Portal de Periódicos da CAPES

Ferns, evolution, scale and intellectual impedimenta

2007; Wiley; Volume: 176; Issue: 3 Linguagem: Inglês

10.1111/j.1469-8137.2007.02232.x

1469-8137

M. C. F. Proctor,

Plant Parasitism and Resistance

When Thomas Henry Huxley wrote in 1881 ‘It is the customary fate of new truths to begin as heresies and to end as superstitions’ he was thinking in particular of Darwin's Origin of Species. He might equally have been thinking of a number of the great insights of the last few centuries: Hofmeister's great work on the life-cycles of the higher cryptogams (1851), or Einstein's theory of relativity (1905). Once these insights gain general currency, it is all too easy to suspend our critical faculties in their presence, and this uncritical acceptance can extend beyond the principle itself to the penumbra of perceived corollaries and illustrative examples which are by no means always logical consequences of it. The paper on tropical fern gametophytes by Watkins et al. (this issue; pp. 708–717) should prompt us to re-examine beliefs about our subject that we have unthinkingly held since our schooldays or first year at university. For me it particularly highlights two common impediments to our thinking – two pieces of intellectual baggage we carry forward from our education. One is an over-rigid and over-simplistic view of evolution, and the other is blindness to the ecological and physiological significance of physical scale. How many elementary textbooks of botany illustrate the life cycle of a fern with Dryopteris filix-mas, and portray its gametophyte as a delicate little heart-shaped structure confined to sheltered moist places, and imply that the need for liquid water for fertilization is a critical limitation for pteridophytes? Is the need for liquid water for germination of seeds any less a limitation to flowering plants? Fern prothalli are somehow left in limbo as ‘nonplants’. If these things did not seem important (or never occurred) to us, we probably never had occasion to give them serious thought. Why, if its prothallus is so poorly adapted for life on land, is Dryopteris filix-mas so common in our woods and hedgebanks? Why are the sporophyte and gametophyte generations so different in size and adaptation? After all, the common little Mediterranean fern Anogramma leptophylla has a perennial gametophyte which bears annual sporophytes (Sporne, 1962), and Watkins et al. cite two references to perennial gametophytes among tropical epiphytic ferns. In western Europe the gametophyte of Trichomanes speciosum is far more widely distributed than the sporophyte (Rumsey et al., 1998). And, taking a linear view of evolution, why are ferns (and bryophytes) still here at all? Surely they should have been supplanted by the better adapted seed plants long ago? Watkins et al. have done us the service of looking closely at the gametophytes of six tropical epiphytic ferns, and, refreshingly, seeing them as real plants making a life in real habitats. They emphasize the morphological diversity in tropical fern gametophytes, from simple prothalli in understorey species, to intricately branched thalli, often ornamented with proliferations or hairs, in drought-prone situations in the canopy where they coexist with epiphytic bryophytes. Parallel with this morphological diversity, they found diversity in desiccation tolerance, with gametophytes of epiphytic species of the upper canopy tolerant of even severe drying. ‘There is good reason to think that, for green land plants less than a few centimetres high, the poikilohydric strategy is generally optimal’ I have argued elsewhere (Proctor & Tuba, 2002; Proctor et al., 2007) that there are essentially two possible strategies for plant life on land. The vascular plants evolved a water-conducting system from the soil to the leaves, providing a continuing supply of water throughout the life of the plant; they may be seen as homoihydric. Many other organisms, including bryophytes, terrestrial algae and lichens, adopted the alternative strategy of metabolizing when water is available, and suspending metabolism when water dries up; they are poikilohydric. Alternatively, the vascular plant can be seen as endohydric (the physiologically important free water is in the xylem), and the bryophyte (or fern prothallus) as ectohydric (the physiologically important free water is in capillary spaces outside the plant). It is easy to see the poikilohydric option as simple, primitive, and a mere remnant of an earlier stage of evolution. But the division between the two strategies is intimately bound up with scale. At a scale of a metre or more, the vascular-plant pattern is unquestionably optimal. Most small vascular plants are short lived, and many are adapted to seasonal or sporadically favourable soil conditions, such as winter and spring annuals, or desert ephemerals. If two plants were exactly in proportion, but one was 10 times the size of the other, the larger would have roots 10 times as deep, its surface area for evaporation would be 100 times as great, its volume and mass would be 1000 times as great, and it would be able to exploit 1000 times the volume of soil. Of course small plants have not the same proportions as large ones, but it is evident from these scaling considerations alone that there must be a lower limit to the size at which the vascular-plant strategy is viable. This limit is probably often considerably above the minimum size envisaged by Raven (1999) for a vascular-plant seedling. There is good reason to think that, for green land plants less than a few centimetres high, the poikilohydric strategy is generally optimal. Perhaps the most persuasive argument is provided by evolution. The fossil record shows three distinctive groups of vascular plants, the lycopsids, the equisetoids and the ferns with their later offshoot the seed plants, coexisting over the past 400 million years with two and (if we are to believe the phyletic evidence; Renzaglia et al., 2007) probably three distinct groups of bryophytes, the liverworts, mosses and hornworts. These six groups, three homoihydric and three poikilohydric, have retained their identity, and their basic pattern of adaptation, through most of the history of plant life on land. There has been remarkably little trespass of these major adaptive types into the territory of the other. Many Palaeozoic lycopsids were tall trees; all extant species are vascular but relatively small plants, and a number of small Selaginella species are poikilohydric. The equisetoids have similarly declined from their Palaeozoic glory, but their modern representatives have remained firmly in the homoiohydric camp. The fern line has been far the most successful and diverse. Some small ferns have gone poikilohydric (Ceterach and Notochlaena are remarkably desiccation tolerant, and the Hymenophyllaceae include some convincing pseudo-bryophytes), but the ferns include herbaceous species of all sizes and sizeable trees, and of course in the later Palaeozoic and the Mesozoic the fern line gave rise to the seed plants that dominate the vegetation of the earth at the present day. The bryophytes, ranging from millimetres to centimetres in height, with dependent sporophytes, number some 20 000 species. They are prominent, sometimes dominant, in tundra, in the ground-layer of boreal forests, and in the mossy forests of hyperoceanic regions and tropical and subtropical mountains. The big Polytrichum and Dawsonia species, a few decimetres tall, have water-conducting tissue in their stems and hold their own amongst small vascular plants in bogs and humid forests, but retain their basically poikilohydric adaptation. Few habitats lack bryophytes completely. Sphagnum may be responsible for more fixed carbon on the surface of the earth than any other plant genus (Clymo & Hayward, 1982). The bryophytes are clearly not ‘an evolutionary backwater’ or evolutionarily unsuccessful at their scale. They compete not so much with the vascular plants as with the lichens, completely unrelated organisms, which match them in size and their poikilohydric pattern of adaptation, and rival them in ubiquity. The ferns, fascinatingly, have a foot in both camps. If we look at the gametophyte generation, they are another group of ‘bryophytes’, scarcely more different from the three bryophyte groups we traditionally recognize than those are from one another. But if we look at the sporophyte, we see a mainstream vascular plant. Our vascular plant-orientated upbringing tends to make us see everything, at whatever scale and in whatever context, in terms of minimizing water loss. Even for vascular plants that is far from the whole story. And for small poikilohydric plants it is hardly even the start of the story, which has to do with boundary-layer resistances and energy budgets (Gates, 1980; Monteith & Unsworth, 1990), and the unit for consideration is the colony and its surroundings, not the individual leaf or shoot. The humidity measures most useful in calculating the rate of water loss from leaves are not the most relevant to evaluating the rate of water loss from poikilohydric plants. Much of the intricacy of form of small poikilohydric plants lies within the laminar boundary layer where water vapour and CO2 move by relatively slow molecular diffusion. Intricacy of form may be related to capillary storage and movement of water (Zotz et al., 2000), to allowing free gas exchange, or to increasing the area for CO2 uptake (Proctor, 2005). We were told as students that the organism is the life cycle as a whole, not just the conspicuous bit of it (that early education is useful sometimes!); the gametophyte and sporophyte do not evolve in isolation. If there is a weak link in a life cycle, natural selection will remedy it or find a way round it – or the organism will go extinct.