Proctor 2002

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fm Page 327 Thursday, November 7, 2002 4:07 PM
Review
Tansley review no. 141

Blackwell Science, Ltd
Poikilohydry and homoihydry: antithesis

or spectrum of possibilities?
Author for correspondence: Michael C. F. Proctor1 and Zoltán Tuba2

Michael C. F. Proctor 1
School of Biological Sciences, University of Exeter, Washington Singer Laboratories, Perry Road, Exeter
Tel: +44 (0) 1392 432255
Fax: +44 (0) 1392 264668 EX4 4PS, UK; 2Department of Botany and Plant Physiology and Departmental Research Group of
Email: [email protected] Hungarian Academy of Sciences, Faculty of Agricultural and Environmental Sciences, Szent István
Received: 17 April 2002 University, H-2103 Gödöllõ, Páter K. u. 1., Hungary
Accepted: 2 August 2002
Contents
Summary 327 IV. Anatomical and physiological requirements and
implications of desiccation tolerance 333
I. Introduction 328
V. Time-scale considerations and ecological adaptation 340
II. The soil–plant–atmosphere continuum 329
VI. Conclusion 344
III. Desiccation-tolerant plants: taxonomic distribution and
Acknowledgements 344
functional characteristics 331
References 344
Summary
Key words: desiccation tolerance, Plants have followed two principal (and contrasting) strategies of adaptation to the
bryophytes, pteridophytes, resurrection irregular supply of water on land, which are closely bound up with scale. Vascular
plants, ectohydry and endohydry, water plants evolved internal transport from the soil to the leafy canopy (but their
stress, poikilochlorophylly, adaptive ‘homoihydry’ is far from absolute, and some are desiccation tolerant (DT)). Bryo-
strategies. phytes depended on desiccation tolerance, suspending metabolism when water was
not available; their cells are generally either fully turgid or desiccated. Desiccation
tolerance requires preservation intact through drying–re-wetting cycles of essential
cell components and their functional relationships, and controlled cessation and
restarting of metabolism. In many bryophytes and some vascular plants tolerance is
essentially constitutive. In other vascular plants (particularly poikilochlorophyllous
species) and some bryophytes tolerance is induced by water stress. Desiccation
tolerance is adaptively optimal on hard substrates impenetrable to roots, and on
poor dry soils in seasonally dry climates. DT vascular plants are commonest in warm
semiarid climates; DT mosses and lichens occur from tropical to polar regions. DT
plants vary widely in their inertia to changing water content. Some mosses and lichens
dry out and recover within an hour or less; vascular species typically respond on a
time scale of one to a few days.
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328 Review Tansley review no. 141
I. Introduction 2. The vascular-plant strategy

We take for granted the basic physiology of water movement
1. Plant life on land: aims of this review
in the vascular-plant. Water is absorbed by roots from the soil
Plants emerging onto land faced quite different constraints at relatively high water potential. The xylem then provides a
from their evolutionary precursors in water. For photosynthetic low-resistance pathway to the photosynthetic tissue of the
organisms in water the environment is essentially uniform; leaves. The leaves (and other subaerial plant parts) are covered
although individual nutrients (e.g. P, Si, Fe) may be limiting with a more-or-less waterproof cuticle, and loss of water
in particular instances, the major fundamental limitation is vapour is regulated by the variable diffusion resistance of the
availability of light. Solid surfaces may be important for stomata. Indisputably effective (and the basis of most plant
support, but mineral nutrients can be absorbed and gas biomass on the planet), this vascular-plant pattern of
exchange can take place over the whole surface of the adaptation has limitations. It depends critically on the more-
organism from the water that surrounds it. Plants on land face or-less continuous availability of a reservoir of water in the
an essentially discontinuous environment. Water and mineral soil. If this fails, or if there is no soil or equivalent substrate in
nutrients may be continuously available below ground, which a root system can develop, the habitat is untenable to
but there is light only above the ground surface, where the plant growth. Stomatal regulation of water loss itself has
supply of water is often intermittent and uncertain. Raven limitations. Uptake of CO2 for photosynthesis necessarily
(1977, 1984) has emphasised the essential role played by carries with it the possibility of water loss. Transpiration is
the development of supracellular transport systems as a linked not only to water balance but also with the heat balance
prerequisite for the evolution of a land flora. These are of the plant, and in some situations evaporative cooling may
exemplified particularly by the xylem and phloem of the be an inescapable price of survival. These limitations, and
vascular plants that dominate present-day vegetation, with adaptations that circumvent or minimise them, are further
their ventilated photosynthetic tissues, impermeable cuticles considered below.
and stomatal regulation of water loss. It is easy to regard this
as the solution to the problem of plant life on land. But
3. The poikilohydric strategy
some major groups of plants depend on the alternative
solution of carrying on their photosynthesis and growth The poikilohydric alternative is exemplified by many
when water is available – and when it is not, suspending bryophytes and lichens, such as the various saxicolous and
metabolism until favourable conditions return. These alternative desert lichens studied by Ried (1960a,b) and by Lange and
adaptive strategies may be contrasted as ‘homoihydry’ and colleagues (Lange & Bertsch, 1965; Lange et al., 1968, 1970;
‘poikilohydry’. Lange, 1969, 1988; Lange & Evenari, 1971; Kappen et al.,
In what follows we argue three propositions. First, 1979), the much-studied moss Tortula (Syntrichia) ruralis
poikilohydry is not merely the primitive starting point of (Willis, 1964; Schonbeck & Bewley, 1981a,b; Tuba, 1985;
plants that failed to achieve homoihydry, but a highly Oliver, 1991; Oliver et al., 1993; Tuba et al., 1996), and
evolved strategy of adaptation in its own right, optimal in various other mosses and liverworts (Abel, 1956; Clausen,
some situations and at least a viable alternative in some 1952; Hosokawa & Kubota, 1957; Hinshiri & Proctor, 1971;
others. Second, these two strategies are not as sharply Dilks & Proctor, 1974, 1976). In general, these plants can
bounded as appears at first sight. Third, they are intimately gain and lose water rapidly, and there is no control over water
confounded with physical considerations of scale. It is loss comparable to that in vascular plants. Water conduction
implicit in much of our argument that traditional vascular- is typically external and diffuse. The plants can survive drying
plant preconceptions are not universally true, and can be to a point where no liquid phase remains in the cells and the
obstacles to understanding – even sometimes of vascular water content may be no more than 5–10% d. wt (equivalent
plants. to an equilibrium water potential of −100 MPa or less). On
We begin with some basic environmental physiology to remoistening, essentially normal metabolism returns within
provide background and context. We then outline the taxo- minutes or hours. The capillary space associated with the
nomic distribution and some characteristics of poikilohydric, plant often provides a substantial reservoir of water external to
desiccation-tolerant (DT) land plants. We conclude by the photosynthesising cells while still permitting relatively
examining in more detail some specific aspects of the physio- free gas exchange (Dilks & Proctor, 1979; Proctor & Smith,
logy of DT plants, and considering their adaptive relationships 1995; Zotz et al., 2000), which is probably essential to the
in a broad ecophysiological context. The present review may functioning of most if not all of these plants. Most of this
be read in the context of, and is complementary to, recent external water can be lost without affecting cell water status.
reviews by Hartung et al. (1998), Kappen & Valladares The response of photosynthesis to cell water content appears
(1999), Scott (2000), and the book edited by Black & to be substantially the same as in vascular plants (Dilks &
Pritchard (2002). Proctor, 1979; Tuba et al., 1996; Proctor, 2000).
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Tansley review no. 141 Review 329
pathways, one via the variable resistance of the stomata (of

II. The soil–plant–atmosphere continuum low resistance when the stomata are open), the second (of
relatively high and constant resistance) through the cuticle.
1. Generalities: internal and external water conduction
Similar diagrams can be drawn for other plants. Figure 1(b) is
In general, water must move from the soil into the roots, for a small ground-dwelling moss (e.g. Barbula convoluta),
through the conducting system to the aerial parts of the plant, which can maintain turgor for a period after rain as long as the
and finally be lost to the atmosphere, down a gradient of ground surface remains moist and evaporation is not too
progressively falling water potential. Conceptually the path- rapid; some mosses of continuously wet habitats are striking
way is analogous to an electrical circuit, in which a current instances of this type of adaptation (e.g. Dicranella palustris,
passes from earth, through a network of resistances, to a Pohlia albicans). Water conduction can take place internally in
terminal at a negative potential (Van den Honert, 1948; the free space of the cell walls, and externally through capillary
Jones, 1992; Tyree, 1997). In principle, the potential at any spaces on the wettable exterior of the shoots. Typically, some
point in the system can be calculated from Ohm’s law if the development of water-repellent cuticular material on the sur-
current and resistances are known. In fact, in the soil–plant– face of the younger cells keeps them free of superincumbent
atmosphere continuum the system falls into two parts. In the water which would interfere with gas exchange (Kershaw,
liquid phase from the soil to the evaporating surface of the 1972, 1985; Dilks & Proctor, 1979; Proctor, 1979b; Nash,
leaf, rate of flow depends on pressure difference (directly 1996; Tuba et al., 1996; Zotz et al., 2000). The diffusion
related to water potential), and a hydraulic resistance which resistance of the laminar boundary layer accounts for the
depends on the dimensions of the channels carrying the whole of the gas-phase resistance to water loss. Figure 1(c)
transpiration stream and the viscosity of the moving liquid represents a mat or cushion-forming moss on an impermeable
(relatively insensitive to temperature). In the gas phase from substrate (e.g. Hypnum cupressiforme on a tree branch, Grim-
the evaporating surface to the free atmosphere, water potential mia pulvinata on a wall top). These plants function on water
dictates the direction of flow, but the rate is determined by stored after rain; the low-resistance path to ‘earth’ of the elec-
(a) the difference in water-vapour concentration between the trical analogy in Fig. 1(a,b) is replaced by a capacitor or
saturated air at the evaporating surface and the surrounding rechargeable battery, charged by rain and then drained over a
atmosphere (which typically changes steeply with temperature), period of time by evaporation. Water conduction is external,
and (b) the diffusion resistance of the laminar boundary layer with very low hydraulic resistance to water movement in the
plus whatever other impediments to free diffusion the plant capillary spaces around the shoots. As long as water remains
surface may impose ( Jones, 1992). in these spaces, the water potential of the cells must remain
Resistance diagrams for the soil–plant–atmosphere con- high. When it is exhausted, water potential rapidly falls to
tinuum are most often drawn for vascular plants, on the lines levels at which all metabolism stops. Intermediates between
of Fig. 1(a), which envisages a series of hydraulic resistances, in these three types occur widely. Some large ground mosses (e.g.
the soil immediately surrounding the roots, in the root paren- Polytrichaceae, Mniaceae) have well-developed internal water-
chyma, in the xylem between root and leaf, and between the conduction strands of ‘hydroids’ (Mägdefrau, 1935; Hébant,
finest tracheids and the evaporating surfaces of the mesophyll. 1977); mosses and leafy liverworts provide a complete range
From the mesophyll to the atmosphere there are two parallel of intermediates between the types of Fig. 1(b,c).
Fig. 1 Resistance to water flow in (a) a

vascular plant (b) an endohydric bryophyte
on a moist porous substrate, and (c) an
ectohydric bryophyte dependent on stored
water, represented as analogous electrical
circuits. Capital letters represent hydraulic
resistances (Rint, internal; Rext, external),
small letters (r) gaseous diffusion
resistances. Cuticular resistance (rc) may be
regarded as substantially constant, but
stomatal resistance (Rs) varies with
stomatal opening, and boundary-layer
resistance (rA) with windspeed; these are
the most important resistances in
controlling water loss. The external
hydraulic resistance varies with water
content, but will generally be low. Redrawn
from Proctor (1982, 1990).
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rather than lack of regulation of water loss. External rather

2. What are the possibilities (and limitations) for
than internal water conduction is a viable adaptive possibility
regulation of plant water content?
for a plant which for other reasons operates only when water
This may at first sight appear a trivial question, because it is is freely available in its immediate surroundings.
so easy to see the answer simply in terms of stomata.
Consideration of the potential limits of regulation shows that
3. What happens when stomatal regulation fails?
the question is far from trivial; indeed we all know that
stomata are not the answer to all the plant’s problems of water For many vascular mesophytes, regulation of water loss may
acquisition and loss ( Jarvis & McNaughton, 1986). If water be no problem. If soil water is adequate, the highest resistance
is freely available from the soil, even with negligible stomatal to water loss is in the gas phase, and we see the common
resistance, the rate of water loss is limited by physical pattern of stomata open during the day, and closed during the
considerations (boundary-layer resistance, supply of latent night – and most of the time serving no more than a minor
heat of evaporation) whose effect can be calculated from the trimming function in relation to water loss. This may seem to
Penman-Monteith equation (Monteith & Unsworth, 1990), belittle the significance of stomata. But it should also alert us
and under all but extreme conditions the plant typically against taking too-facile a view of the leaf with its ventilated
remains turgid. If the soil dries (or its solute content increases) mesophyll, epidermis and stomata, as simply a set of adap-
to the point where its water potential equals that of the tations for regulation of water loss. Arguably the primary
mesophyll, water cannot flow from root to leaf and turgor functional significance of ventilated photosynthetic tissues
cannot be maintained, even with fully closed stomata and zero is in increasing the effective area for CO2 uptake (driven by
transpiration. But zero water loss will generally entail zero a small concentration gradient, with the main resistance in
CO2 uptake; a positive carbon balance is generally inseparable the liquid phase within the mesophyll cells), without increasing
from some loss of water. Even with a substantial water- the area for water loss (driven by a large concentration
potential difference between soil and mesophyll, loss of cell gradient, with the resistance mainly in the much longer
water and wilting may still occur if this is exceeded by the gas-phase diffusion path outside the cells) (Von Caemmerer,
potential difference needed to drive the transpiration stream 2000). Stomatal closure at night may relate mainly to conserv-
through the xylem. Vascular plants only achieve homoihydry ing respired CO2, so enhancing early morning photosynthesis
within certain limits. (Martin, 1996). In this scenario, regulation of water loss by
Absorbed solar radiation must be balanced by heat loss, stomata could be secondary!
principally through a combination of radiation, convective Accepting that regulation of water loss by stomata is often
heat transfer to the air, and the latent heat of evaporation of important, what are the fall-back options when stomatal reg-
transpired water (Campbell, 1977; Gates, 1980; Monteith & ulation fails? A common vascular-plant solution to predicta-
Unsworth, 1990; Jones, 1992). If irradiance and resistance to ble seasonal drought is to set seed and die – the ‘therophyte’
convective heat loss are both high, as in many situations close strategy, which of course involves a desiccation-tolerant phase
to the ground, convective and radiative heat loss alone are in the life-cycle, the seed. Another solution is to senesce the
often inadequate to keep the surface temperature below lethal above-ground parts of the plant and to withdraw under-
levels on a clear sunny day. Evaporative cooling is then vital to ground for the dry season into a bulb, tuber or rhizome – the
survival. Low-growing plants of open sunny habitats typically ‘geophyte’ strategy. Both of these are well-known Raunkiaer
transpire rapidly even under apparently dry conditions. If life forms (Raunkiaer, 1934; Whittaker, 1975), common in
water is limiting they progressively senesce leaf area, or die seasonally dry habitats.
(usually having first set seed). Perennial plants of semiarid Maintaining a continued living presence above ground is
habitats typically have a plant and leaf form offering minimal another matter. As already indicated, some perennial plants of
resistance to convective heat transfer, and little or no leaf close dry grasslands respond by progressively senescing older leaves,
to the ground in the dry season. Trees and shrubs with small so reducing demand on the root system, but this is merely a
or narrow leaves are closely coupled to the temperature of the survival expedient differing from the geophyte strategy only in
air, and can close their stomata to minimise water loss – but degree. Species of semiarid or saline habitats have evolved
at the price of limiting significant carbon gain and growth to adaptations allowing more or less normal cell function at
periods when water is more freely available. A plant cover in lowered water potentials, often by segregating high concentra-
which heat exchange is concentrated within the boundary tions of ions in the vacuole, balanced by the production of
layer close to soil level is very much at the mercy of water compatible solutes in the cytoplasm. In effect the water poten-
availability and its radiation environment, regardless of tial of the whole soil–plant–atmosphere continuum is shifted
stomatal regulation. downwards.
Nonvascular plants without stomatal regulation may thus A different category of adaptations still depend on stomatal
be less disadvantaged than appears at first sight. Their ‘dis- regulation but increase water-use efficiency. These are devices
advantage’ is lack (or limitation) of water supply from the soil, minimising the water loss concomitant with growth rather

than a fall-back when regulation fails. The carbon-concentrating steppe grasslands, are scarcely less tolerant. These and com-
mechanism of C4 photosynthesis gives a CO2 compensation parable mosses typically have small or narrow cells, with
point an order of magnitude lower than the simple C3 path- apparently rather dense contents and small vacuoles, and have
way, allowing tighter regulation of water loss. C4 plants are readily wetted surfaces, the leaves expanding within a couple
commonly well coupled to the atmosphere so have minimal of minutes from the dried state to their normal moist
need of transpirational cooling; they typically have high opti- appearance on addition of water. Liverworts as a group tend
mum temperatures for photosynthesis, and rather high lethal to favour rather moister habitats than the mosses, but many
temperatures. Crassulacean acid metabolism (CAM) largely are at least moderately desiccation tolerant, some markedly
evades the problems of water loss by temporal separation of so (Clausen, 1952). Porella platyphylla (which grows in dry,
(daytime) photosynthesis and (night-time) CO2 uptake. CAM but usually somewhat shaded situations) showed apparently
plants typically have compact plant bodies which present a complete recovery after 60 days desiccation at 50% rh
limited target to solar radiation and, with their succulence, form (Hinshiri & Proctor, 1971); Frullania dilatata, Gymnomitrion
a substantial heat sink – the big columnar cacti and succulent spp. and other leafy liverworts which commonly grow on
euphorbias are the ultimate expression of this morphology. sun-exposed rocks are likely to be at least as tolerant as this.
As a group, CAM succulents can generally survive higher P. platyphylla has moderate-sized cells, with a large vacuole
temperatures than typical C3 plants (Larcher, 1995a,b). (Marschall et al., 1998). All of these desiccation-tolerant
A final possibility is evolution of true desiccation tolerance. bryophytes are ‘ectohydric’ in the sense of Buch (1945, 1947).
This is very widespread (Crowe et al., 1992), occurring, for Many bryophytes that are at least in some degree desiccation
instance, in nematodes, tardigrades, crustacea (brine shrimps, tolerant show no obvious concession to intermittent drying
etc.), lichens, bryophytes, and vascular plants (spores, pollen, in the form and structure of their cells and leaves, and once
seeds, and mature plants from taxonomically diverse groups), as dry, remoisten comparatively slowly. This is the case, for
well as in numerous microorganisms. Desiccation tolerance instance, in Funaria hygrometrica and some common Bryum
is, in a real sense, the ultimate drought-evading mechanism. species, and in the big Polytrichaceae and Mniaceae. Buch
The plant continues to occupy its physical space in the characterised such bryophytes as ‘endohydric’ or ‘mixohydric’.
habitat, fully developed and ready to resume active meta- A broad (but not sharp) division can be drawn between
bolism and growth when favourable conditions return, while desiccation-tolerant species that withstand long drying better
escaping the need to maintain normal cell function under at low than at higher water contents (usually surviving best
unfavourable conditions of water stress. But this undoubtedly in the range c. −100 to −300 MPa), and those that can toler-
imposes its own morphological limitations, and carries its ate light desiccation but are progressively more damaged as
own physiological price. Desiccation tolerance cuts across water content falls (Fig. 2). The first category, for example
other functional categories. It occurs in heterotrophs and Racomitrium lanuginosum (Dilks & Proctor, 1974) and
autotrophs, in unicellular and multicellular organisms, and in Tortula ruralis (Schonbeck & Bewley, 1981a), match the usual
plants with and without vascular systems and functional sto- situation encountered with seeds in storage. The second
mata. This paper is primarily concerned with the more highly category, for example Plagiothecium undulatum (Dilks &
organised green land plants, bryophytes, pteridophytes and Proctor, 1974) and the species of Fig. 2(a–c), have their
flowering plants, but there are relevant insights to be drawn counterpart in so-called ‘recalcitrant’ seeds (Farrant et al.,
from other organisms too. 1993) which will not withstand drying to low water content.
They grade continuously into desiccation-sensitive species
(e.g. many Hookeriales amongst mosses, many liverworts
III. Desiccation-tolerant plants: taxonomic of moist habitats), which are damaged by even moderate
distribution and functional characteristics drying.
Desiccation tolerance is not an absolute and constant char-
1. Bryophytes
acteristic of a bryophyte species. Some degree of drought
Desiccation tolerance is very common amongst bryophytes, hardening can take place in many if not all (Höfler, 1946;
but varies greatly between species. The greatest degree of Abel, 1956; Proctor, 1972; Dilks & Proctor, 1976; Schonbeck
tolerance is seen in mosses of dry, sun-exposed rock surfaces & Bewley, 1981a), and there is evidence of hormonally
and comparable habitats experiencing extreme desiccation. mediated changes of desiccation tolerance in several species
Andreaea rothii, which grows as small blackish cushions on (Schwabe & Nachmony-Bascomb, 1963 (lunularic acid/
hard, acidic mountain rocks, can recover and photosynthesise Lunularia cruciata); Hellwege et al., 1994 (abscisic acid/
apparently normally after 12 months desiccation at 32% rh Exormotheca)); Bopp & Werner, 1993 (abscisic acid/Funaria
and 20°C. Grimmia pulvinata, a common small cushion moss hygrometrica)), as in some (perhaps most) vascular ‘resurrec-
of dry wall tops, and Racomitrium lanuginosum and Tortula tion plants’ (see Section 6 below). Desiccation-tolerant bryo-
ruralis, abundant and characteristic species, respectively, of phytes will survive much higher temperatures dry than moist,
mountain and subarctic fellfields and dry sand-dune and but survival time is steeply related to temperature (Lange,

Fig. 2 Relation of desiccation tolerance to

desiccation intensity: values of the
chlorophyll-fluorescence parameter FV/FM
20 min (open circles) and 24 h (closed
circles) after re-wetting in (a) Porella
obtusata, East Prawle, Devon, UK (b)
Weymouthia mollis, Otway Range, Vic.,
Australia (c) Anomodon viticulosus,
Chudleigh, Devon, UK (d) Tortula
(Syntrichia) ruralis, Felsötárkány, Hungary
(e) Pleurochaete squarrosa, Chudleigh,
Devon, UK (f) Leucodon sciuroides, Tejeda,
Gran Canaria; (a) (d) and (e) after 60 d
desiccation, (b) (c) and (f) after 30 – 31 d.
1955; Nörr, 1974; Hearnshaw & Proctor, 1982; Meyer & Pteridophytes. Lycopsida. Isoetes (corms only, at least 1
Santarius, 1998). terrestrial sp.), Selaginella (13). Pteropsida. Actiniopteris (2),
Adiantum (1), Anemia (1), Arthropteris (1), Asplenium (8),
Ceterach (2), Cheilanthes (27), Ctenopteris (1), Doryopteris (3),
2. Vascular plants
Hymenophyllum (3), Mohria (1), Notholaena (3), Paraceterach
In vascular plants desiccation tolerance of the vegetative (1), Pellaea (13), Platycerium (1), Pleurosorus (1), Polypodium
tissues has been demonstrated in only some 350 species, (4), Schizaea (1), Woodsia (1).
making up less than 0.2% of the total flora. Lists of the higher Angiosperms. Monocotyledons. Cyperaceae. Afrotrilepis
taxa including DT species are given by Bewley & Krochko (1), Carex (1), Coleochloa (2), Cyperus (1), Fimbristylis (2),
(1982) and Porembski & Barthlott (2000), and a more Kyllingia (1), Mariscus (1), Microdracoides (1), Trilepis (1).
detailed list by Proctor & Pence (2002), but the tally is Liliaceae (Anthericaceae). Borya (3). Poaceae. Brachyachne
constantly being extended. Genera with DT species include (1), Eragrostiella (3), Eragrostis (4), Micraira (5), Microchloa
(number of currently known DT members in parentheses): (3), Oropetium (3), Poa (1), Sporobolus (7), Tripogon (10).

Velloziaceae. Aylthonia (1), Barbacenia (4), Barbaceniopsis (2), resurrection plants typically roll rather than becoming flaccid
Nanuza (1), Pleurostima (1), Vellozia (c. 124), Xerophyta in response to water loss, protecting the more delicate
(c. 28). Dicotyledons. Myrothamnaceae. Myrothamnus (2). desiccated cell walls and giving the plants mechanical
Cactaceae. Blossfeldia (1) (Barthlott & Porembski, 1996). strength; the surface exposed in the dry state is often heavily
Acanthaceae. Talbotia (1), Gesneriaceae. Boea (1), Haberlea pigmented, hairy or scaly (e.g. Ceterach, Fig. 3a–b). The lack
(1), Ramonda (3). Scrophulariaceae. Chamaegigas (1), Crater- of obvious wilting is due to the even shrinking of the
ostigma (3), Ilysanthes (1), Limosella (1), Lindernia (> 15). mesophyll cells and intercellular spaces, compared with the
Lamiaceae. Micromeria (1), Satureja (1). collapse of mesophyll cells and enlargement of intercellular
Desiccation tolerance is thus widely, but thinly and spaces that occurs in sensitive species (Lebkuecher &
unevenly, scattered amongst vascular plants. Virtually all Eickmeier, 1991). Leaf area can decrease by as much as 85%
vascular plants have DT spores (including pollen) or seeds, so the in Craterostigma as the leaves contract and curl during
potentiality for desiccation tolerance is probably universal. desiccation. The leaf cells shrink, preserving the contact
However, its expression in vegetative tissues is rare, and must between plasmalemma and cell wall during desiccation, with
have re-evolved independently in Selaginella, in ferns, and at accordion-like folding of the cell walls (Sherwin & Farrant,
least eight times in angiosperms (Oliver et al. 2000a). In 1996; Hartung et al., 1998). Leaf folding can occur along or
bryophytes it is a reasonable assumption that vegetative perpendicularly to the leaf axis. Ferns and some DT grasses
desiccation tolerance is primitive. In vascular plants it is curl rather than folding. These movements are caused by
clearly a derived condition, and DT vascular plants have often differential imbibition, rather than by osmotic effects (Gaff,
evidently evolved from precursors adapted in other ways to 1989). The remarkable longitudinal zigzag folding of Nanuza
cope with drought. Thus DT angiosperms include species plicata (Velloziaceae) leaves is a result of the alternating
showing some indication of CAM activity or with close reinforced and nonreinforced bands in the epidermis (Rosetto
CAM relatives, and DT and drought tolerant C4 species & Dolder, 1996). The similar contraction of mesophyll
can be found within the same genus (e.g. in Eragrostis and between parallel veins of Xerophyta scabrida (Velloziaceae)
Sporobolus), though DT plants are in general C3. For many during dehydration results in a decreasing specific leaf area,
DT vascular plants, their tolerance can be seen as a fall-back which in turn minimizes water loss (Tuba et al., 1996). Borya
option when ‘homoihydry’ fails. nitida has small, needle-like leaves with cutinised outer
Because of their larger size and greater complexity, DT epidermal walls and stomata confined to longitudinal grooves
vascular plants tend to dry out and rehydrate more slowly than (Gaff & Churchill, 1976). Similar morphology is often seen
bryophytes or lichens. In most cases they have a fully func- in plants tolerant of drought but not of desiccation. Other
tional vascular system which can support the needs of the features traditionally seen as xeromorphic, like leathery or
photosynthetic tissues as long as water is reasonably plentiful. pubescent leaves, sclerenchyma, hairs and scales, also occur
Recovery entails refilling of the xylem to re-establish water among DT ‘resurrection’ plants, but not consistently. They
conduction as well as return to normal cell metabolism. This should be interpreted with the same caution as the
is no great problem for a small plant, in which (given time) ‘xeromorphic’ features of peat-bog Ericaceae, which a century
xylem embolisms can be repaired by root pressure or from ago were explained as adaptations to ‘physiological drought’.
neighbouring tissues when water is freely available. However, It is not possible to be sure from its anatomy whether a plant
a DT tree is hardly conceivable, and the recorded limit for a is desiccation tolerant or not.
DT angiosperm is c. 3–4 m (monocotyledonous pseudo-
shrubs; Porembski & Barthlott, 2000).
2. Questions of scale
Appropriate adaptation depends greatly on scale (Niklas,
IV. Anatomical and physiological requirements 1994). Area increases as the square, and volume (and mass) as
and implications of desiccation tolerance the cube, of linear dimensions. Surface tension operates on
linear liquid–surface contacts and is therefore most effective
1. Morphological adaptation, changes of volume,
and important at small scales. It is a trivial force for large
tissue protection
vertebrates but life-or-death for insects; it plays little part in
Morphological adaptations are important to DT plants both the rise of water up tall trees but is vitally important for lichens
mechanically, and in protection against the deleterious effects and bryophytes. Conversely, effects of gravity are trivial at
of excessive irradiance (Demmig-Adams & Adams, 1992; small scales, but paramount at the scale of large animals or
Björkman & Demmig-Adams, 1995). DT bryophytes mostly trees. Fluid boundary-layer thickness varies as the square
have rather thick cell walls and often look remarkably root of the linear dimensions of an obstruction in the flow.
different wet and dry, exposing much less leaf area in the dry To a first approximation the thickness of the atmospheric
state (Fig. 3c–d). The dry leaves often show regular patterns boundary layer may be thought of as an invariant part of the
of folding and shrinkage (Proctor, 1979a). Leaves of vascular environment as perceived by an individual plant.

Scale thus has profound effects on mechanical and physio- Raven (1999) has emphasised that there is a lower size limit
logical constraints and adaptation in plants. The small size of for homoihydric vascular plants. In fact, the vascular pattern
bryophytes gives them larger cross-section to mass ratios, of adaptation probably ceases to be optimal at a considerably
reducing the need for specialised supporting and conductive larger scale than the limit he suggests, because the vascular
tissues; a bryophyte is similar in scale to an individual leaf or pattern of adaptation only becomes seriously competitive for
root of a vascular plant. Small vascular plants seldom show a plant large enough to tap reserves of water at significant
much secondary thickening; wood is a structural material depth in the soil, and tall enough to create its own individual
evoked by the mechanical needs of trees. Large size both boundary layer above ground.
permits and demands a specialised internal conducting
system. It is among the largest erect-growing mosses (e.g.
3. Water-content components, water storage and
Polytrichaceae, Dawsoniaceae, Mniaceae) that the nearest
water movement in vascular and nonvascular plants
approach to a seed-plant vascular system and seed-plant rigid-
ity are seen. The small size of bryophytes means that surface The water associated with a plant may be divided into several
tension is a powerful force determining the distribution of components. Water inside the plasmalemma is symplast
water around their shoots, and that the shoots and leaves water. Water in the cell walls and intercellular spaces is often
tend to lie within the laminar atmospheric boundary layer. referred to as apoplast water, but this is less satisfactorily
Mass-transfer rates in their immediate vicinity are therefore defined, and various components may be excluded from it. In
dominated by (slow) molecular diffusion rather than (fast) vascular plants it is physically continuous with the xylem sap,
turbulent mixing. Consequently, bryophytes do not in general which often may be better considered separately. Again, for
need to package their photosynthetic systems within a ven- some purposes, intercellular water may be recognised as a
tilated epidermis, although Polytrichaceae, Dawsoniaceae and separate component, distinct from (and much more mobile
Marchantiales demonstrate that they have the evolutionary than) the water in the cell walls (Beckett, 1995, 1997).
potential to produce functional equivalents of vascular-plant Bryophytes generally lack intercellular spaces, but often
leaves. Individual bryophyte leaves are not comparable carry large amounts of (physiologically important) external
physiologically with vascular-plant leaves. A typical bryophyte capillary water (Buch, 1945, 1947; Dilks & Proctor, 1979;
colony is a photosynthetic system on a scale intermediate Proctor et al., 1998). Water may be stored in various parts
between a vascular-plant leafy canopy and a vascular-plant of the soil–plant system, buffering the plant against rapid
mesophyll. At low windspeeds, a higher-plant leaf as a gas- changes in availability of water in the environment. Vascular
exchange system may be compared with the surface of a plants typically rely almost entirely on the store of water in the
smooth bryophyte mat or cushion, in which the surfaces of soil. Halophytes and CAM succulents store large amounts
the individual leaves are functionally a scaled-up mesophyll. of water in the symplast, and symplastic water storage is
Leaf canopies of bryophytes tend to have very high ‘LAIs’ by important in underground storage organs of geophytes,
vascular-plant standards; a few estimates by one of us gave sometimes providing most or all of the water for development
figures of 6 in Tortula (Syntrichia) intermedia, 18 in Mnium of inflorescences during the dry season. The structure of many
hornum and 20–25 in Scleropodium (Pseudoscleropodium) bryophytes favours short-term storage of large quantities of
purum. The higher of these figures are in the same range as external capillary water. Many algae and cyanobacteria have
mesophyll/leaf-area quotients of vascular plants (Nobel, thick gelatinous cell walls or mucilaginous envelopes. Lichen
1974, 1977). At higher windspeeds the bryophyte colony thalli can store substantial amounts of water, generally in
has no close analogue in terms of familiar vascular-plant intercellular or apoplast locations (including the thick
physiology, but is readily comprehensible in terms of the mucilaginous cell walls of Collema and other lichens with
physics of boundary layers, gaseous diffusion and heat Nostoc as photobiont). In all of these nonvascular plants,
balance. Evolution of much of the detailed morphology of much or most of the extracellular water can be lost before
bryophyte shoot systems has probably been driven by selec- water potential falls sufficiently to affect metabolism.
tion pressures balancing movement and storage of water Although conventionally regarded as ‘poikilohydric’, when
against free gas exchange to the leaf surfaces (Dilks & Proctor, they are hydrated they probably experience less variation in
1979; Proctor, 1979a). Carbon isotope discrimination cell water content or water potential than most ‘homoihydric’
measurements of bryophytes (Rundel et al., 1979; Teeri, vascular plants.
1981; Proctor et al., 1992) generally give δ13C figures in the Water movement in a plant may take place entirely through
same range as C3 vascular plants, which suggests that the the symplast, passing from cell to cell through the plasmades-
relation between diffusive and ‘carboxylation’ resistances is mata, or water may pass through the plasmalemma of one cell,
similar in the two groups. This is consistent with the finding across the intervening cell wall, and enter through the plasma-
of Martin & Adamson (2001) that on a per-chlorophyll basis lemma of the other. These have generally been taken to be
photosynthetic rates of bryophytes and vascular plants are relatively high-resistance pathways. The apoplast pathway
similar. through the ‘free space’ of the cell walls and intercellular

spaces commonly shows a lower resistance to water move- rates and integration of metabolic processes during drying
ment, and is generally assumed to be the main pathway within and remoistening; vitrification of the cell contents as water is
the root cortex and the mesophyll of vascular-plant leaves, lost may be important in achieving all of these needs (Crowe
though this assumption has been questioned recently (Steudle et al., 1998; Buitink, 2000; Buitink et al., 2002). The second
& Peterson, 1998). The xylem of vascular plants provides a group includes larger-scale structural adaptations, and, for
pathway of very much lower resistance than either. Although example, metabolic protection against oxidative damage
‘intracellular’ in origin, the lumina of the mature xylem vessels (Smirnoff, 1993; Foyer et al., 1994; Alscher et al., 1997) –
and tracheids are in effect a major extension of the apoplast important to all plants, but a hazard often assumed as likely
pathway with which they are in contact. The hydroids of some to bear more heavily on DT plants during drying and recovery.
large mosses (e.g. Polytrichaceae, Dawsoniaceae, Mniaceae) High concentrations of disaccharide sugars are a common
(Hébant, 1977) are in effect a parallel evolutionary develop- characteristic of DT organisms. Trehalose fills this role in
ment of different ontogeny serving a similar function organisms ranging from bacteria and fungi to nematodes,
(Ligrone et al., 2000). But typically, water movement in brine shrimps and the clubmoss Selaginella lepidophylla Adams
bryophytes is mostly external (Mägdefrau, 1935; Buch, 1945, et al. (1990). Yeast (Saccharomyces cerevisiae) produces little
1947), and many species show elegant external capillary trehalose during rapid growth and is then relatively intolerant
conducting structures (Dilks & Proctor, 1979; Proctor, 1979a). of drying, but trehalose accumulates and dehydration toler-
External capillary water movement is also important in the ance increases in the stationary phase, or following heat shock.
monocotyledon Xerophyta and other Velloziaceae, especially In plants, sucrose is generally the dominant disaccharide that
during the initial stages of remoistening. accumulates in DT cells. Disaccharides stabilise phospholipid
In general, the internal symplastic and apoplastic pathways bilayers by hydrogen bonding to the polar head groups, main-
can support substantial differences in water potential. Despite taining the spacing between them and preventing damaging
recent controversy (Zimmerman et al., 1993; Canny, 1995; phase transitions. Trehalose has also been shown to be effective
Milburn, 1996; Tyree, 1997), there can be little doubt that in stabilising labile proteins during drying (Crowe et al.,
the internal xylem pathway of vascular plants, sealed from 1992), and sucrose has similar effects (Schwab & Gaff, 1990;
the exterior by the surrounding tissues, can also support sub- Bustos & Romo, 1996; Suzuki et al., 1997). By contrast with
stantial negative water potentials – though the water relations the protective effects of the disaccharides, reducing sugars
of trees are probably less simple, and local negative tensions in show a browning reaction with dry proteins, which leads to
the xylem may not be as large, as has been commonly envis- denaturation (Wettlaufer & Leopold, 1991). The possible
aged. The external conducting systems of bryophytes (and stabilising role of linear polyols (Crowe et al., 1998; Buitink
Xerophyta) are dependent on the maintenance of high water et al., 2002), which occur widely in DT (and non DT) liver-
potentials (> c. −0.05 MPa) in their immediate surroundings worts, algae and lichens needs further investigation.
– which must include the cells with which they are in contact. Sucrose levels show marked increases in the course of
dehydration in most DT vascular plants (Albini et al., 1994;
Bianchi et al., 1991, 1993; Müller et al., 1997; Ghasempour
4. What are the fundamental requirements for
et al., 1998). With occasional exceptions, reducing sugars
desiccation tolerance? Why are some species more
decrease or remain at low levels on drying (Koster & Leopold,
tolerant than others?
1988; Bianchi et al., 1991, 1993). Trehalose occurs widely
The minimum requirements for survival of desiccation must in DT plants, but usually at low concentrations, and
include preservation intact of the genetic material, the Ghasempour et al. (1998) found no consistent pattern with
mechanism for protein synthesis, and some essential spatial drying; trehalose seems to be completely absent from such DT
relationships of structures within the cell. Considerations species as Boea hygroscopica and Xerophyta villosa (Bianchi et al.,
of energetics and synthesis capacity in relation to observed 1991; Ghasempour et al., 1998). The carbon source for sucrose
rates of recovery suggest that retention intact of the major synthesis probably varies from species to species. In Craterostigma
structural proteins and enzyme systems should be added to plantagineum the main source is 2-octulose stored in the leaves
that minimal list. (Bianchi et al., 1991; Norwood et al., 2000). Possible sources
The adaptations involved in desiccation tolerance are of in other species include starch (or other carbohydrate) in the
two kinds, those essential to tolerance (without which toler- leaves or other parts of the plant, or photosynthesis during the
ance would not be conceivable), and those that are conse- drying period, but few critical measurements have been made
quences or corollaries of it. In the first group are factors that (Scott, 2000). In bryophytes, the available evidence indicates
preserve the integrity of membranes and macromolecules in that sucrose concentrations remain constantly high, with no
the dry state, and maintain essential spatial relationships increase on drying, but reducing sugars remain at (or decline
within the cytoplasm; this must include ability of cell walls to to) very low levels as the plant dries (Smirnoff, 1992).
shrink or fold without strain as the cytoplasm loses volume on It is generally agreed that disaccharides (and other sugars)
drying. Control must also be maintained over the relative have an essential role in desiccation tolerance, but that other

factors must be important too. The most discussed of these is release of active oxygen species, and that high antioxidant
the part played by proteins and protein synthesis. Two ques- activity to deal with it should be an essential part of the adap-
tions may be asked. Are particular protein molecules an essen- tation of DT plants (Stewart, 1990; Smirnoff, 1993; Navari-
tial part of the equipment of desiccation-tolerant cells?; and, Izzo et al., 1997). Protection against active oxygen species
where and when is protein synthesis important in reinstating produced during normal metabolism is essential to all plants
or repairing cell components damaged or inactivated during (Foyer et al., 1994; Alscher et al., 1997), and up-regulation of
dehydration and re-wetting (Osborne et al., 2002; Walters active oxygen-scavenging enzymes in response to drought is
et al., 2002)? well documented in nonDT plants. However, when responses
At least a partial answer to the first question may be drawn to desiccation are compared, both DT and sensitive species
from analogy with seeds, where late-embryogenesis abundant show stimulation of antioxidant activity at one or another
(LEA) proteins play a major part in establishing the desicca- point in the drying–rehydration cycle but it generally appears
tion tolerance of the mature embryo. LEA proteins (including that oxidative damage in the DT species is well controlled
dehydrins (Close, 1996)) are hydrophilic and resistant to whereas the sensitive species show clear signs of oxidative
denaturation, and fulfil a role in membrane and protein pro- damage (Dhindsa & Matowe, 1981; Seel et al., 1992a,b).
tection parallel with that of the disaccharides. They are also Dhindsa & Matowe found activities of both superoxide dis-
important along with the sugars in maintaining vitrification mutase (SOD) and catalase higher in the DT moss Tortula
of the cell contents; indeed the physical properties of intra- ruralis than in the sensitive Cratoneuron filicinum by a factor
cellular glasses appear to be determined primarily by their pro- of around four. Seel et al. (1992b) found SOD and catalase
tein rather than their sugar component (Buitink et al., 2000, activity substantially higher in (DT) Tortula ruraliformis than
2002). in (sensitive) Dicranella palustris, but activities of peroxidase
In answer to the second question, it is evident that a wide and ascorbate peroxidase (AP) were somewhat greater in the
range of response exists between poikilochlorophyllous DT sensitive than in the DT species; they suggested that the role of
vascular plants such as Xerophyta humilis in which recovery active oxygen-processing enzymes may be less important than
entails extensive protein synthesis (mostly translation of that of antioxidants (tocopherols and glutathione) in deter-
existing transcripts) for reinstatement of the photosynthetic mining desiccation tolerance. Sgherri et al. (1994a) found the
system (Dace et al., 1998), and DT bryophytes of exposed sites activity of glutathione reductase (GR) and dehydroxyascor-
such as Racomitrium lanuginosum or Tortula (Syntrichia) ruralis bate reductase (DHAR) approximately doubled, and that of
in which recovery is essentially complete within an hour or AP halved, in dried leaves of the DT grass Sporobolus stapfi-
two, even in the presence of protein-synthesis inhibitors anus, with a return towards normal levels after 24 h rehydra-
(Proctor & Smirnoff, 2000; Proctor, 2000, 2001). Some tion. The proportion of oxidized ascorbate roughly doubled
(probably many) vascular DT plants fall between these on drying, and doubled again on rehydration, but there was
extremes. Thus Craterostigma wilmsii requires protein syn- little change in the ratio of oxidized to reduced glutathione. In
thesis for full recovery of photosynthetic function if dried fast the dicotyledon Boea hygroscopica (Sgherri et al., 1994b) they
(< 24 h), but not if it dries slowly over several days (Cooper, found total ascorbate doubled and glutathione increased 50-
2001). In all DT plants there is of course likely to be an ongo- fold on drying; activity of GR and DHAR fell markedly on
ing need for some protein synthesis to balance protein degra- drying but AP was little changed. All the variables returned to
dation when partially hydrated (Gaff, 1989). Characteristic normal levels after 24 h rehydration, in both slowly dried
changes in gene expression during desiccation and rehydra- plants which recovered, and rapidly dried plants which did
tion have been reported from vascular resurrection plants not. In Craterostigma wilmsii, Myrothamnus flabellifolia and
including the fern Polypodium virginianum (Reynolds & Xerophyta viscosa Sherwin & Farrant (1998) and Farrant
Bewley, 1993a), the dicotyledon Craterostigma plantagineum (2000) found activity of all three enzymes, AP GR and
(Ingram & Bartels, 1996), the monocotyledon (grass) Spo- SOD increased during at least some phase of the drying–
robolus stapfianus (Gaff et al., 1997; Blomstedt et al., 1998), rehydration cycle, but the detailed pattern of response varied
and in the DT moss Tortula (Syntrichia) ruralis (Oliver, 1996; greatly between species. Thus there is plenty of evidence of
Oliver & Bewley, 1997; Oliver et al., 1998; Wood et al., 1999; responses of antioxidants and antioxidant enzyme systems to
Oliver et al., 2000a). It has been possible to point to a few drying and rehydration, but it is hard to discern any consistent
homologies with proteins of known function in other organ- general pattern. Lebkuecher & Eickmeier (1991, 1993) and
isms (e.g. genes in Craterostigma and Tortula which appear Muslin & Homann (1992) showed that leaf curling in dry
homologous with LEA proteins of seeds, and various meta- Selaginella lepidophylla and Polypodium polypodioides brings
bolic enzymes), but the function of most of these genes is clear benefits in limiting photodamage during rehydration in
unknown and relating them to processes involved in desicca- bright light, but their results do not suggest any fundamental
tion tolerance remains a research challenge for the future. differences from nonDT plants. Over all, the evidence suggests
It is widely considered that cell damage and metabolic that DT plants generally deal with the potential hazards of
disruption during drying and rehydration must exacerbate oxidative damage during the drying–re-wetting cycle by

anticipating the problem at source rather than by invoking extra- Poikilochlorophylly is currently known in eight genera of four
vagantly high activity of antioxidant enzymes or antioxidants families (Cyperaceae, Liliaceae (Anthericaceae), Poaceae and
after the event. Protective mechanisms include leaf and stem Velloziaceae). Most occupy the almost soil-less rocky outcrops
curling, heavy anthocyanin pigmentation (Sherwin & Farrant, known as inselbergs, in strongly seasonal subtropical climates
1998; Farrant, 2000), progressive reduction of molecular (Porembski & Barthlott, 2000); the best studied physio-
mobility and controlled down-regulation of metabolism on logically are the African Xerophyta scabrida, X. viscosa and
drying (Hoekstra et al., 2001), and high levels of zeaxanthin- X. humilis and the Australian Borya nitida (Gaff & Churchill,
mediated photo-protection (Demmig-Adams & Adams, 1992; 1976; Hetherington & Smillie, 1982a,b; Hetherington et al.,
Eickmeier et al., 1993; Björkman & Demmig-Adams, 1995) 1982a,b; Gaff & Loveys, 1984; Tuba et al., 1993a,b, 1994, 1996;
manifested in chlorophyll-fluorescence measurements as high Sherwin & Farrant, 1996; Dace et al., 1998; Farrant, 2000;
levels of (quickly relaxing) NPQ (Csintalan et al., 1999; Cooper, 2001).
Marschall & Proctor, 1999; M.C.F. Proctor, unpublished). A HDT plants preserve much or all of their chlorophyll
fuller discussion of active oxygen and antioxidant systems in through a drying–re-wetting cycle. The fern Pellaea
relation to desiccation tolerance is given by Smirnoff (1993), calomelanos retains chlorophyll and chloroplasts with discern-
and further references will be found in Walters et al. (2002). ible grana when dry (Gaff & Hallam, 1974). DT dicotyle-
dons, although all retaining chlorophyll, vary in the details of
their behaviour. In the southeast-European HDT Gesne-
5. Homoichlorophylly and poikilochlorophylly
riaceae Haberlea rhodopensis and Ramonda serbica, Markovska
Vascular DT plants fall into two groups depending on the et al. (1994) found no significant changes in chlorophyll con-
degree to which they retain their chlorophyll when dry. tent on drying and re-wetting, but Drazic et al. (1999) found
Homoiochlorophyllous (HDT) species retain their photo- that Ramonda nathaliae lost 20% of its chlorophyll when
synthetic apparatus and chlorophylls in a readily recoverable desiccated in the glasshouse and 70% in natural habitats;
form. Poikilochlorophyllous (PDT) species dismantle their Myrothamnus flabellifolia preserves its thylakoids but loses
photosynthetic apparatus and lose all of their chlorophyll half its chlorophyll on drying (Farrant et al., 1999). The extent
during drying; these must be resynthesised following rehydra- of chlorophyll loss in dicotyledons thus varies from species to
tion (Tuba et al., 1994; Sherwin & Farrant, 1996; Tuba species, and may be influenced by environmental factors. By
et al., 1998). The phenomenon of loss of chlorophyll during contrast, Xerophyta scabrida, a characteristic PDT plant, loses
desiccation was first described by Vassiljev (1931) in Carex all its chlorophylls and dismantles apparently all of the inter-
physoides from central Asia; the concept was reintroduced nal structures of the chloroplast during desiccation (Tuba
and the terms homoichlorophylly and poikilochlorophylly et al., 1993a,b).
coined by Hambler (1961), and it was regarded as a special Desiccation-induced breakdown of the photosynthetic
case in certain DT monocotyledonous plants (Hambler, apparatus in PDT plants is different from the processes
1961; Gaff & Hallam, 1974; Gaff, 1977, 1989; Bewley, involved in leaf senescence. Indeed Gaff (1986) found that
1979; Hetherington & Smillie, 1982a,b). senescence reduced desiccation tolerance. The dismantling of
The HDT strategy is based on the preservation of the the photosynthetic apparatus can be seen as a strictly organ-
integrity of the photosynthetic apparatus by protective mech- ized protective mechanism, rather than ‘damage’ to be
anisms considered in earlier sections of this review. The PDT repaired after rehydration. If the PDT Borya nitida is desic-
strategy evolved in plants which are anatomically complex cated rapidly, it does not have the time to break down chloro-
and which include the biggest in size of all DT species, and it phyll and loses viability (Gaff & Churchill, 1976) and the
can be seen as the evolutionarily youngest strategy. It is based same is true of Xerophyta humilis (Cooper, 2001). Chlorophyll
on the dismantling of internal chloroplast structure by an breakdown in Borya nitida does not appear to be controlled by
ordered deconstruction process during drying, and its resyn- abscisic acid (ABA) (Gaff & Loveys, 1984), and Xerophyta
thesis upon rehydration by an ordered reconstruction process. scabrida preserves most of its chlorophyll when desiccated in
These processes can thus be thought of as not only being the dark, so most of the loss seems to be a result of photooxi-
superimposed on an existing cellular protection mechanism dation under natural circumstances (Tuba et al., 1997). This
of vegetative desiccation tolerance (Oliver et al., 2000) but suggests that PDT plants in general probably do not decom-
as a distinct new DT strategy (Tuba et al., 1994; Tuba et al., pose their chlorophyll enzymatically, but rather do not invest
1998). The selective advantage of poikilochlorophylly, in in preserving it through the dry state. However, dismantling
minimising photo-oxidative damage and not having to main- of the thylakoid membranes is strictly organized and leads to
tain an intact photosynthetic system through long inactive the formation of nearly isodiametric ‘desiccoplasts’, which,
periods of desiccation, presumably outweighs the disadvant- unlike chromoplasts, are able to regreen and photosynthesise
age of slow recovery and the energy costs of reconstruction. after rehydration (Tuba et al., 1993b). Desiccoplasts contain
Taxonomically the PDT plants appear to be restricted to granular stroma, a couple of translucent plastoglobuli possibly
the monocots (Gaff, 1977, 1989; Bewley & Krochko, 1982). containing lipoquinones and neutral lipids. The thylakoid

material is not arranged in plastoglobuli but can be found as these conditions it is evidently more advantageous to dis-
osmiophilic lipid material stretched in the place of the former mantle the whole photosynthetic apparatus and reconstitute
thylakoids (Tuba et al., 1993b). In X. villosa not only chloro- it after rehydration. Of course there is variation within each
plast internal membranes but even most of the mitochondrial category and the categories overlap in their ecological adapta-
cristae disappear on dehydration and the remaining ones tion, and two or more may coexist in one habitat, for example
appear to decompose within 30 min after rewetting. This is on inselbergs (Ibisch et al., 1995). Both ends of this ecological
mirrored by a loss in insoluble or structural proteins (almost spectrum have particular points of interest. There is probably
50%), which is much less marked (generally c. 10%) in HDT a trade-off between the ‘cost’ of protection and repair to the
plants (Gaff & Hallam, 1974). photosynthetic apparatus if this is kept in a quickly recover-
On re-wetting X. scabrida, reconstruction of thylakoids has able state through prolonged periods of desiccation, and the
already begun by the time the tissue has reached full satura- ‘cost’ of reconstituting the photosynthetic apparatus de novo.
tion. Chlorophyll synthesis starts 8–10 h after rehydration
(Tuba et al., 1993a). In this process, osmiophil lipid material
6. Constitutive and induced tolerance
is used up. Primary thylakoids with a small stacking ratio
make up an intermediate step in resynthesis. Regeneration of In the bryophytes and lichens of habitats that frequently
the photosynthetic apparatus is complete within 72 h after dry out, desiccation tolerance appears to be essentially
rewetting. The restitution of cristae in mitochondria was constitutive and influenced to only a limited extent by
faster than that of chloroplast internal membranes. Net CO2 previous desiccation history or rate of drying. Recovery
assimilation was first measurable after 24 h rehydration. At takes place quickly, and depends essentially on reactivation of
this point, chlorophyll content was just 35% of that in fully components conserved undamaged through the drying–re-
active control plants (Tuba et al., 1993b). wetting cycle. By contrast, in DT angiosperms tolerance is
CO2 gas-exchange of desiccating Xerophyta scabrida leaves generally induced in the course of slow drying (Gaff, 1980,
was studied by Tuba et al. (1996, 1997). Photosynthetic activ- 1989, 1997). These plants may tolerate severe and prolonged
ity declined steeply to zero through the first 4 d of drying. By desiccation under appropriate conditions, but show little or
this time the leaves had lost approx. 60% of their water con- no tolerance if they are dried rapidly. This antithesis may
tent. The fall in net CO2 assimilation was caused mainly by at least in part reflect different evolutionary origins of
the rapid stomatal closure, but it was the decrease in chloro- desiccation tolerance, primitive in bryophytes (and lichens),
phyll content (as shown by the fluorescence signal) that finally secondary and polyphyletic in vascular plants (Oliver et al.,
brought photosynthesis to a halt. Dark respiration continued 2000a), where it has probably often evolved as a fall-back in
until the 14th day of dehydration, at 24% of the original plants already more or less tolerant of drought stress. Slow
water content. The declines in water content and respiration drying is a natural consequence of the vascular-plant habit,
were closely correlated. The prolonged respiration during and in some cases elements of the induction process are
desiccation may cover the energy demand of controlled dis- obvious, as in the conversion of 2-octulose to sucrose in
assembly of the internal membrane structures in PDT plants Craterostigma, and the controlled dismantling of the
(Tuba et al., 1997). In rehydrating Xerophyta scabrida leaves, photosynthetic system in Borya and Xerophyta. However, the
respiratory processes are fully operational before full turgor antithesis is not clear-cut. Leaf cells of mosses in exposed
is achieved (Tuba et al., 1994); fast recovery of respiration is sunny situations switch from full turgor to air dryness with a
important as the only ATP-source during the primary phase few minutes, but many forest bryophytes dry much more
of rehydration (Gaff, 1989). A high initial respiration rate on slowly, and a degree of drought hardening is readily
re-moistening, so called ‘resaturation respiration’ (Smith & demonstrated (Höfler, 1946; Abel, 1956; Proctor, 1972;
Molesworth, 1973), is seen in lichens, bryophytes and HDT Dilks & Proctor, 1976). Also, desiccation tolerance appears to
vascular plants, but this elevated rate persists much longer in be essentially constitutive in various small saxicolous ferns
PDT species – 30 h in the case of X. scabrida (Tuba et al., (Hymenophyllym tunbrigense, H. wilsonii, H. sanguinolentum,
1994). Asplenium trichomanes, A. ruta-muraria) and Selaginella
The HDT and PDT strategies solve the same ecological species (S. cf. underwoodii) which can dry out and recover as
problem, but cover a broad temporal range of adaptation. The quickly as many bryophytes (Kappen, 1964; M.C.F. Proctor,
HDT pteridophytes and angiosperms are generally adapted to unpublished). These species dry out quickly once water
longer drying–wetting cycles than bryophytes and lichens, becomes limiting, and show no conventional adaptations to
but to more rapid alternations of wet and dry periods than conserve water within the plant, a habit probably related to
the PDT monocot species (Schwab et al., 1989; Ingram & the high temperatures reached in their saxicolous habitats in
Bartels, 1996; Sherwin & Farrant, 1996; Tuba et al., 1998), the absence of evaporative cooling. By contrast the taller (and
though some can survive dry for very long periods of time. often epiphytic) polypody ferns (Polypodium vulgare agg.)
The PDT strategy has evolved in habitats where the plants show strong stomatal control over water loss and dry out
remain in the desiccated state for 5–8(−10) months. Under slowly (Lange et al., 1971; M.C.F. Proctor, unpublished).

It is generally accepted that ABA produced in roots under Mniaceae, imbibition is slower and may take an hour or two
water stress induces various drought responses in vascular to complete even when liquid water is present. The water-
plant shoots (Schulze, 1986; Zeevaart & Creelman, 1988). conducting hydroids of mosses collapse without embolising
Molecular-biological evidence (Ingram & Bartels, 1996) has on drying ( J.G. Duckett, pers. comm.), so they are able to
tended to confirm earlier speculation that ABA may have a refill immediately through their lateral walls as the stem re-
general role in evoking desiccation tolerance in DT plants. imbibes water.
However physiological evidence for this is equivocal. Chamae- Vascular resurrection plants in general require liquid water
gigas intrepidus and Craterostigma lanceolatum increased their for rehydration (Gaff, 1977), and the continuity of water
ABA content 20–30-fold on drying (Schiller et al., 1997). On within the xylem must be restored as the tissues rehydrate if
the other hand, ABA concentration did not increase in drying the leaves are to remain turgid for more than a few hours after
leaves of Polypodium virginianum, but exogenous ABA rain. Embolism in xylem vessels has been assumed to hinder
enhanced survival of rapid drying (Reynolds & Bewley, resaturation of the photosynthetic tissues in some species
1993b). Gaff & Loveys (1984) found a substantial rise in ABA (Sherwin & Farrant, 1996). The fact that resurrection plants
levels (along with increased desiccation tolerance) in detached are generally low herbs or shrubs (Gaff, 1977; Kappen &
leaves of both (homoichlorophyllous) Myrothamnus flabellifo- Valladares, 1999) is consistent with the idea that restitution of
lia and (poikilochlorophyllous) Borya nitida equilibrated at xylem transport is a real challenge for these plants, and prob-
96% rh; cell survival was significantly promoted by exogenous ably imposes a practical limit on their height. If normal func-
ABA without concurrent water stress in B. nitida, and slightly tion of the vascular system is to be re-established, it is vital that
so in M. flabellifolia. In the grass Sporobolus stapfianus the vascular bundles remain essentially undamaged in the des-
isolated leaves became DT only if detached below 61% relative iccated state. Rosetto & Dolder (1996) found that vascular
water content (RWC), but ABA peaked in shoots at 15% bundles of the desiccation tolerant Nanuza plicata showed no
RWC, and originated in the leaves rather than the roots (Gaff significant changes due to dehydration. By contrast, drought
& Loveys, 1992). In the same species, Ghasempour et al. (1998) stress severely impaired vascular bundles in nonDT barley
found desiccation tolerance was promoted only marginally by leaves (Pearce & Beckett, 1987), which would preclude the
exogenous ABA, whereas brassinolide and methyljasmonic reestablishment of water flow even if all the other factors nec-
acid had much larger effects. In the DT thalloid liverwort essary for rehydration were present. In Myrothamnus flabelli-
Exormotheca holstii, high levels of ABA went with high folia, a DT shrub with a height of at most a few decimetres
desiccation tolerance under field conditions, ABA level and (Figs 3g and 4a), Sherwin et al. (1998) considered capillary
desiccation both declining under well-watered cultivation, but rise in the narrow reticulate xylem vessels sufficient to achieve
desiccation tolerance could be restored by exogenous ABA continuity of water column, but Schneider et al. (2000) and
(Hellwege et al., 1994). Tolerance of water stress was increased Wagner et al. (2000) presented evidence that root pressure is
significantly by ABA treatment even in the aquatic thalloid implicated in the initial filling of a proportion of xylem ele-
liverwort Riccia fluitans (Hellwege et al., 1996). Similar effects ments, water then moving radially in a complex manner into
of ABA in promoting desiccation tolerance have been found the adjacent xylem and other tissues. In Pellaea calomelanos,
in protonema of the moss Funaria hygrometrica (Werner et al., Gaff & Hallam (1974) found capillary rise unable to trans-
1991; Bopp & Werner, 1993) and leafy shoots of Atrichum port water even into the lowest leaves, and concluded that
androgynum (Beckett, 1999). In the highly DT moss Tortula root pressure must also play a part. In Borya nitida, the leaves
ruralis ABA is undetectable (Oliver et al., 1998). A systematic on the upper half of the shoots had still not rehydrated from
search for endogenous ABA in bryophytes is much needed. the soil after 6 d (Gaff & Churchill, 1976), so in this case
rehydration through the leaf cuticle seems also to be essential.
Xerophyta scabrida roots die back when desiccated, therefore
7. Recovery; re-establishment of water-relations
rehydration can only occur via the leaves. In this species leaf
and metabolism
turgor is regained within 6 h and maximum water content
Highly DT bryophytes growing in exposed situations after 12 h in immersed leaves (Tuba et al., 1994). After re-
typically re-moisten quickly and diffusely. The thin leaves establishment of metabolism in the leaves, adventitious roots
of bryophytes (and lichen thalli and algal mats) equilibrate develop and ensure continuous water supply (Tuba et al.,
rapidly with the humidity of the surrounding air, and can 1993a). The relative importance of the water received by the
regain turgor from overnight dewfall even if no obvious roots and water absorbed through leaves varies from species to
deposition of liquid water has taken place (Lange et al., 1968, species (Gaff, 1977).
1990, 1991, 1994; Csintalan et al., 2000). Liquid water from In desiccation-tolerant mosses that have been air dry for a
rain or cloudwater deposition is imbibed by the leaves directly few days, respiration recommences almost instantaneously on
as it spreads by capillarity over the surface of the shoots. In remoistening and net photosynthetic carbon fixation typically
species with well-developed internal conduction and water- reaches two-thirds or more of normal levels within the first
repellent leaf surfaces, such as many large Polytrichaceae and few minutes. The initial respiratory carbon loss is typically

made good within 30 min or so (Tuba et al., 1996; Proctor & can dry from full turgor to a water content of 10% d. wt or
Pence, 2002) Chlorophyll-fluorescence measurements show less within 30 min without damage, and return to a near-
that initial recovery of the photosystems is extraordinarily normal rate of net CO2 fixation within a similar time on
rapid, and independent of protein synthesis (Csintalan et al., remoistening. Lichens of comparable habitats respond
1999; Proctor & Smirnoff, 2000). Complete return to similarly fast (Ried, 1960a,b; Lange, 1988; Tuba et al., 1996);
unstressed levels of fluorescence parameters may take a indeed some lichens of exposed rock surfaces seem able to
number of hours, but is unaffected by protein-synthesis ‘switch’ on and off within a minute or two (e.g. Rhizocarpon
inhibitors in the dark. There are indications that some cyto- geographicum, Fig. 5a). However, even amongst bryophytes of
plasmic protein synthesis following remoistening is needed relatively open habitats, many species respond more slowly;
for return to predesiccation levels of CO2 fixation (Proctor & substantial differences are apparent in the rate of recovery of.
Smirnoff, 2000), but this may be ‘maintenance’ repair of the chlorophyll-fluorescence parameter FV/FM following re-
ongoing photo-damage during recovery in light, rather than moistening (Fig. 5b; Proctor, 2001). Forest-floor bryophytes
the repair of damage from desiccation. Over all, the results such as Rhytidiadelphus loreus (Dilks & Proctor, 1976; Proctor
suggest that recovery of respiration and photosynthesis in & Smirnoff, 2000), Mnium hornum or Polytrichum formosum,
these plants is largely a matter of reassembly and reactivation experiencing higher ambient humidity and lower windspeeds
of components which have survived drying and re-wetting and net radiation exchange, dry out relatively slowly, and full
essentially intact. A substantial ‘repair’ element in the recovery recovery of normal rates of photosynthesis may take many
of DT bryophytes was suggested by Bewley (1979) and hours. Drying and recovery rates do not necessarily correlate
Bewley & Krochko (1982) primarily in relation to restoration with either relative tolerance of different intensities of
of membrane integrity. Oliver & Bewley (1984, 1997) postu- desiccation or with maximum survival times.
lated that desiccation tolerance in ‘fully DT plants’ (primarily Vascular DT plants typically dry out and re-moisten on a
bryophytes) is essentially ‘repair based’, while that in ‘modi- longer time scale than bryophytes and lichens, but there is
fied DT plants’ (vascular plants) is based on inducible ‘protec- much overlap between the two groups (Fig. 6). The filmy
tion’ systems set in place in the course of slow drying. This ferns (e.g. Hymenophyllum spp.) behave much like bryophytes
division broadly reflects the phylogenetic distribution of DT of similar sheltered humid habitats; they lose and absorb water
plants (Oliver et al., 2000a), but its value depends heavily on readily over the whole leaf surface and water conduction by
how ‘repair’ is defined – and it underplays not only the wide the vascular system is limited (Härtel, 1940); they recover
range of behaviour within both bryophytes and DT vascular remarkably quickly from periods of a few days dry (Fig. 6). In
plants and the speedier recovery of many bryophytes, but also the field there is probably rather little difference between rates
the features in common between the two groups. Leakage of of drying and recovery of bryophytes such as Polytrichum,
membranes for a short time after re-wetting occurs in all Dawsonia or the big Mniaceae, and some species of Selaginella
desiccation-tolerant organisms (Crowe et al., 1992), and ‘repair’ and small DT ferns such as Polypodium polypodioides (Stuart,
processes in the limited sense originally envisaged by Bewley 1968) or Asplenium trichomanes (Fig. 6). However, drying and
must be common to all DT plants. Indeed the greatest com- recovery rates of vascular DT plants are generally slower. Cra-
mitment to repair is seen in the poikilochlorophyllous vascu- terostigma wilmsii regains substantially normal photosynthetic
lar plants where much of the photosynthetic system must be function within 24 h; the woody Myrothamnus flabellifolia
rebuilt each time the plant dries out. Much further research requires rather longer (Fig. 6b; Sherwin & Farrant, 1996).
is needed on the distribution and mechanisms of inducible Recovery of PDT plants is slower again. Xerophyta spp. (Vel-
desiccation tolerance in both bryophytes and vascular plants. loziaceae) generally need 3–4 d to re-establish fully normal
Oliver and colleagues have reported the synthesis of many metabolism (Fig. 6b; Sherwin & Farrant, 1996; Dace et al.,
rehydration-specific proteins in Tortula ruralis (Oliver, 1991; 1998; Tuba et al., 1998). Borya nitida (Liliaceae (Antheri-
Oliver et al., 1998; Wood et al., 1999; Oliver et al., 2000b), caceae); Gaff & Churchill, 1976) and Eragrostis nindensis
and this too is an area in which we may expect interesting (Poaceae; Vander Willigen et al., 2001) recover on a similar
developments in the future. time scale).
Taking DT plants as a whole, we thus see a wide spectrum
of time responses to alternating wet and dry periods. At the
V. Time-scale considerations and ecological ‘low-inertia’ end are the lichens and bryophytes of exposed
adaptation situations, responding within minutes to rapid changes of water
content. At the ‘high-inertia’ end are the PDT vascular plants,
1. The time scale of drying–wetting cycles: low-inertia
adapted to an essentially predictable annual ‘wet-season–dry-
and high inertia responses
season’ pattern in which quick response to brief dry spells or
Rates of both water loss and rehydration vary enormously isolated showers would be counterproductive, and times of
between different DT plants. Mosses of exposed situations response to drying and re-wetting are measured in days. A
such as Tortula (Syntrichia) ruralis or Grimmia pulvinata majority of DT plants lie somewhere between these extremes.

Fig. 3 (a) The desiccation tolerant (DT) fern Ceterach officinarum fully hydrated and metabolically active, and (b) dry during summer, with the
leaves tightly rolled and the densely scaly undersides exposed. Chudleigh, Devon, UK. (c) Tortula (Syntrichia) intermedia, a DT moss (above)
fully hydrated, and (below) dry. Chudleigh, Devon, UK. (d) The DT moss Leptodon smithii; (above) hydrated and fully expanded, and (below)
dry, with the shoot systems tightly rolled in characteristic balls recalling the growth habit of Selaginella lepidophylla. Locronan, Brittany, France.
(e) Xerophyta retinervis, a tall (c. 2 m) member of the Velloziaceae, seen here fully hydrated with green leaves, in open seasonally dry forest,
Itala Game Reserve, KwaZulu-Natal, South Africa. (f) Xerophyta villosa, a lower-growing species, on sun-exposed rock outcrops, here hydrated
and green. Itala Game Reserve, KwaZulu-Natal, South Africa. (g) The DT shrublet Myrothamnus flabellifolia, hydrated, with fully expanded
leaves. Louwsburg, KwaZulu-Natal, South Africa. (For photographs of Craterostigma in hydrated and desiccated states see Bernacchia et al.
(1996); Bohnert (2000); Scott (2000)).

Fig. 4 (a) Habitat of Myrothamnus flabellifolia, Cheilanthes sp. and Selaginella dregei over flat-bedded sandstone slabs near Louwsburg,
KwaZulu-Natal, South Africa. (b) Sandy dry grassland near Fülöpháza, Hungary; the desiccation tolerant (DT) moss Tortula ruralis carpets much
of the ground under the sparse grass cover. (c) ArnavatnsheiDi, C. Iceland: the DT moss Racomitrium lanuginosum dominant on stony slopes
in foreground (with yellowish DT lichens, Alectoria sp.), and giving its grey-green colour to much of the rest of the landscape. (d) Lichen field
dominated by the orange DT lichen Teloschistes capensis, near Cape Cross, Namibia. (e) Quercus robur wood under high rainfall, Black Tor
Copse, Devon, UK; DT mosses and lichens cover almost every available surface. (f) Cool-temperate rainforest, Newell Creek, SW Tasmania;
dense DT bryophyte cover on trunks, branches and fallen logs.

Fig. 5 Recovery rates in lichens and bryophytes. (a) A saxicolous

lichen of exposed situations, Rhizocarpon geographicum: recovery of
chlorophyll-fluorescence parameters following re-wetting (arrow) Fig. 6 Recovery rates in vascular desiccation tolerant (DT) plants,
after 18 d dry (c. −100 MPa); FV/FM is at high levels throughout, and re-plotted for comparison as percentage of maximum value (FV/FM
FM reaches half its maximal value within 10 min Plotted points are or PS) attained on full recovery. (a) Three pteridophytes and a
mean ± s.d. (n = 2). (b) Recovery of FV/FM in three mosses after 10 – homoichlorophyllous dicotyledon: Hymenophyllum wilsonii,
16 d dry (c. −100 MPa): Racomitrium lanuginosum, Holne, Dartmoor, UK (15 d dry); Asplenium trichomanes, Chudleigh,
Dartmoor, UK; Polytrichum formosum, Exeter, Devon, UK; Mnium Devon UK (8 d dry); Selaginella cf. underwoodii, Utah (8 months
hornum, Salcombe Regis, Devon, UK. For rapid recovery of mosses dry); Craterostigma wilmsii, South Africa (Sherwin & Farrant,
from short periods of desiccation see Proctor & Smirnoff (2000), 1996, > 1 month dry). (b) On a longer time scale, a pteridophyte,
Proctor (2001, 2002). two homoichlorophyllous dicotyledons, and a poikilochlorophyllous
monocotyledon; H. wilsonii and C. wilmsii as in Fig. 6(a) above;
Myrothamnus flabellifolia, South Africa (Sherwin & Farrant,
1996, > 1 month dry); Xerophyta scabrida, Tanzania (Tuba et al.,
2. Desiccation tolerance in an ecological and 1998, several months dry). Original data unless otherwise indicated.
biogeographical context
What are the situations in which desiccation tolerance is an
adaptive optimum? Obviously, the habitat must be at least when the rain stops. In all but extreme arid climates, DT
intermittently dry. It must also at least sometimes be wet, and lichens and bryophytes colonise the surfaces of rocks and the
the wet periods should be at least predictably seasonal and the bark of trees. Crustose lichens (together with some species of
dry periods not too long. Many DT bryophytes and vascular foliose and fruticose growth form) occupy bare rock surfaces
plants can survive dry for 6 months or a year (sometimes from the polar regions to the equator, a mosaic of individual
more) but in general they do not remain viable as long as thalli of various species often completely covering the rock.
seeds, so the optimum niches for DT plants and desert Bryophytes are relatively more prominent in oceanic regions.
ephemerals are different. ‘Dryness’ may arise from two causes. Vast tracts of lava desert and stony morainic ground in the
In even the wettest climate it does not rain continuously, and cold rainy climate of Iceland, and boulder fields on mountain
hard substrates impenetrable to roots quickly become dry summits in Scotland and Scandinavia, are dominated by

the moss Racomitrium lanuginosum (Fig. 4c), and bryophytes poikilohydry and homoihydry, but between plants that are
cover every available surface in humid forests in temperate desiccation tolerant and those that are not – and, over the
hyperoceanic regions (Fig. 4e,f ) and at high altitudes in the whole range of DT plants, this is broadly associated with the
humid tropics. All of these plants must be able to endure contrast between ectohydry and endohydry as the predominant
periods of at least a few days desiccation. Even some DT mode of water movement. Many ‘poikilohydric’ bryophytes
vascular plants (e.g. Ceterach officinarum (Fig. 3a,b), maintain a rather constant water content and are sensitive to
Asplenium trichomanes, Polypodium vulgare) reach into humid drying, and all DT vascular plants are ‘homoihydric’ under
temperate regions as epiphytes or on rock outcrops. In favourable conditions. Despite some argument to the contrary
seasonally arid habitats the growth of nonDT vascular plants in particular groups (Schuster, 1984) bryophytes in general
is limited by seasonal drought; bryophytes, lichens and must certainly be primitively desiccation tolerant; all are C3
vascular ‘resurrection plants’ are often prominent in such plants and they show few of the characteristics associated with
places, especially where the soil is shallow and nutrient poor; drought tolerance in vascular plants. Virtually all vascular
carpets of Tortula ruralis and other mosses commonly form an plants have desiccation-tolerant spores, pollen or seeds, but
understorey to the thin cover of grasses on stabilising Atlantic- expression of desiccation tolerance in vegetative tissues has
coast dunes, or in dry sandy steppe grasslands in central and evidently evolved (or re-evolved) independently a number of
eastern Europe (Fig. 4b), and in comparable habitats in other times (Oliver et al., 2000a), probably in most cases from
parts of the world. These two broad habitat types – rock (and ‘homoihydric’ but drought-tolerant antecedents. Accordingly,
bark) surfaces and thin drought-prone soils – intergrade, and DT vascular plants, although themselves generally (perhaps
some of the most characteristic situations for DT plants are invariably) C3 species, often have relatives showing C4
on thin soils over and around rock outcrops in such areas as adaptation. A few even show indications of CAM behaviour
central and southern Africa (Fig. 4a), tropical South America or are closely related to CAM species (Barthlott & Porembski,
and Australia; indeed the tropical inselbergs of South America 1996; Markovska et al., 1997). DT bryophytes and vascular
and Africa are the principal centres of diversity for DT plants are not simply an odd sideline from mainstream
vascular plants (Porembski & Barthlott, 2000). Arid regions homoihydry. They are an adaptive optimum in particular
can be notably diverse in their plant life forms (Ehleringer, ecological situations, and (like ‘normal’ vascular plants) can be
1995; Ehleringer et al., 1999), and DT plants often coexist understood fully only in the context of a wide and multidi-
with plants of other adaptive types, especially therophytes mensional field of physiological and ecological possibilities.
(adapted to seasonal drought by DT seeds rather than
DT vegetative tissues), CAM plants, and in tropical and
subtropical climates C4 grasses. In general they do not
Acknowledgements
occur in true deserts with very low and unpredictable We are indebted to many colleagues for answering queries and
rainfall, with the interesting exception of those coastal deserts for helpful discussion, and to Dr C.J. Proctor for help with
where cloudwater deposition from fog provides enough scanning and editing the colour photographs. The support to
moisture for lichen growth, as in the extensive stands of Z.T. of a DAAD (Bonn) Professorial and a NATO Senior
Teloschistes capensis along the coast of Namibia (Fig. 4d; Lange Fellowship at the Department of Botany II (University of
et al., 1990). Karlsruhe) is greatfully acknowledged.
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NPH_526.

fm Page 327 Thursday, November 7, 2002 4:07 PM

Tansley review no. 141

Poikilohydry and homoihydry: antithesis

Author for correspondence: Michael C. F. Proctor1 and Zoltán Tuba2

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I. Introduction 2. The vascular-plant strategy

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pathways, one via the variable resistance of the stomata (of

Fig. 1 Resistance to water flow in (a) a

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rather than lack of regulation of water loss. External rather

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Fig. 2 Relation of desiccation tolerance to

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Fig. 5 Recovery rates in lichens and bryophytes. (a) A saxicolous

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VI. Conclusion References

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About New Phytologist

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