J. B. S. Haldane (1927) wrote in his essay Possible worlds‘I suspect that there are more things in heaven and earth than are dreamed of, or can be dreamed of, in any philosophy.’ Since then we have had nuclear fission and the atomic bomb, ever-faster electronic computing and the internet, plate tectonics, almost all of our present knowledge of metabolic biochemistry, elucidation of the structure and role of DNA and all that has followed from it, space rockets and satellite communication and global positioning system (GPS) – and much, much more. And that leaves aside current thinking on cosmology. None of those things could have been predicted (except in the vaguest terms) in 1927 and none of them fundamentally violates the laws of thermodynamics. But there are many new ideas less momentous than these. We ought to think carefully before we dismiss concepts which may be new to us, even if they seem contrary to our preconceptions. I admit I was sceptical when I first saw the title of the paper by Lakatos et al. in this issue of New Phytologist (pp. 245–253), but that changed as I read and thought about it.
‘Lichens and bryophytes are sophisticated photo-autotrophs in their own right, not in any way “primitive” or “lower” in the sense of “haven’t made the grade”.’
For most of us our experience of dew is limited to dewfall on lawns and grazed pastures in the early morning after clear nights. We notice this because the leaves of the grasses are more or less water repellent so that the dew is condensed in spherical droplets, and dewfall is commonly supplemented by guttation. The daily dewfall is seldom > 0.2–0.4 mm (Monteith & Unsworth, 1990), too little to be a significant source of water for temperate crops but, as Lange and his colleagues have shown, sufficient to provide a positive daily carbon balance for desert lichens (Lange, 1969; Lange et al., 1970, and references cited therein). Dew in temperate forests is seldom considered. Energy exchanges in forest canopies are much more diffuse than in closely-grazed or mown grasslands, and in any case out of sight – and, too easily, out of mind too.
We are familiar with the idea that in a sun-exposed site the diel march of temperature is greatest and tracks the air temperature and radiation input most closely at the surface, and is progressively attenuated and delayed with depth in the soil. The same happens in a forest. The temperature in the canopy is rather closely coupled with air temperature. Yet it is common experience that at ground level woods are cool in the morning, and in late afternoon and evening on clear days they are the warmest place to be. As the measurements of Lakatos et al. show, at their field site the diel march of temperature of the trunks lags c. 6 h behind the ambient air temperature. The consequence is that water evaporated in the warming canopy diffuses downwards and some part of it is deposited on the cooler trunks, which have both a higher heat capacity and higher thermal conductivity than air. Lakatos et al. estimate the average quantity of this dew at just under 0.5 mm d−1. This is sufficient to bring lichens and bryophytes to full turgor and full metabolic activity.
In a nonforested landscape the early-morning rise of air temperature, and with it saturation-deficit, lags an hour or two behind radiation income. This means that there is potentially a ‘window’ of an hour or two immediately after sunrise during which a poikilohydric plant can recover, photosynthesize and establish a positive carbon balance, before it dries out again (Lange et al., 1970; Tuba et al., 1996; Csintalan et al., 2000). During most of the day net radiation and saturation-deficit are both high, and poikilohydric organisms are dry and metabolically inactive. To a first approximation the two major drivers of evaporation are roughly in phase. The physical structure and dimensions of the authors’ lowland tropical rainforest in French Guiana shifts the march of trunk temperature c. 6 h out of phase with net radiation income. Consequently the trunk surfaces are below the dew-point from c. 08:00–09:00 h in the morning to noon or 14:30 h in early afternoon, when light is near maximal. Because the bark and lichen surfaces are porous and hydrophilic the dew does not form discrete droplets but adds to the water already hydrating the lichen or the surface of the bark. By the time light is declining in late afternoon net evaporation rules again, but from 17:00 h onwards relative humidity has risen to over 80% again and saturation deficit will be low.
The energy for dew deposition on the cool trunks comes from the (intermittent) morning temperature difference between the ambient air and the trunks, prolonged by the phase-shift between the diel march of temperature in the canopy and in the understorey of the forest. The analogy of a tide mill comes to mind, driven by the intermittent source of energy presented by the regular rise and fall of the tides. It is an inherent strength of poikilohydric plants that they can take advantage of intermittent sources of water, which may be too little in total for vascular plants which need a constant supply of water to support a transpiration stream.
The photosynthetic responses of the lichens at Lakatos et al.’s site are complex and not clear cut, with one exception; the behaviour of the filamentous lichen Coenogonium linkii (projecting into the ambient air) stands apart from the three crustose species (in intimate contact with the trunk surface). The overall picture is that the epiphytes on the trunk surfaces probably never dry out completely. With hindsight, one could feel that chlorophyll fluorescence alone is not the ideal tool for a critical evaluation of the photosynthetic performance of poikilohydric epiphytes. One could wish for at least limited infrared gas-analysis or carbon isotope-uptake measurements to provide some fixed points – in conjunction with which chlorophyll fluorescence becomes a much more powerful and incisive tool. In particular, the use of Fv/Fm is subject to various pitfalls. Because this parameter is a ratio and nondimensional it says nothing about the quantity of material surviving (Proctor, 2003; Pressel et al., 2009). Further, Fv/Fm is not necessarily zero when poikilohydric autotrophs are dry; that depends on species and preceding conditions (Heber et al., 2006a,b; Proctor, 2010). This in no way diminishes the value of the authors’ contribution to our understanding of the complexity of the water supply – from direct rainfall, stemflow, dew, cloudwater interception – of epiphytic lichens and bryophytes in forests in general.
For the first 50 million yr of plant life on land the vegetation of the Earth seems to have consisted entirely of poikilohydric plants. The evolution of the ‘vascular-plant package’– the combination of roots, a conducting system, and ventilated photosynthetic tissue enclosed within a waterproof cuticularized epidermis with stomata – allowed exploitation of the third dimension, height, with all the advantages that gave. But in return for the advantages of the vascular habit there was a price to pay. A vascular plant is only viable above a certain minimum size (of the order of 1(−10) cm); it needs a constant supply of water and must acquire essential nutrients proportionate to its height, and it is dependent on a substratum penetrable by roots. Tall vascular plants are closely linked to air temperature, and forgo the intermittent microclimatic warming that smaller plants experience. Throughout evolutionary history poikilohydric plants have dominated habitats which are too cold, too dry, too nutrient-poor, too hard for roots to penetrate, or simply too small for vascular plants. ‘Biological soil crusts’ occupy many square kilometres in semi-arid and circumpolar regions and on high mountains, bryophytes are prominent in many wetlands, and bryophytes and lichens are a prominent part of the photosynthesizing biomass in many forests from the equatorial lowlands to the latitudinal and altitudinal limits of forest growth.
We need much more research on the ecophysiology of poikilohydric plants and their plant–habitat relations. This includes more long runs of high-resolution microclimatic and plant-response data. The sensors and computing power now available make this relatively cheap and easy to do. Lichens and bryophytes are sophisticated photo-autotrophs in their own right, not in any way ‘primitive’ or ‘lower’ in the sense of ‘haven’t made the grade’. They are the products of the same 400 million yr of evolution, and should be approached from cell-biological and physical first principles. The label ‘lower’ plants is like the label ‘black’. As simple adjectives they are both harmless, but in plant science as in society it is the cluster of associations they arouse in many people that do the damage.