Most animals and plants have only a limited ability to survive water loss. Humans may die if they lose 14 per cent of the water from their bodies. Some frogs can lose 50 per cent and some earthworms 83 per cent of their water and still recover. Some organisms, however, can lose more than 95 per cent, or even more than 99 per cent, of their water and enter into a state of anhydrobiosis (life without water) in which their metabolism comes, reversibly, to a standstill. There is a problem, however, in defining which organisms are capable of anhydrobiosis. Organisms show a whole range of abilities to survive water loss, ranging from losing just a little bit (as can humans) to losing almost all of it. At what point do we consider an organism to be anhydrobiotic?
Anhydrobiosis is best defined in terms of its effect on metabolism. Losing a little bit of water may have no effect on metabolism. Losing more may depress metabolism, but further water loss will cause it to cease altogether. Consider what happens to metabolism in mammals which survive the winter in a state of deep hibernation. Hibernating mammals have a reduced rate of metabolism, but they do not cease metabolising altogether. We have one term for animals which have ceased metabolising - we refer to them as being 'dead'. The difference between anhydrobiosis and death is that an organism in a state of anhy-drobiosis will recover, grow and reproduce when normal conditions return (when immersed in water), whereas a dead organism will not. We could thus define anhydrobiosis as 'the ability to survive the cessation of metabolism due to water loss'.
Anhydrobiosis represents an extreme example of a resistance adaptation, where the organism shuts down operations completely as a result of water loss and survives in an ametabolic state until water returns. Are there any organisms which can continue to function in the absence of water? The answer is almost certainly no, given the vital role of water in metabolism. There have been, however, some interesting reports concerning nematodes from the Dry Valleys of Antarctica. Diana Wall, from Colorado State University, and her coworkers, have reported the presence of nematodes in the very dry soils of the Dry Valleys. These must be relying on very occasional inputs of water from melting snow or from glaciers, or are blown there from more productive sites. They presumably spend most of their time in anhydrobiosis.
Among animals, there appears to be an upper limit on the size and complexity of those which are capable of anhydrobiosis. The largest such animal is the midge larva Polypedilium vanderplanki from rain-filled rock pools in Africa, which is about 5 millimetres long (Figure 3.1). P. vanderplanki and the larvae of a few other species of chironomids or midges are the only higher insects known to survive anhydrobiotically. Springtails (collembolans) are a group of primitive wingless insects, a figure 3.1 The larva of the midge Polypedilium vanderplanki, found in rain-filled ponds in Africa, is the largest known anhydrobiotic animal (about half a centimetre long). Drawing by Jo Ogier (redrawn from Hinton, 1960).
few species of which are capable of anhydrobiosis. A number of crustaceans which inhabit temporary and saline ponds can survive anhydrob-iotically; the best known of these is the brine shrimp Artemia, which survives as an encysted embryo. Nematodes, rotifers and tardigrades are groups of invertebrates, consisting mainly of species which are microscopic in size. They need at least a film of water for activity and growth, but, in some environments, they are exposed to desiccation for varying periods of time. Such environments include soil, moss, deserts, temporary ponds, terrestrial polar habitats, the aerial parts of plants and, for plant-parasitic nematodes, plant tissue which dries out when the plant dies or sets seed. Not all species of these invertebrates are capable of anhydrobiosis; their desiccation survival abilities match the stresses they face in their environment.
Most plants have stages in their life cycles which are very dry. Dehydration is part of the maturation process of plant seeds and most have a water content of 5-20 per cent. Some have even lower water contents; for example, the seeds of birch trees have a water content of only 0.01-0.4 per cent. At such low water contents, these seeds are likely to be anhydrobiotic. The pollen (male reproductive agent) of many plants is also very dry and can tolerate the desiccation experienced during its dispersal by the wind or on the bodies of insects. Most plants lose the ability to survive desiccation once their seed germinates and starts to grow. There are a few plants, however, that can survive anhydrobiosis in their mature growth forms. Some plants from southern Africa can survive after losing so much water that their leaves crumble into dust if rubbed between the fingers. These 'resurrection plants' will survive exposure to 0 per cent relative humidity and a water content of less than 5 per cent and yet recover and grow when it rains. Over 100 species of resurrection plants have been described, mostly from the hot dry regions of Southern Africa and Australia, including species from a variety of groups of flowering plants and from ferns and their allies. These plants are the first to colonise rock surfaces and shallow soils, where they are likely to be exposed to extreme desiccation and conditions which are too harsh for other plants to survive.
Mosses have no roots and are dependent on absorbing water across their surface, which confines their growth to habitats which are, at least periodically, wet. Nevertheless, many species can survive desiccation. This is particularly important for mosses that live in dry regions such as deserts, but also for those that live on the surface of rocks or of plants (such as the bark of trees), where they may occasionally dry out. The spores of mosses, and of other groups of primitive plants, can also tolerate desiccation. A wide variety of algae are associated with sites where they are exposed to desiccation, such as the surface and interior of rocks and in desert and other arid soils. These must also have life cycle stages which can survive anhydrobiotically. Algae (and cyanobacteria) also associate with fungi to form lichens which colonise desiccation-prone sites, including bare soil, the surface of rocks and tree trunks. Many fungi can tolerate desiccation and their spores are particularly resistant. Yeasts, which are single-celled fungi, will survive dehydration if desiccated and rehydrated under the right conditions. Yeasts, which are used for making bread, wine and beer, are often supplied commercially as a dry powder. Protozoa can also survive anhydrobiosis, particularly as cysts.
Many bacteria have some ability to survive anhydrobiosis, although their ability to do so depends on the rate of desiccation. Some will survive high rates of water loss, while others require a slow rate of water loss in order to survive. In general, however, bacteria can survive better after slow rather than fast drying. Spores are particularly resistant. Cyanobacteria are prominent members of the bacterial communities of a variety of extreme environments. They survive anhydrobiotically in deserts, polar regions and in a variety of other terrestrial sites where they are exposed to desiccation, such as depressions in rocks and the surface of roofs.
Although this may seem already to be a fairly long list of organisms, anhydrobiosis is probably much more widespread than we presently realise. As we will see later, many anhydrobiotic organisms need a slow rate of water loss in order to survive. Many anhydrobiotic animals and plants were discovered from material collected dry in the field, where they naturally experience slow water loss. Drying an organism on a glass slide on the laboratory bench or over a desiccant is not a fair test of its ability to survive anhydrobiosis. It needs to be dried at a rate which mimics the rates of water loss it is likely to experience in its natural environment. For many, this means drying them very slowly indeed. Using environmentally relevant rates of desiccation will certainly allow us to discover many more anhydrobiotic organisms.
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