NUMBER TWENTY NINE - OCTOBER 1998

Mechanisms stabilising plant-dominance are shown in Table 1. These include: luxury consumption, by the plants, of nitrogen compounds which may prevent phytoplankton build-up by nutrient limitation [116,143]; allelopathy, by which the plants may secrete organic algal inhibitors into the water [156,21,61]; and provision of physical refuges (shade, complex structure) from their fish predators for crustacean zooplankton grazers on algae [109, 130,145], particularly water fleas of the genus Daphnia but also other crustaceans. Similar provision may exist for periphyton grazers, such as snails [26,27,28]. Metabolism of the plants, may create conditions within the plant beds (high pH, low oxygen concentrations) which may reduce the efficiency of fish predation on the grazers.

The coarse debris laid down at the end of the growth season by the plants may also stabilise the sediment and provide a favourable rooting medium for regeneration the following spring. The plant bed itself also absorbs wave energy and may minimise wind disturbance of the sediments and consequent turbidity in the water.

Table 1 Mechanisms stabilising the plant-dominated and algal-dominated states (bufer mechanisms)

(a) Mechanisms involving grazers on algae

Fig 11 Typical zooplankters and some size relationships between the zooplankters and the algae on which they may graze. Based on Moss [108]

Some of the water fleas (Cladocera), on the other hand, are easily taken, with their comparatively large size and slow, predictable movement. The Cladocera have some counter-advantages, however, in that they more efficiently filter phytoplankton and other organic particles from the water, compared with the others. They can also reproduce more rapidly than the copepods and hence more easily replace losses to predation.

The impact of fish predation on a zooplankton community that has developed in the previous absence or scarcity of fish is thus to convert a community dominated often by large Cladocera, or sometimes a mixture of Cladocera and copepods to one dominated by rotifers and copepods, with perhaps some of the smaller cladoceran genera. The former community is efficient at grazing and can keep the water clear, the latter community is relatively inefficient and associated algal populations can quickly build up. An example of these relationships at work can be seen if goldfish are introduced in too great a number to aquarium tanks (Fig 12) or featureless garden ponds. Commonly the water goes very green, very quickly.

This simple relationship can, however, be complicated by the provision of refuges which allow the coexistence of the fish and their favoured prey, the larger Cladocera, particularly the genus Daphnia. Plants do this through their structure and the chemical conditions their metabolic activity creates in the water . There are usually small fish present in the plant beds [154]; these find refuge themselves from their own predators, piscivorous fish and birds, but the entangled structure of the beds and deoxygenation of the deeper water often confines them to the fringes and to near the surface. Fish need sufficient light and sufficient striking distance to capture their prey and, for the most part, dense plant beds frustrate these requirements. Some fish, such as perch (Perca fluviatilis) cope better than others like roach (Rutilus rutilus) but experiments [109] have shown that when the density of plants is reduced, perch are more readily able to feed on Daphnia (see Box 2). Recent work [9,80,143,150] suggests that grazer, especially Daphnia, buffers are most important in the early establishment of plants but may become less important than nitrogen limitation once the plant community has fully developed.

Plant photosynthesis changes the chemistry of the water. Carbon dioxide and bicarbonate are withdrawn and through the operation of well-known inorganic carbon equilibria, this increases the pH often to values well above 9, sometimes 10. This appears to inhibit fish feeding [8] and provides a chemical refuge in addition to the deoxygenation deeper in the beds caused by decomposition of organic matter in the darkness of the lower layers.

Plant beds thus allow substantial populations of large cladocerans to find refuge and build up, but this would be immaterial if these animals remained in the beds and did not move out to graze on phytoplankton in the adjacent or overlying water. At night, however, greater numbers of these animals are present outside the beds than during the daytime [98]. It is not certain that they make deliberate movements or whether they simply drift out at all times, in water currents, but are quickly removed by the fish during the day. Zooplankters make upward and downward movements (vertical migration) in deep lakes and this movement is more prominent when zooplanktivorous fish are present than when they are not [41,58,143,150]. The zooplankters are then using the deeper, darker layers of the lake as a refuge from predation. Whether the zooplankters of shallow lakes have the potential for innate horizontal migratory movements [40] is not certain.

The nature of the plants is important in determining how efficient the refuge is. Water lilies appear to be very efficient [109,145] and may support large populations of Daphnia. Finer-leaved plants are less effective [9,98] but this may be because Daphnia themselves do not favour the dense structure that prevails among such plants [97]. Other genera, such as Sida, Simocephalus and Eurycercus, which are strongly associated with plant surfaces may be more important in such beds [80]. Overall density of plants is important; sparse stands are ineffective at providing much refuge [130].

Periphyton algae may pose as great a competitive threat to submerged plants as phytoplankton algae [118,123]. They may form a dense fur over the surfaces and compete for carbon dioxide, light and nutrients. Some plants have coverings of mucilage which deter periphyton colonisation, but most do not. This may be because the mucilage is itself disadvantageous in lengthening the pathways of diffusion of carbon dioxide and nutrients into the plant. Periphyton growths are often controlled by the grazing of macroinvertebrates such as snails, mayfly nymphs and chironomid larvae [25,26,27,39,146].

Where these are abundant, very little periphyton is allowed to build up but these invertebrates are vulnerable to predation by larger fish. Experiments where species such as tench have been stocked, show that a decline in invertebrates is soon followed by an increase in periphyton and a decrease in plant growth (Fig 13). Deoxygenation deep in dense plant beds must deter fish entry, and the main feeders on plant-associated invertebrates are notably those cyprinid (carp family) species that are tolerant of low oxygen concentrations. We have, however, little information on how the invertebrate populations and their fish predators may co-exist in the plant beds to the advantage of the plants and the detriment of the periphyton. One clue may come from the fact that the ratio of piscivorous fish biomass to zooplanktivorous fish biomass tends to be higher in plant-dominated lakes [87] so that annual recruitment to the populations of the latter may be restricted by predation. These populations include the young of plant-invertebrate-eating fish.

One clue may come from the fact that the ratio of piscivorous fish biomass to zooplanktivorous fish biomass tends to be higher in plant-dominated lakes [87] so that annual recruitment to the populations of the latter may be restricted by predation. These populations include the young of plant-invertebrate-eating fish.

Fig 13 Exposure to high tench density of a system of aquatic plants, periphyton and snails led to a reduction in snails, an increase in periphyton and a reduction in plant growth. From Bronmark [27]

Mechanisms involving inhibition of algal growth

Evidence for allelopathy is strong in the laboratory, but lacking in the field [52]. Plants do secrete substances which inhibit growth of laboratory algal cultures and some of the substances have been characterised. However, the extent to which these substances, faced with a barrage of heterotrophic bacteria, may accumulate and be effective in natural waters on a range of many species of algae which may easily substitute for one another, is unknown and will be extremely difficult to investigate. The potential, however, undoubtedly exists.

Other ways in which the plants may change the water chemistry to disfavour algae include the removal of nitrogen compounds [53,75,76,151]. Plants can take up large amounts of both nitrogen and phosphorus (luxury consumption) compared with their immediate growth needs. Except at very low phosphorus concentrations, where charophytes are common and where phosphorus limitation of growth may be important, phosphorus is normally not scarce among dense plant beds, even if luxury uptake occurs, because of release from the sediments. There are several possible mechanisms for this, but anaerobic sediments favour phosphate release and the sediments laid down under plant beds tend to be deficient in oxygen through decomposition of sloughed off leaves and periphyton and the excreta of the invertebrate populations. Even aerobic sediments in shallow lakes emit much phosphorus, however, perhaps by physico-chemical as well as biologically mediated mechanisms [47,102].

Combined nitrogen, however, is very vulnerable. Not only can it be taken up by the plants, it can be denitrified to nitrogen gas especially in the conditions within plant beds, which include a gradient from severe deoxygenation at night to supersaturation with oxygen at the surface by day. Such alternation favours mineralisation of combined nitrogen to ammonia and oxidation to nitrate followed by denitrification to nitrogen gas. Combined nitrogen is frequently undetectable in the open water of plant-dominated lakes during the summer. One response of the phytoplankton community to this can be the development of nitrogen-fixing blue-green algae, but their growth is usually slow and large populations may not be able to build up before the growth season has ended. In theory, under nitrogen-limiting conditions, nitrogen fixers should become dominant [128], forming dense growths and potentially suppressing the plants. In practice this does not readily happen in temperate lakes, though it might in the longer growing seasons of sub-tropical and tropical lakes.