Not known, probably —2
This newly separated group of species tolerant of chronic nutrient stress accom
modates the prokaryotic picoplankters that dominate the rarefied environments
of the tropical seas and which, increasingly, have been shown to be active in the
open waters of the world's largest and most oligotrophic lakes (Reynolds et al.,
2001). They are non-
motile but have very low sinking rates. Their small size is the
key to living on very
dilute nutrient sources. It would leave them very vulnerable
to grazing by filter-feeders, except that they inhabit environments that fail to sus
tain filter-feeding zooplankton. Representative genera Prochlorococcus (in the sea;
Cyanobium, Cyanodictyon are considered to be limnetic analogues).
commonly supposed by many plankton ecolo-gists that nutrient exhaustion is followed by mass clonal mortalities. This view was perhaps encouraged by numerous observations of 'bloom collapse', of diatoms running out of silicon (e.g. Moed, 1973) or the photolysis of surface scums of Cyanobacteria (e.g. Abeliovich and Shilo, 1972). These relatively impressive eventualities apart, however, phytoplankters are rather better prepared than this to be able to avoid sudden death and disintegration. Depletion of one of the essential resources usually leads to a cellular reserve of the others and the cell may be able to use stored carbohydrate, polyphosphate or protein reserves to maintain some essential activity. However, it is quite clear that it is better for the cell to lower its metabolism and to close down those processes not directly associated with actually staying alive. Earlier chapters have emphasised the mechanisms for internal communication of nutrient-uptake activity of the membrane- transport system (Section 4.2.2), the activation of inhibitory nucleotides (such as ppGpp) in response to falling amino-acid synthesis (Section 4.3.3) and the suspension of nuclear division (Section 5.2.1). Each represents a step in the biochemical procedure by which the cell senses its environmental circumstances and organises its appropriate defences to enhance its survival prospects. These may include the inception of a 'cytological siege economy' and the structural reorganisation of the protoplast into resting cells, with or without thickened walls.
The biological forms of most kinds of resting cell are well recognised by plankton ecolo-gists and, in many cases, so are the environmental attributes which induce them. Equally, the implicit benefit of survival of resting stages is widely accepted as a means to recruit later populations from an accumulated 'seed bank'. They need to recognise and respond to their reintroduction into favourable environments or to ameliorating conditions by embarking upon a phase of renewed vegetative growth. However, it has to be stated that, in marked contrast to the efforts that have been made to observe and understand the mechanisms generating the spatial and temporal patterns of phytoplankton occurrence, detailed information on the significance of reproductive and resting propagules has been mainly confined to studies on particular phyloge-netic groups (Sandgren, 1988a). It is not inappropriate to give a brief perspective at this point.
Resting stages come in a variety of forms and are stimulated by a variety of proximate events and circumstances, and their success in 'carrying forward' biomass and genomes is also quite variable. Among the simplest resting stages are the contracted protoplasts produced in such centric diatoms as Aulacoseira (Lund, 1954) and Stephano-discus spp. (Reynolds, 1973a). These form quite freely in cells falling into aphotic layers and may be prompted by microaerophily and low redox, which conditions may be tolerated for a year or more. The contents pull away from the wall, abandon the central vacuole and shrink to a tight ball, a micrometre or so in diameter. Individual cells or filaments containing resting stages litter the surface sediments. If seeded sediment is placed under low light in the laboratory, Aulaco-seira will 'germinate' and produce swathes of new filaments in situ. Germination in nature may be only a little less spectacular but it always depends upon the resuspension of filaments and cells by entrainment from sediments accessible to turbulent shear. Thus, formation and germination of the resting stages is governed by the activity or otherwise of its photosynthetic capacity. Perhaps 5-20% of the sedimenting population may form resting stages. The percentage of these that return to the plankton is probably small but they can provide quantitatively important inocula to future populations (Reynolds, 1988a, 1996b).
The Cyanobacterium Microcystis has the ability to control its own vertical migrations through regulating its buoyancy and, in warm latitudes, it may move frequently (perhaps dielly) between sediment and water, very much as part of its vegetative activity (May, 1972; Ganf, 1974a; Tow, 1979). In temperate lakes, Microcystis is frequently observed to overwinter on the bottom sediments (Wesenberg-Lund, 1904; Gorham, 1958; Chernousova et al., 1968; Reynolds and Rogers, 1976; Fallon and Brock, 1981; and many others reviewed in Reynolds, 1987a). There is a massive autumnal recruitment of vegetative colonies from the plankton to depth (Preston et al., 1980), where they enter a physiological resting stage.
No physical change occurs (they do not encyst) and chlorophyll, as well as a latent capacity for normal, oxygenic photosynthesis, is retained (Fallon and Brock, 1981). Curiously, the cells also remain gas-vacuolate. Despite being (initially) loaded with glycogen, other carbohydrates, proteinaceous structured granules and polyphosphate (Reynolds et al., 1981), they would be buoyant but for the precipitation of iron hydroxide on the colony surfaces, which acts as ballast and causes the organisms to sink (Oliver et al., 1985). Once on the sediments, in very weak light and at low temperatures, they experience considerable mortalities, although some cells live on under these conditions, apparently for several years in some cases (see Livingstone and Cambray, 1978). The surviving cells function at a very low metabolism and are tolerant of sediment anoxia (and consequent re-solution of the attached iron) but there are, by now, too few of them to lift the erstwhile colonial matrix back into the water column.
Reinvasion of the water column follows a phase of in-situ cell division, in which clusters of young cells are formed, constituting a pustulelike structure that buds out of the original, 'maternal' mucilage matrix, until it is released or it escapes into the water. The process was described originally by Wesenberg-Lund (1904), but the information was largely ignored. The 'nanocytes' found by Canabeus (1929) and, later, 'rediscovered' by Pretorius et al. (1977), seem to refer to the young, budding colonies. Sirenko (pesonal communication quoted in Reynolds, 1987a) has viewed the entire sequence, claiming that the potential mother cells are identifiable in advance by their larger size and more intense chlorophyll fluorescence. The process has also been reproduced under controlled conditions in the laboratory (Caceres and Reynolds, 1984), using material sampled from autumnal sediment. It requires the exceedence of a temperature and insolation threshold and it occurs more rapidly while anaerobic conditions persist. These conditions have to be mirrored in natural lakes of the temperate regions before Microcystis colonies begin to be recruited to the water column in the spring. Sediments have to retain colonies through the winter period, where colonies apparently need the low temperatures and low oxygen levels for their maturation. Ultimately, they also require low oxygen levels and simultaneous low insolation to persuade them to initiate the formation of the new colonies that recolonise the water column in the following year (Reynolds and Bellinger, 1992; Brunberg and Blomqvist, 2003). The completion of this cyclical process depends on interactions among light, temperature and sediment oxygen demand. Whereas upwards of 50% of the colonies constituting the previous summer maximum number of colonies may settle to the sediments, <10% might contribute to the re-establishment of a summer population the following year (Preston et al., 1980; Brunberg and Blomqvist, 2003; Ishikawa et al., 2003).
It may be noted that Microcystis colonies also survive in microenvironments created by downwind accumulations of surface scums on large lakes and reservoirs, especially where warm summers, high energy inputs and high upstream nutrient loadings are simultaneously prevalent. Good examples come from the reservoirs of the Dnieper cascade (Sirenko, 1972) and the Hart-beespoort Dam in South Africa (Zohary and Robarts, 1989). The conditions in these thick, copious 'crusts' or 'hyperscums' are effectively lightless and strongly reducing (Zohary and Pais-Madeira, 1990) but, save those actually baked dry at the surface, Microcystis cells long remain viable and capable of recovering their growth.
Many species respond to the fabled 'onset of adverse conditions' by producing morphologically distinct resting propagules. Among the best known are the cysts of dinoflagellates, which are sufficiently robust to persist as a fossils of palaeontological significance (for a review, see Dale, 2001). Some 10% of the 2000 or so marine species are known to produce resting cysts. In some instances, they are known, or are believed, to be sexually produced hypnozygotes. The cell walls in many species contain a heavy and complex organic substance called dinosporin, chemically similar to sporopollenin of higher-plant pollen grains. Some species deposit calcite. In the laboratory, cyst formation may, indeed, be induced by nutrient deprivation and adverse conditions but the regular, annual formation of cysts in nature (coastal waters, eutrophic lakes) possibly occurs in response to cues that anticipate 'adverse' conditions rather than the actual onset of those adversities. The protoplasts of newly formed cysts usually contain conspicuous reserves of lipid and carbohydrate, accumulated during stationary growth (Chapman et al.,
1980). The number of cysts produced by freshwater Ceratium hirundinella in autumn has been estimated from the sedimentary flux to account for <35% of the maximum standing crop of vegetative cells (Reynolds et al., 1983b). The success in recruiting vegetative cells from excysting propag-ules in the following spring is, in part, proportional to the abundance of spores retained from the previous year (Reynolds, 1978d; Heaney et al.,
The excystment of vegetative cells from cysts was first described by Huber and Nipkow (1922). Much detail has been added from such landmark micrographic investigations as those of Wall and Dale (1968) and Chapman et al. (1981). A naked flagellate cell, or gymnoceratium, emerges through an exit slit and soon acquires the distinctive thecal plates of the vegetative cell. Heaney et al. (1981) noted a sharp, late-winter recruitment of new, vegetative cells of Ceratium to the plankton of Esthwaite Water, UK, after the water temperature exceeded 5 °C, and coincident with an abrupt increase in the proportion of the empty cysts recoverable from the bottom sediments of the lake.
Among the Volvocales, sexually produced zygotes of (e.g.) Eudorina (Reynolds et al., 1982a) and Volvox (Reynolds, 1983b) have the robust appearance of resting cysts and, indeed, serve as perennating propagules between population maxima. Deteriorating environmental conditions may trigger the onset of gametogenesis but formation of the eventual resting stages cannot be claimed certainly to have been consequential on resource starvation. Among the Chrysophyceae, there has evolved an opportunistic perennation strategy, involving zygotic and asexual cysts that are produced early in the growth cycle, when conditions are supposedly good (Sandgren, 1988b). This pattern of encystment apparently ensures the production of resting stages during what often turn out to be short phases of environmen tal adequacy but which are tenanted briefly by vegetative populations.
In contrast, nostocalean Cyanobacteria produce their asexual akinetes in rapid response to the onset of physiological stress. Akinetes are the well-known 'resting stages' of such genera as Anabaena, Aphanizomenon and Gloeotrichia (Roelofs and Oglesby, 1970; Wildman et al., 1975; Rother and Fay, 1977; Cmiech et al, 1984). These, too, have typically thickened external walls, within which the protoplast remains viable for many years. Livingstone and Jaworski (1980) germinated akinetes of Anabaena from sediments confidently dated to have been laid down 64 years previously. On the other hand, rapid akinete production has been stimulated in the laboratory by the sort of carbon : nitrogen imbalance that occurs as a consequence of surface blooming, and from which conditions an effective means of escape is offered (Rother and Fay, 1979). Moreover, substantial germination can take place shortly (days rather than months or years) after akinete formation, provided the external conditions (temperature, light and, possibly, nutrients) are suitable (Rother and Fay, 1977). Reynolds (1972) observed that Anabaena akinetes were regularly resuspended by wind action in a shallow lake but failed to germinate before a temperature or insolation threshold had been surpassed. In other years, vegetative filaments surviving the winter were sufficient to explain the growth in the following season. These thresholds could be important to the distributions of individual species. The current spread of Cylindrospermopsis raciborskii from the tropics to continental lakes in the warm temperate belt may be delimited by a germination threshold temperature of 22 °C (Padisak, 1997). The akinetes of Gloeotrichia echinulata are able to take up phosphate through their walls and colonies germinating the following year can sustain substantial growth even when limnetic supplies are small (Istvanovics et al., 1993).
As suggested above, regenerative strategies are not uniform among the phytoplankton, neither is the production of spores and resting stages exclusively brought on by 'adverse conditions'. However, the existence of resting propagules of a given species are likely tolerant of more severe conditions than vegetative cells and they do increase the probability of survival through difficult times and also perhaps raise the scale of the infective inoculum when favourable conditions return.
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