.336 Silicon can also be a limiting element for diatom growth in some very productive coastal upwelling systems.1115
The other major environmental factor that limits total phytoplankton photosynthesis by limiting biomass is grazing by the aquatic fauna. The spring bloom of phytoplankton is typically followed by a bloom of zooplankton, which graze upon the phytoplankton cells. It is undoubtedly true that zooplankton grazing can have a major impact on phyto-plankton populations and in some cases can be the cause of the decline in phytoplankton numbers following the bloom: the relations, however, are complex and fluctuations in phytoplankton populations cannot always be interpreted easily in terms of zooplankton grazing. The matter is discussed in more detail for inland waters by Hutchinson (1967) and Reynolds (1984), and for the oceans by Raymont (1980) and Frost (1980). The composition of the phytoplankton population can be affected by selective feeding: the copepod, Calanus finmarchicus, for example, in the Norwegian Sea, was found to graze selectively on certain phytoplank-ton types, such as diatoms, but avoid others, such as cyanobacteria.900 In addition to those zooplankton large enough to be visible to the naked eye, such as the crustaceans (copepods, krill), single-celled protozoa (ciliates, heterotrophic or mixotrophic flagellates) are also an important part of the food chain, and are thought to be the primary grazers, particularly on the prokaryotic members of the phytoplankton, such as Synechococcus. Large colonial phytoplankton forms, such as occur in the Peruvian upwelling, can be grazed directly by herbivorous fish such as the anchovy.1158
Benthic filter-feeding fauna, such as shellfish, in shallow coastal or estuarine waters can also make significant inroads into phytoplankton populations. Asmus and Asmus (1991) found that an intertidal mussel (Mytilus edulis) bed in the German Wadden Sea (eastern North Sea) reduced phytoplankton biomass by about 37% between the incoming and outgoing tide. Parallel with the uptake of phytoplankton there was, however, a substantial release of nitrogen, as ammonium, from the mussel bed, leading these authors to suggest that the shellfish were simultaneously reducing the standing stock of phytoplankton, and promoting phytoplankton primary production, or to put it another way, the mussel bed was accelerating phytoplankton turnover.
Although throughout most of the world's oceans, phytoplankton biomass appears to be limited by the availability of the major nutrients, there are substantial regions - the Southern Ocean, the equatorial Pacific and the northeast Pacific Ocean - where there is a surplus of phosphate and nitrate in the surface waters, but primary productivity is low. These are sometimes referred to as HNLC (high nitrate, low chlorophyll) regions. A number of plausible hypotheses have been put forward to explain the failure of the phytoplankton in these regions to fully utilize the major nutrients. It has been proposed, for example, notably by Martin and coworkers,872 that phytoplankton growth in these waters is limited by iron deficiency. Another proposal, specifically for the equatorial Pacific, is that the standing crop of phytoplankton is controlled by closely coupled zooplankton grazing.270,1434 For the Antarctic Circumpolar Current in the Southern Ocean, Mitchell et al. (1991) argue that as a consequence of the high wind strength, low solar irradiance (persistent clouds) and weak stratification, deep circulation will lead to light limitation of phytoplankton growth to such an extent that they cannot possibly use more than a small fraction of the available nutrients. Another possibility, for the Southern Ocean, is the inhibitory effects of chronic low temperature on nitrate uptake by the phytoplankton.335 Detailed discussions of these and other possible explanations of 'What controls phytoplankton production in nutrient-rich areas of the open sea?' may be found in the special issue of Limnology and Oceanography published under this title and edited by Chisholm and Morel (1991).
Notwithstanding the alternative hypotheses, the theory that a deficiency of iron is the factor primarily responsible for the low productivity of HNLC waters has now received direct experimental support. Martin et al. (1994) (IronEx I) and Coale et al. (1996) (IronEx II) carried out enrichment of substantial patches of ocean (64 and 72 km2, respectively) in the equatorial Pacific, using (Martin et al.) 450 kg Fe, and (Coale et al.) 225 kg (day 1) plus 2 x 112 kg (days 3 and 7), with acidified ferrous sulfate as the iron source. Iron addition triggered a massive phytoplankton bloom, which consumed large quantities of carbon dioxide and nitrate. In the case of IronEx II it was found that during the week following first enrichment there was a dramatic change in the phytoplankton community structure, from one dominated by picoplankton to one dominated by large diatoms.213
Boyd et al. (2000) carried out a similar experiment at a location, 61° S 140° E, in the Pacific sector of the Southern Ocean. Once again, fertilization was followed by a large algal bloom. Initial increases were due to pico-eukaryotes, but after day 6 there was a shift to large diatoms. Gervais et al. (2002) observed several-fold increases in primary productivity and chlorophyll a, following iron fertilization in the Atlantic sector (48° S 21° E) of the Southern Ocean. They concluded that iron supply is the central factor controlling phytoplankton primary productivity in the Southern Ocean, even where the mixing depth is >80 m. Lance et al. (2007) carried out in situ iron-enrichment experiments at two locations along longitude 172° W in the Pacific sector of the Southern Ocean: at 56° S in the Subantarctic Zone, just north of the Subantarctic Front, and at 66° S, just south of the Antarctic Circumpolar Current. In both cases there was a many-fold increase in both chlorophyll and primary productivity. At the northern location there was a population shift from prymnesiophytes towards diatoms, but at the southern site there was no change in the phytoplankton assemblage from its initial composition of ^50% diatoms.
De Baar et al. (2005) have reviewed the findings of eight of these iron-addition experiments, carried out in various locations around the world's oceans. They find that the maximum chlorophyll a, the maximum dissolved inorganic carbon (DIC) removal and the overall DIC/Fe efficiency (moles carbon removed per mole iron added) all scale inversely with the depth of the wind-mixed layer that defines the light environment. Large diatoms always benefit the most from iron addition.
While it is beginning to look as if iron deficiency is the default explanation for the low productivity of HNLC regions of the ocean, other explanations may apply in certain locations. For example, Goericke (2002) presents evidence that in the HNLC areas of the monsoonal Arabian Sea, where iron is present in abundance, phytoplankton biomass is controlled within tight bounds by microzooplankton grazing.
The impact of zooplankton grazing on phytoplankton populations can be greatly affected by the extent to which the zooplankton themselves are subject to predation by larger animals. The addition of planktivorous fish to a pond in Minnesota was found to lead to an order-of-magnitude increase in total phytoplankton biomass.835 In addition to the increased levels of those algal species already present, several new species appeared. In a survey of shallow wetlands in northern Alberta (Canada), which tend to be either in a turbid, pea-green (high phytoplankton chlorophyll) or clear, low chlorophyll, state, Norlin et al. (2005) found that the two categories corresponded to waters with low, or high, submerged aquatic vegetation coverage, respectively. They suggested that high aquatic vegetation coverage provides protection for efficiently grazing cladocerans (crustacean zooplankton, 'water fleas') from the larger invertebrates that prey on them, leading to effective control of the phytoplankton. In a set of shallow lakes in England, Moss et al. (1994) found an inverse correlation between chlorophyll a and cladoceran abundance: they suggested that this was due to the dominance of submerged macrophytes and the refuges they provide for these grazing zooplankton.
A limiting factor for one particular group among the phytoplankton, the dinoflagellates, is small-scale turbulence. It appears that turbulence in the water, at levels such as might result from quite moderate winds, can cause the cells to lose their longitudinal flagellum: cell division and growth are also inhibited.98,1353 In the Sea of Galilee (Lake Kinneret), the absence of the usual winter-spring bloom of the dinoflagellate, Peridinium, in 1996 occurred at a time when the dissipation rates of turbulent kinetic energy were extremely high, while record high amounts of dinoflagellates appeared (1994, 1995) when dissipation rates were very low.100 The inhibitory effect of turbulence is thought to explain why dinoflagellate red tides only develop in calm weather.
As we have previously noted, in addition to their specific effects on dinoflagellates, high winds are normally inhibitory to primary production because they bring about deep mixing of the phytoplankton so that the average light intensity to which the cells are exposed is too low for net production to occur. In one special case, however, the contrary behaviour is observed. The Sargasso Sea (North Atlantic subtropical gyre) is an oligotrophic, highly unproductive, region of the ocean. Babin et al. (2004) used remotely sensed ocean colour data (SeaWiFS) to follow the consequences of the passage of 13 hurricanes through this region in 1998-2001. They observed that in every case there was an increase (5-91%) in surface chlorophyll in the wake of the hurricane. They attributed this to an increased supply of nutrients, mixed in from below, possibly together with entrainment of phytoplankton cells from the deep chlorophyll maximum.
In freshwater bodies, infection of phytoplankton populations by parasitic fungi can, particularly in eutrophic lakes, significantly reduce their numbers, and even terminate blooms. , , In marine waters, pathogenic viruses have been shown to infect a range of phytoplankton types including diatoms, cryptophytes, prasinophytes and cyanobac-teria.1093,1326 Although little quantitative evidence is yet available, preliminary indications are that viral mortality could be another significant factor regulating phytoplankton populations and primary production, in the sea. Cottrell and Suttle (1995) studied the impact of a lytic virus, MpV, on populations of the cosmopolitan and abundant prasinophyte phytoplankton species, Micromonas pusilla, in Texas coastal waters. The abundance of infective MpV was high, and decreased from 1.3 x 105 ml-1 in January 1993 to 2.1 x 103 ml-1 at the end of April. Using a laboratory measurement of the adsorption coefficient for MpV on M. pusilla, they calculated that 2 to 10% (average 4.4%) of the M. pusilla population was lysed per day.
Phytoplankton growth can itself limit primary production by the benthic flora. In eutrophic waters interception of light by dense phytoplankton populations can prevent the growth of benthic macrophytes.663 From their studies on the Norfolk Broads (England), Phillips et al. (1978) consider that during progressive eutrophication of water bodies, overgrowth of the macrophyte leaves by epiphytes and mats of filamentous algae, with consequent reduction in light availability, initiates the macrophyte decline even before dense phytoplankton populations have developed. Overgrowth of leaves by epiphytes has also been implicated in the decline of seagrasses in eutrophicated Cockburn Sound, Western Australia.197 Eutrophication of shallow estuaries can lead to the proliferation of bloom-forming 'nuisance' macroalgae, typically filamentous (such as Cladophora) or sheet-like (such as Ulva) forms, usually chloro-phytes, that can shade, and eventually displace, seagrasses as the dominant benthic autotrophs.882
The density and therefore total photosynthetic rate of the benthic flora is also affected by grazing by invertebrate and vertebrate animals. In the case of macrophytes, snails and other gastropods feed on the photosyn-thetic tissue, as well as on the attached epiphytes, in both fresh and salt waters: in the sea, limpets and sea urchins are important invertebrate grazers, while in fresh waters insect larvae can be significant consumers. Some specialized species of herbivorous fish such as the grass carp (China) in fresh waters, and the parrot fish, which feeds on seagrasses, eat macrophytes. Higher aquatic grazing animals such as sea turtles and dugongs, as well as ducks and geese, also eat macrophytes. In inland waters, grazing by invertebrates, fish and birds is a significant factor limiting biomass and photosynthesis in some macrophyte commu-nities.1456 Protection of Potamogeton filiformis in Loch Leven (Scotland) from grazing by waterfowl substantially increased its biomass throughout the growing season.663 Similar observations have been made for three macrophyte species in Lake Stigsholm, Denmark.1266 Herbivory on freshwater macrophytes has been reviewed by Lodge (1991). In shallow coastal sea waters, grazing by sea urchins can be a major factor limiting the growth of kelps and other seaweeds. Overgrazing in seagrass by sea urchins can cause localized denudation of patches (up to 0.5 km2) of meadow, and is thought, for reasons not yet understood, to be on the increase world-wide.354 Grazing by sea turtles can also have a major impact on seagrass beds.
The biotic relations are complex: whether or not a particular region of the sublittoral zone is colonized by brown algae, and the density at which they grow, are likely to be determined by the abundance of animals such as crabs, lobsters and sea otters (which prey on sea urchins), and the numbers of these animals may in turn be influenced by the activities of man.
The lower limit of Laminaria hyperborea at one site in the Isle of Man (UK) was found to be controlled by the sea urchin Echinus esculentus, which was present at a density of five animals m~2.667 In a study area in Nova Scotia (Canada), Breen and Mann (1976) found that the lobster
Homarus americanus, a major predator of sea urchins, decreased by nearly 50% in 14 years: in the latter six years of this period the sea urchin Strongylocentrotus destroyed 70% of the Laminaria beds. Areas of bare rock protected from sea urchin grazing were rapidly recolonized by Laminaria plants. Similarly, off California, the mass mortality by disease of a localized population of sea urchins on the seaward side of a kelp forest was followed by the rapid seaward expansion of four species of brown algae.1037 On the basis of archaeological evidence from the Aleutian Islands, Simenstad et al. (1978) concluded that when the Aleut people colonized this area and commenced hunting the sea otter, the diminution in otter numbers led to a population explosion of sea urchins, which was in turn followed by the decimation of the abundant kelp beds in the area: since fur hunting in the Aleutians ceased in 1911, both the sea otter and abundant kelp beds have become re-established. In Fiji, extinction of the dugongs and a reduction in sea turtle numbers has caused the seagrasses to increase to the point of becoming a nuisance.894
The chloroplasts of some macroalgae can continue to photosynthesize for a limited time after they have been ingested by certain grazing animals. This is the phenomenon of kleptoplasty.1110,1472 This is distinct from the phenomenon of algal symbiosis, common among the marine biota (e.g. coral, tunicates), where intact algal cells live and photosynthe-size within their animal host. In kleptoplasty, the chloroplasts of the grazed plants are liberated from their cells during ingestion, and survive, and continue to photosynthesize as naked organelles within the cells of the grazer. At the microbial level, kleptoplasty on unicellular phytoplank-ton as the source is carried on by some species of flagellates and ciliates, and also by some dinoflagellates. McManus et al. (2004) found that two tide-pool ciliates, Strombidium oculatum and S. stylifer, are able to ingest ulvaceous green macroalgae (Enteromorpha sp.) and retain their chloro-plasts. Green algae in the Ulvaceae do not have specialized reproductive structures, and simply convert a large proportion of their vegetative tissue to the reproductive state, in which they release massive numbers of flagellated swarmer zoospore cells. McManus et al. observed the ciliates to congregate near the reproductive portion of the Enteromorpha tissue, and suggested that they were ingesting the zoospores as they were shed by the thallus. If given a modest supply of food with which to replenish its chloroplasts, S. stylifer grew rapidly in the light, but did not survive long in darkness.
The only metazoans that can carry out kleptoplasty are the sacoglos-sans (sea slugs). They feed mainly on green algae, such as species of
Caulerpa, and on red algae, such as Griffithsia. The algal chloroplasts are retained by the animal in certain specialized cells, and can remain active, supplying the animal with some of its dietary carbon requirements, for days or weeks. The subject is reviewed by Williams and Walker (1999). By comparing 13C/12C ratios in sacoglossans with those of the algae on which they were feeding, Raven et al. (2001) estimated that up to 60% of the total carbon input to the sacoglossans came from photosynthesis by their kleptoplastids.
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