Download Physiological correlates of the morphology of early vascular plants

Botanical Journal of The Linncan So&& (1984),88: 105-126
Physiological correlates of the morphology
of early vascular plants
JOHN A. RAVEN
Department of Biological Sciences, University of Dundee, Dundee DDl 4HN
Received January 1983, acceptedfor publication A U ~ U 1983
S~
RAVEN, J. A,, 1984.Physiological correlates of the morphology of early vascular plants. The early
evolution of vascular land plants is considered in relation to the physiological problems of life on
land. The universal characteristics of vascular plants (xylem, cuticle, stomata, intercellular air
spaces, long-distance symplastic transport and alternation of generations) are discussed in terms of
the essential properties of a homoiohydric phototroph. Likely precursors of vascular plants, and the
physico-chemical and biotic environment in which they occurred, are outlined prior to a discussion
of the selective forces acting on the evolution of vascular plants in the Upper Silurian and Lower
Devonian. Emphasis is placed on biochemical and structural ‘pre-adaptations’ which may have
occurred in the precursors of vascular plants and on which natural selection could have acted with
lignified xylem, stomata, etc., as the end-products. Guiding principles in the analysis include the
physiology of extant plants, physico-chemical constraints, and compatibility with the fossil record.
I t is concluded that the likely sequence of acquisition of vascular plant characteristics was:
heteromorphic alternation of generations with an erect sporophyte; cuticularization of sporophyte;
evolution of xylem; occurrence of intercellular air spaces with pores in the epidermis; stomata1
activity of the pores. Endodermis and phloem-type long-distance transport probably originated
around stages (3)-(5).
KEY WORDS:-Cuticles - Devonian - endodermis - homoiohydry - intercellular air spaces lignin - non-vascular land plants - phloem - Silurian - stomata - vascular land plants - xylem.
CONTENTS
Introduction . . . . . . . . . . . . . . . . . . .
The vascular condition.
. . . . . . . . . . . . . . . .
The physico-chemical and biotic environment of the early evolution of vascular plants .
How vascular plants may have arisen . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . . . . . .
Acknowledgements
. . . . . . . . . . . . . . . . .
Appendix 1: T h e relative specific H,O conductance of parenchyma and xylem tissues .
Appendix 2: T h e H,O loss associated with photosynthetic CO, fixation in a terrestrial
plant . . . . . . . . . . . . . . . . .
Appendix 3: The significance of exposing large areas of cell surface to the gas phase in
relation to the plant’s investment in RUBISCO and in structure . . .
Appendix 4: The significance of xylem water transport for supplying water to cells
. . . . . . .
photosynthesizing with air as the CO, source.
Appendix 5: T h e costs of homoiohydry and desiccation-resistance . . . . . .
References
. . . . . . . . . . . . . . . . . . .
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INTRODUCTION
Kenneth Sporne kept British plant morphology alive as a discipline at the
undergraduate and postgraduate level while all around there were defections to
palaeobotany per se, to electron microscopy, and to developmental biology. His
research and teachings concentrated on the contribution which classical
anatomy and morphology had to make to our understanding of how plants were
related to each other, and he was always scrupulous in distinguishing fact from
speculation. While trying to keep to this latter precept, my facts and
speculations will be drawn from physiology to at least as great an extent as from
morphology and anatomy.
My aim is to comment on some of the possible selective pressures, and the
processes, involved in the evolution of a vascular land flora, to think about the
events and processes at the very beginning of the story of pteridophytes,
gymnosperms and angiosperms which is so clearly told in the three textbooks of
vascular plant morphology produced by Sporne over the last two decades
(Sporne, 1974a,b, 1975). The present essay is essentially a precis, extension and
reformulation of Raven (1977a), with contributions from: Raven (1970, 1977b,
1980, 1981a, b, 1983a, b), Raven & F. A. Smith (1976), Raven, F. A. Smith &
S. E. Smith (1980) and Raven, S. E. Smith & F. A. Smith (1978) and many others
acknowledged in this article. I have tried to heed warnings from Garland ( 1981 )
as to the difficulties in applying Occam’s razor to evolutionary speculation, and
of Osmond, Bjorkman & Anderson (1980) as to the difficulties in attributing
selective significance to physiological attributes even in extant plants.
THE VASCULAR CONDITION
In order to put the evolution of vascular plants into perspective it is necessary
to consider the essential attributes of a vascular plant sporophyte, and their
significance.
The vascular land plant lives at the interface between a liquid phase (the soil
solution, supplying H,O and nutrients, e.g. N, P and K, other than CO,, with
the solid phase of the soil providing support, and generally a gas phase present
in the soil as well) and the atmospheric gas phase (supplying CO, and
transparent to photosynthetically active radiation (400-700 nm)). There are
substantial differences between this pattern of resource availability and that
of a submerged benthic rhizophyte (cf. Luther, 1949; Raven, 1981b)
in that H,O is available to the terrestrial vascular plant only via the rooted
portion and, indeed, is lost from the shoot system as a concomitant of CO,
fixation. An even larger contrast is found in comparison with benthic submerged
haptophytes (and phytoplankters) where CO,, other nutrients and water, as well
as light, can be absorbed all over the plant surface. A major attribute of the
vascular land plant is the homoiohydric condition (see Raven, 1977a; Walter &
Stadelmann, 1968); the mechanism and significance of homoiohydry is a major
theme of this article.
Extant terrestrial vascular plants are characterized by the possession of:
xylem; cuticle; stomata; intercellular air spaces; phloem; endodermis (or its
functional equivalent); alternation of generations.
Xylem: This is the sine qua non of vascular plants, and is essentially a means of
transmitting large quantities of H,O up the plant under relatively low H,O
PHYSIOLOGY AND FOSSIL PLANTS
I07
potential (#w) gradients (Appendix 1). A large water flux from soil to shoot is
needed to supply not only the 5-10 kg H,O retained in shoot material for every
kg dry weight increment in shoot growth, but also the 300 or more kg of H,O
transpired per kg dry weight gain as a concomitant of CO, fixation (Appendix
2). Since the xylem H,O is under tension (Appendix 1; Pickard, 1981) there is a
tendency for the xylem elements to collapse, the tension in the contained water
being perceived as a compressive force in the wall. This tendency to collapse is
resisted by the presence of lignin (complex polymers of phenylpropanoid units:
Gross, 1980). The low resistance to longitudinal (axial) water flow in the xylem
is related to the absence of living cell contents: programmed cell death as a part
of the development of phototrophic organisms at many phylogenetic levels, for
example, the ‘necridia’ of cyanobacteria (Addicott, 1982; Lamont, 1969).
Lignin also functions in anti-biotroph defences (probably preceding its
structural role in xylem in compression resistance in H,O-conducting elements)
and in the support of the plant shoot in the low-density fluid medium of air
(probably a later role than its function in conducting elements): Raven (1977a).
Cuticle: The cuticle is a hydrophobic, water-repellent and water-impermeable
layer over the surface of the shoot and; indeed, at all cell-air interfaces such as
on root surfaces, and the linings of intercellular gas spaces (Hadley, 1981;
Raven, 1977a). The cuticle per se consists of a complex mixture of cross-linked
long-chain esters, alcohols and fatty acids, and has a wax (long-chain
hydrocarbon) layer on its surface. The water permeability is not readily related
to the cuticle thickness (Martin &Juniper, 1970; Schonherr & Merida, 1980); it
is largely controlled by the composition and thickness of the wax layer. For a
given number of wax molecules per unit shoot surface area the H,O
permeability is approximately halved for each additonal two-carbon unit added
to the hydrocarbons (paraffins) in the wax, thus rationalizing the occurrence of
such long-chain hydrocarbons in the wax (Schonherr & Merida, 1980). This
outer wax layer facilitates H,O run-off following rain or dew, thus decreasing
the resistance to CO, influx; it also forms a layer which, when complete (i.e.
when stomata are closed or absent) very greatly reduces the H,O permeability
of the plant surface, thus reducing water loss from a plant whose H,O supply
cannot keep pace with the evaporative demand of the atmosphere but also, alas,
reducing CO, entry and photosynthetic fixation, since no known cuticle-wax
complexes have a significantly higher permeability to CO, or 0, than to H,O
(see Lendzian, 1982; Raven, 1977a). The negligible resistance to H,O
evaporation from the (waxless) walls of mesophyll cells lining intercellular
spaces in the leaf does not increase with decreased water content in contrast to
the situation in many poikilohydric plants (Jones & Higgs, 1980; Jones &
Norton, 1979; Proctor, 1979). The cuticle (plus wax) also acts as a defence
against biotrophs, and, in plants growing in environments with a high photon
flux density, thick cuticles can reflect deleterious radiation of both UV and
longer wavelengths Klein ( 1978).
Sfornufa: The variable-aperture stomatal pores are in the epidermis and cuticle;
when open, they permit gas exchange between the external atmosphere and the
internal gas phase of the shoot (see Appendix 1); when closed, gas exchange is
greatly restricted. The regulation of stomatal conductance appears to operate to
optimize CO, gain in photosynthesis per unit H,O lost in transpiration
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J . A. RAVEN
(Cowan, 1977; Wong, Cowan & Farquhar, 1979; see Jones, 1976, for a
discussion of the effect of different fractions of leaf photosynthesis being
consumed in dark respiration on this optimization).
Internal air spaces: These are the necessary correlate of stomata. Without an
internal aeration system to ‘distribute’ CO, in a medium in which CO, diffuses
lo‘ times faster than it does in H,O, the photosynthetic rate per unit plant
external surface would be much lower than the rate achieved by homoiohydric
plants. Appendix 3 discusses how the balance between diffusive and biochemical
constraints on the rate of CO, fixation is struck. In brief, the large N and energy
input in producing the primary photosynthetic carboxylase, ribulose
bisphosphate carboxylase-oxygenase (RUBISCO), is not optimally used (in
terms of CO, fixed s/unit N or unit energy invested in producing the enzyme)
unless the enzyme is displayed over a large area of cell-gas phase interface with
a minimal aqueous-phase diffusion path. Most terrestrial vascular plants have
about one-third of their total limitation on photosynthesis in transport
(diffusion) processes in the gas phase of the boundary layer, stomata and
intercellular air spaces, and the liquid phase; the remaining two-thirds of the
resistance is attributable to biochemical processes including RUBISCO activity
(Begg, 1980; Caemmerer & Farquhar, 1981; Nobel, 1980; O’Leary, 1981;
Raven, 1981a). Thus the intercellular space system is crucial to the gas
exchange of the shoots of homoiohydric vascular plants. We may contrast the
contention of Church (1919) who asserted that the stomata air space system was
not essential for photosynthetic CO, uptake since CO, could cross a wet
membrane as easily as a comparable air barrier: this view is clearly wrong and
the importance of stomata had been pointed out by Brown & Escombe (1900).
Nutrient solute acquisition and transport: Several features not completely restricted to
vascular plants are associated with the acquisition of nutrients. For N, P, K and
some micronutrients the analyses of Grubb (1977), Nye & Tinker (1977), Oliver
& Barber (1966a,b) and Prenzel (1979) show that the soil solution
concentration in non-agricultural soils is too low for the H,O flux toward the
plant during transpiration to supply the nutrient to the root surface at a rate
fast enough to supply the plant’s requirements. In quantitative terms, the P per
unit dry weight of plant divided by the H,O transpired per unit dry weight
increment of plant exceeds by up to a thousand fold the P concentration in the
soil solution, with analagous relations holding for N and K. The supply of these
nutrients to the plant is thus a function of the (very slow) diffusion of phosphate
(and the much faster diffusion of K + and of the NH: and NO2 which demands
that the plant must continually extend its subterranean portions into relatively
unexploited parts of the soil in order to obtain sufficient of these elements (Nye
& Tinker, 1977; Scott-Russell, 1977). In extant vascular plants these extending
organs are roots and/or rhizomes bearing root hairs (rhizoids) and/or
mycorrhizas (see Smith, 1980). The extension rate through soil is, of course,
limited by the need to concentrate growth in a limited apical region otherwise
buckling of the extending organ would occur in the mechanically resistant soil
(see Scott-Russell, 1977). It is likely that, in well-watered soil, the extent of the
root system is a function of nutrient acquisition capacity rather than the need
for mechanical support for the shoot.
The plant’s nutrient requirements demand selective uptake by the plant;
PHYSIOLOGY AND FOSSIL PLANI'S
109
further, selective transfer to the shoot is required in view of the very limited
capacity for the shoot to dispose of excess solutes by direct excretion or by
phloem retranslocation to below-ground portions: particular difficulties are
experienced with H + / O H - and C a 2 + (Raven, 1977a,b). Church (1919; see
Mabberley, 1981) pointed out the significance of the transpiration stream as the
main mode of nutrient transport to the shoot; clearly diffusive transport of
solutes within the plant is inadequate over distances of the order of the height of
even small vascular plants, since Nobel (1974) showed that the time taken for a
solute of diffusion coefficient lo-' m2 s-' to reach I/e (0.37) of its source
concentration is 0.6 s for a sink 50 pm distant but 8 years when the sink is 1 m
distant from the source!
The selectivity of transport into the phloem is maintained by a restriction on
apoplastic (extracellular) H , O flux, which could (depending on the properties
of the apoplastic pathway) give a non-specific solute entry to the xylem, to some
1-3% of the total H,O flux (Pitman, 1977; Raven, 1983a). The symplastic
movement of solutes and H,O permits a much greater selectivity of solute
loading into the xylem. The endodermis contains suberin in the casparian strip
as an apoplastic barrier; this structure may have originated from the internal
cuticle (see Krassilov, 1981), and may also function in maintaining the polarity
of solute porters between the stelar and the cortical symplast plasmalemma (see
Dragsten, Blumenthal & Handler, 1981, for the analogous role ofanimal epithelial
tight junctions).
The xylem is apoplastic, and thus does not suffer from the deficiencies of the
symplast phloem with respect to the carriage of such solutes as H + and C a 2 +
(Raven, 1977a,b). However, the H , O carried by the xylem ends u p mainly in
mature photosynthetic organs which are the main sites of transpiration, rather
than in the growing portions of the shoot where there is the major net
requirement for the xylem-borne solutes. Pate (1980) and Pate & Layzell (1981)
point out that xylem-to-xylem transfer of solutes takes place within the stem,
with a depletion of xylem streams destined for the mature photosynthetic organs
and an enrichment of those streams passing to immature regions of the shoot in
xylem-borne solutes. This transfer, and xylem-to-phloem solute transfer, recalls
some older pre-occupations of plant morphologists with stelar morphology in
relation to exchanges between the stele and extra-stelar tissues (e.g. Bower,
1930). However, the modern thrust is aimed more at exchanges between stelar
elements themselves, and the morphological expression of the surface/volume
relationships discussed at length by Bower (1930) is now thought to reside at the
level of vascular transfer cells (see Gunning, Pate & Green, 1970) as well as in
grosser aspects of vascular structure. As with many transfer cell locations it is not
easy to see a taxonomic pattern behind the presence or absence of vascular
transfer cells; but it may be significant that xylem transfer cells are lacking in
extant lycopsids which lack leaf gaps (Gunning, Pate & Green, 1970; cf. Sporne,
1974a,b, 1975).
The symplastic phloem appears to be optimized for the transport of organic C
and N with minimum energy expenditure in propelling the phloem sap
containing the C and N (Lang, 1977; Passioura, 1976) from C sources to C
sinks. As a 'general carrier' the phloem suffers, as does the xylem, from the
problem of directionality, since the phloem moves solutes only from
photosynthetic or storage regions to growing regions; there is the further
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J. A. RAVEN
problem that certain solutes (H’, C a 2 + )are not transported readily in phloem,
at least in comparison to the potential physiological need for their transport.
This latter difficulty is quantified by Raven (1977b) via the ratio of elements in
the phloem and the ratio of elements required in the sink tissue.
Reproduction: All vascular plants show a heteromorphic alternation of generations
(Keddy, 1981), and the properties of the homoiohydric plant discussed above
relate essentially to the sporophyte generation; the gametophyte generation is
essentially poikilohydric, with protection from H,O stress afforded by the
megaspore wall of heterosporous free-sporing plants, and by seeds of
spermatophytes where the megasporangium is indehiscent. The wind dispersal
of spores (and later seeds) was probably a major early selective pressure for
plants of greater sporophyte stature, thus allowing the release of propagules into
turbulent air. Other advantages relate to the competition for light (see Givnish,
1982) and the avoidance of grazers and parasites which, in the case of the insects
and fungi, soon evolved wings and aerially dispersed spores respectively! (see
Raven, 1977a; Swain, 1978; Swain & Cooper-Driver, 1981). Despite biophage
‘short-circuiting’ of some of the advantages of size, a large size is still an
important adaptive stratagem in extant plants of stable habitats which have
reasonable resource availability (the C strategists of Grime, 1979). Such
increased size demands quantitative and qualitative additions to the amount
and efficiency of the homoiohydric H,O regulation system.
THE PHYSICO-CHEMICAL AND BIOTIC ENVIRONMENT OF THE EARLY EVOLUTION OF
VASCULAR PLANTS
The physico-chemical environment: The description of the physicochemical environment of the Silurian and Devonian presents difficulties. The
solar radiation available to the earth may have increased by some 30% over the
last 4.109 years (Newman, 1980), although the ultraviolet component may have
been much more important early in this period (Canuto et al., 1982); thus
photosynthetically active radiation in the Silurian-Devonian was probably
similar to extant levels. The CO, content of the atmosphere early on in the
earth’s evolution may well have been substantially higher than present-day
levels. The biological and geochemical factors regulating this content are
discussed by Holland (1965) and Lovelock & Whitfield (1982), while substantial
variations over periods of 10’- 1O5 years are documented by Neftel et al. ( 1982).
The 0, content of the atmosphere was probably less than the current level, with
a recent estimate of some 13 kPa (cf. the current 21 kPa) for the Lower
Carboniferous 0, partial pressure probably representing an upper limit for the
Siluro-Devonian (Cope & Chaloner, 1980, 1981; cf. Clark & Russell, 1981).
Mechanisms regulating atmospheric 0, levels are imperfectly understood
(Margulis, 1981 ; Redfield, 1958). The earliest sites for vascular macrofossils
were at low latitudes, although it is not clear what the ambient temperatures
would have been. The soil would have been very substantially modified by the
pre-vascular plant biota discussed below.
The biolic environment; It is important to realize that there was probably a
substantial non-vascular phototrophic flora on land before the first vascular
land plants. This consisted of ‘soil algae’, probably mainly members of the
PHYSIOLOGY AND FOSSIL PLANTS
Ill
Chlorophyta and Cyanobacteria (Metting, 1981) as well as the metaphyta
which possessed trilete spores and thick cuticles (Chaloner & Sheerin, 1979).
Such organisms could have been involved in pedogenesis, including the release
of mineral nutrients (K, P) into solution and the fixation of N, to give
‘combined N’ (see Gorham, Vitousek & Reiners, 1979).
Furthermore, there was probably a substantial range of heterotrophs present,
including fungi and arthropods. Some were presumably necrophages, but others
were probably biophages, and the production of secondary products by the
phototrophs was probably an early counter-measure (see Raven, 1983b). Extant
soil and freshwater Chlorophyta produce phenolics and sporopollenin (Raven,
1977a); these compounds could have had a role in mitigating the effects of UV
light which could have been more significant when the oxygen/ozone screen was
less complete (see Margulis, 1981). Cuticle-like structures can reflect UV light,
and epidermal phenolics (Lowry, Lee & Hebant, 1980) can absorb UV light
before it has penetrated to ‘sensitive’ DNA, RNA and proteins. These
compounds are important precursors of essential elements of the homoiohydric
apparatus of vascular plants; Gomes & Gottlieb (1978) make a contrary
suggestion (based on little evidence) that chemoprotectant micromolecules are
secondary to the macromolecular phenolic polymer lignin which had (and has)
a mechanically protective role in preventing biophagy.
HOW VASCULAR PLANTS MAY HAVE ARISEN
How large were the transmigrant algae?: The fossil record is not very helpful in
indicating the origin of vascular plants. Biochemical and ultrastructural studies
of extant plants suggest that it is the algal division Chlorophyta, and more
specifically the class Charophyceae, which is most closely related to the
Bryophyta and Tracheophyta (Graham, 1982; Graham & Wilcox, 1981;
Melkonian, 1982; Raven, 1977a; Stebbins & Hill, 1980; Stewart & Mattox,
1978; Taylor, 1982; Whatley, 1982). The general (ultrastructural, enzymic)
attributes of the Charophyceae are not readily ascertained from fossils, so only
more specific attributes which associate a fossil with an extant charophycean
alga can indicate their occurrence. Upper Silurian gyrogonites (oogonia), and
Lower Devonian rhizoids, suggest that the specialized charophycean
macroalgae were contemporaries of the earliest vascular plants, but give little
information on the nature of the presumed common ancestor of the
Charophyceae and the Tracheophyta (Edwards & Lyon, 1983; Grambast,
1974).
Various hypotheses have been put forward as the degree of morphological
complexity of the transmigrant alga. Church ( 1919) suggested transmigration
from an aquatic environment of a large, complex plant, while Stebbins & Hill
( 1980) adopted an antithetic stance in proposing unicellular tranmigrants;
authors such as Bower (1930), Fritsch (1945) and Raven (1977a) occupy the
middle ground.
Church (1919) maintained that vascular plants derived from ‘stranded’
benthic haptophytic marine algae; such algae had the biochemical attributes of
green (we would now say charophycean) algae, but a parenchymatous thallus
rivalling in complexity that of extant Laminariales or Fucales in the
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Phaeophyceae, together with fertilization in situ and an alternation of
generations. These ‘Thalassiophyta’ no longer exist (if they ever did).
In contrast, Stebbins & Hill (1980) suggested that members of the
Charophyceae are essentially soil-dwelling green algae, and that the evolution of
structural complexity led to both the predominantly terrestrial Bryophyta and
Tracheophyta, and to a multicellular algal residuum, most of which are
freshwater submerged aquatics.
The supporters of the intermediate view seek the origin of vascular land
plants from reasonably differentiated Fritschiella-like benthic freshwater
rhizophytes, which became soil-dwellers at a stage of morphological and
reproductive complexity intermediate between the unicells of Stebbins & Hill
(1980) and the complex parenchymatous (Graham, 1982) plants of Church
( 1919; Corner, 1964).
Space does not permit an exhaustive analysis of these different possibilities.
However, the views of Stebbins & Hill (1980) and of Fritsch (1945) seem
plausible in that the sorts of selective pressure which led to differentiated,
perennial multicellular thalli in several classes of marine algae could also
operate in freshwater and on land. Such selective pressures include greater
immunity from biophages, the ability to shade out competitors at their own
trophic level; the ability to sequester seasonally available nutrients; and the
ability to place propagules into turbulent, fast-flowing fluid (H,O or air): see
Grime (1979); Raven (1977a); Raven (1981b); Raven, Smith & Glidewell
(1979); Swain (1977); Swain & Cooper-Driver (1981). Accordingly,
characteristics such as multicellularity, well-defined growing zones,
plasmodesmata and oogamy could have been selected for in freshwater or on soil
just as occurred in the marine Phaeophyceae and Rhodophyceae. Certainly
some of the arguments of Church (1919) against a freshwater or soil origin of
vascular plants have been falsified by later investigations; examples are the
claims of a very marked contrast in N and P availability between seawater and
freshwater (Morris, 1980; Moss, 1980), and the inability of marine algal
propagules to invade freshwater and terrestrial habitats in the absence of
animals to move them.
Characteristics of prevascular land plants: A wide range of plants occurred on land in
the Silurian; multicellular plants with a cuticle, and spores with sporopollenin,
were established by mid-Silurian times (Banks, 1975; Chaloner, 1970; Chaloner
& Sheerin, 1978; Edwards, 1979; Edwards, Bassett & Rogerson, 1979; Edwards,
Edwards & Rayner, 1982; Edwards, Feehan & Smith, 1983). In addition to the
UV-reflective and anti-biophage roles (see above), the very thick cuticles of
some of these plants may have had a structural role, as well as being something
of an impediment to photosynthetic CO, uptake. However, as noted above, the
thickness of the cuticle is not a good guide to H,O permeability. Certainly, a
thick, hydrated cuticle might inhibit CO, entry more than the entry of this gas
would be facilitated by a non-wettable plant surface increasing ‘run-off of
liquid H,O, thus decreasing the liquid phase resistance to CO, transport. The
exact nature of the sporangia from which the early and mid-Silurian spores were
produced is unknown.
An early Silurian fossil which Raven (1977a) took as a model for the
immediate precursor of a vascular plant is Eohostimellu: the coalified material
PHYSIOLOGY AND FOSSIL PLANTS
I13
represents (presumably) erect cylindrical axes 1-2 mm in diameter (Schopf el
a f . , 1966); no reproductive structures or details of internal structure are known,
although the nature of the preservation is presumed by Schopf el a f . (1966) to
indicate the existence of a cuticle and of thick-walled hypodermal tissue
(Edwards, Bassett & Rogerson, 1979). Appendix 4 shows how large a difference
in H , O potential between the top and bottom of the plant would be needed to
supply water at a rate commensurate with a CO, fixation rate of lpmol m - 2
s-I for a plant lacking intercellular air spaces; such a low @
,,, at the apices
would presumably have an adverse effect on the biochemical reactions of
photosynthesis (Hsaio, 1973; Larcher, 1979).
The evolution of earh vascular plants: The ‘upward urge’ (for the selective reasons
discussed earlier) could be sustained only by an improved water supply to the
aerial axes. Such an improved supply could be envisioned for Cooksonia, one of
the earliest vascular plants so far described. This plant had dichotomizing,
cuticularized axes bearing terminal sporangia, and had peripheral
(collenchymatous) supporting tissue similar to that presumed by Schopf et a f .
(1966) to occur in Eohostimeffa; it also had a central strand of tracheids
(Edwards et a f . , 1979 and Edwards el a f . , 1983). The advantage to the plant in
terms of H,O supply to the aerial, photosynthetic axes of the presence of xylem
is discussed in Appendices 1 and 2. The programmed cell death inherent in
xylem production has precedents in prokaryotes (the necridia of cyanobacteria)
and in eukaryotic algae (death of some products of meiosis in oogenesis in some
fucalean algae: Bold & Wynne, 1977), but is not commonly a part of
morphogenesis of the vegetative plant body (see Wetherbee & Kraft, 1981).
Lignin (claimed to be present in early Silurian strata containing no vascular
plants: Niklas & Pratt, 1980) had precursors in the UV-screening for antibiophage phenolics (see above).
The final stage in the evolution of the homoiohydric plant involved the
acquisition of the stomata/intercellular air space system. These attributes are
both found in Rhynia, but the occurrence of intercellular gas spaces in
<osterophyffum (the earliest plant with stomata) is still conjectural (see below).
The selective advantage of the intercellular air space system can be readily seen
in terms of the improved surface/volume ratio which minimizes the liquid-phase
diffusion path of CO, from the gas phase to RUBISCO in organisms which, by
growing taller, must for mechanical reasons increase the diameter of their axes
(see Niklas, 1978) and thus have a decreased ratio of external surface to volume
(see Appendix 4). Other methods of increasing the surface to volume ratio are
seen in extant poikilohydric plants such as members of the Polytrichaceae (see
Proctor, 1979; Raven, 1977a), but these surface corrugations have less potential
than the development of intercellular gas space for the subsequent evolution of
homoiohydry. The schizogenous production of gas spaces in an initially (in the
meristem) ‘solid’ aqueous tissue is clearly a well-ordered process (Roland, 1978),
but the physical details are still poorly understood (see Raven, 1977a).
Precedents for the production of intercellular air spaces in parenchymatous tissues
seem to be lacking in algae, but an analagous phenomenon is found in the
gametophytes of the Marchantiales and in sporophytes of Musci (see Raven,
1977a; Appendix 4). It is possible that intercellular air spaces in the sporophytes
of vascular plants were first found in the sporangia, with haploid spores
1 I4
J . A. RAVEN
immediately prior to their release being separated from the diploid sporangium
wall by an air space; the extent to which this situation is relevant to the
production of intercellular spaces in a mass of diploid vegetative tissue is not
clear.
Stomata may have originated from ‘passive’ aerating pores of the type found
in the Marchantiales (Raven, 1977a); their origin as secretors of liquid H,O
(Church, 1919) implies that root pressure was occurring and that an
endodermis (or its functional equivalent) was present. The acquisition of the
‘active’ opening and closing movements involves the special mechanical
properties of the guard cell walls, and the coupling of osmotica-generating and
osmotica-removing reactions, which alter cell turgor and thus stomata1 aperture,
in response to environmental stimuli of light, intercellular space CO,
concentration, relative humidity, leaf H,O potential, abscisic acid concentration
and, most importantly, the metabolic capacity for photosynthesis of the
mesophyll cells (see Wong, Cowan & Farquhar, 1979).
While ~osterophyllumand subsequent vascular plants had (with the proviso of
adequate preservation) stomata (see Chaloner, 1970; Chaloner & Sheerin,
1979), it is less easy to be sure that they had intercellular air spaces; this point
seems proven for Rhyniu, but not for ,&lerophyllum. It would be most interesting
(and puzzling!) if stomata occurred in the absence of intercellular gas spaces.
Turning to the quantitative aspect, the frequency of stomata (number mm -,)
in the early vascular plants seems to have been lower than the range in extant
plants (cf. Stubblefield & Banks, 1978, with Table 1 of Meidner & Mansfield,
1968); however, the dimensions for the stomata of Rhyniu and <osterophyllum
stomata (Kidston & Lang, 1917; Walton, 1964) are at the upper end of the
range quoted in Table 1 of Meidner & Mansfield (1968); thus the conductance
(computed from frequency and dimensions according to Meidner & Mansfield,
1968: 59, equation (6)) is probably a t the low end of the range for extant
vascular plants (Woodhouse & Nobel, 1982). This sets limits on the
photosynthetic capacity of the plants relative to that of extant plants, although
this may have been offset in part by higher ambient CO, concentrations (see
above) in the Devonian (cf. Appendix 4).
The foregoing arguments suggest that the sequence of acquisition of H,Oconducting and gas-exchange-regulation mechanisms revealed by the fossil
record is generally in accord with teleological expectation, in that the H,Oconducting system in the absence of the gas-exchange-regulation mechanism
would be of more selective advantage than the reverse state of affairs in an erect
plant.
Much less is known about the evolution of the below-ground portions of the
sporophytes of vascular plants. The diageotropic subterranean axes of Rhyniu
and other plants in the assemblage had root hairs and mycorrhizas (inferred
from the presence of fungal cysts). The ‘root’ and ‘-rhiza’ terminology is not
entirely appropriate with respect to the Rhynie plants which did not have true
roots. The ‘root hairs’ and ‘mycorrhizas’, together with the (presumably) apical
growth of the axis and its branches, probably served to exploit the nutrient and
H,O reserves of the soil. These subterranean organs are assumed to have had an
important role in relation to acid-base balance during nitrogen assimilation
(Raven & Smith, 1976); Raven et al. (1978) have suggested that the
mycorrhizas of these plants may have had a particular role in acid-base
PHYSIOLOGY AND FOSSIL PLANTS
115
regulation. In terms of the wider problem of the regulation of solute transfer to
the shoot in the transpiration stream it has been argued above that some
apoplastic barrier to solute transfer from the soil solution to the xylem is a
prerequisite for the regulation of solute supply to the shoot. A well-defined
endodermis in fossil vascular plants was apparently a relatively late acquisition
(e.g. in Carboniferous Equisetites: Walton, 1940). Before the absence of a welldefined endodermis in the axes of Rhynia (see Schoutte, 1938) is taken to indicate
poor capacity to regulate the shoot solute content, it should be noted that the
absence of a casparian band in the ‘endodermoid’ layer of endohydric moss
gametophytes (Scheiner, 1976) and in roots of Lycopodiaceae (Clarkson &
Robards, 1975) does not have large effects on the shoot K/Na or K/Ca ratio
relative to lower vascular plants possessing an endodermis (Walland & Kinzel,
1966), although the acquisition of solutes from leachate from leaves above them
in the canopy may account for some of the high K/Na and K/Ca ratio in the
shoots. Further work is clearly needed on the correlation between shoot solute
content and the occurrence of a morphologically ‘normal’ endodermis (Grubb,
1967).
The problems of regulating solute supply to the shoot of early vascular plants
would have been greatly increased if the plants were living in a saline
environment (see Church, 1919; Edwards el al., 1983). If the concentration of
NaCl in the total plant water and the external solution is the same at, for
example, 300 mol NaCl m-3, and the ratio of water transpired to water
retained by the plant shoot during growth is 80 (Appendix 2), then the mean
xylem concentration of NaCl must be only & of that in the soil solution.
CONCLUSIONS
It is hoped that this article has helped to relate the sequence of changes in the
morphology and anatomy of plants seen in Silurian-Devonian fossils to
physiological imperatives for the evolving vascular plants. However, it must be
borne in mind that before the first known vascular plant (Cooksonia) and also
subsequently, there was also a great variety of non-vascular terrestrial plants;
not all of these were likely to have been closely related to the precursors of
vascular plants (see Edwards, Bassett & Rogerson, 1979; Edwards, Edwards &
Rayner, 1982; Edwards, Feehan & Smith, 1983). Eventually, competition with
vascular plants and bryophytes extinguished these plants, leaving organisms
which were obviously algae (including lichenized algae) and bryophytes as the
only competitors with the homoiohydric vascular plants.
The data most useful for ‘palaeoecophysiology’ which analysis of fossils can
provide are (as seen in Appendices 1-3) the dimensions of xylem elements, the
thickness of the cuticle, the stornatal frequency and size, the ratio of stornatal
pore size to the size of the substomatal cavity (Pickard, 1982) and the ratio of
internal to external area exposed to the gas phase. This is, of course, but a small
fraction of the quantitative data available from the study of early vascular plant
fossils, although the significance of the other data (e.g. the analysis by Bower
(1930) of the surface/volume ratio of the stele) is less obvious in terms of today’s
plant physiology. As mentioned in the Introduction, I do not propose to discuss
the details of the evolution and significance of leaves, roots, heterospory, etc.,
116
J.
A. RAVEN
which were later acquisitions by vascular plants (c( Raven, 1977a; Givnish,
1979).
We may note that, as plants got larger, with greater bulk of nonphotosynthetic tissues to be produced and maintained, the rate of photosynthesis
per unit of photosynthetic tissue required for growth becomes larger. Thus, as
plants grew taller, with more conducting and structural tissue, they require
more light to give adequate rates of photosynthesis. Thus large homoiohydric
plants have higher light compensation points for growth than do many smaller
homoiohydric plants, with the poikilohydric gametophytes (with essentially no
non-green tissue) having even lower light compensation points (Raven &
Beardall, 1982). Hence we can see how the diversity of plants, including herbs
and gametophytes, could co-exist with forest trees in Upper Devonian and later
forests (Phillips & Dimichelle, 1981). The forest trees had disposed, by
abscission, of leaves or branches which were receiving so little light that they
were below the whole-plant compensation point; this permits sufficient light to
pass through the canopy to support the growth of plants of lower stature with
lower light compensation points.
ACKNOWLEDGEMENTS
Dr Dianne Edwards and Professor W. G. Chaloner have provided very
generous assistance with palaeobotany and morphology; errors which remain
are entirely the responsibility of the author.
APPENDIX 1: THE RELATIVE SPECIFIC H 2 0 CONDUCTANCE OF PARENCHYMA AND XYLEM
TISSUES
The units ofspecific H 2 0 conductance are m 2 s- 1 Pa- 1 (i.e. m 3 H 2 0 moving
s __ , (m 2 area ofpathway normal to the H 2 0 flux)-' (Pa m-'ofdriving force in
the direction of the H 2 0 flux)-'). Data discussed by Raven (1977a) suggest that
the specific H 2 0 conductance of living parenchyma tissue (i.e. the apoplastic,
cell wall pathway, involving no crossing of membranes, and the cellular
pathway involving the crossing of at least two membranes per cell crossed, i.e.
the plasmalemma at the 'influx' end and that at the 'efHux' end) is some w-IS
m 2 s- 1 Pa- 1• Xylem consisting of tracheids has a specific conductance of some
I0- 9 m 2 s-' Pa-', i.e. 10 6 times that of the parenchyma cell pathway.
APPENDIX 2: THE H 2 0 LOSS ASSOCIATED WITH PHOTOSYNTHETIC C0 2 FIXATION IN A
TERRESTRIAL PLANT
The net photosynthetic rate of a plant can be expressed as:
(I)
PHYSIOLOGY AND FOSSIL PLANTS
where
Pnct
Dco
I
'
117
= C0 2 fixation rate/mol m- 2 s- 1
= Difussion coefficient of C0 2 in air/m 2 s- 1
= Diffusion path length from bulk air to the surface of the
photosynthetic cell/m
= C0 2 concentration in bulk air/mol m- 3
= C0 2 concentration at surface of photosynthetic cell/mol m- 3
The transpiratory water loss can similarly be expressed as:
Tr =
DHo
~
1
(H 2 0] 1 -[H 2 0].)
(2)
= H 2 0 vapour transpired/mol m - 2 s- 1
=Diffusion coefficient of H 2 0 in air/m 2 s- 1
= Diffusion path from the surface of the photosynthetic cell to
the bulk air/m
[H 2 0]. = H 2 0 vapour concentration in bulk air/mol m - 3
[H 2 0Ji = H 2 0 vapour concentration at surface of photosynthetic
cell/mol m - 3
where Tr
Dividing equation (2) by equation (1):
Tr _ DH,o ([H 2 0] 1 -[H 2 0].)
Pnet- Dco, ([C0 2 ].-[C0 2 Ji)
(3)
With DH 0 = 1.6, air temperature leaf= temperature = 25°C, internal
relative hum'idity of 99% ([H 2 0] 1 = 1270 mmol m-1, equivalent to a relatively
low leaf 1/Jw of - 1.38 MPa), external relative humidity of 50%
([H 2 0].=640mmol m- 3 ), external C0 2 partial pressure of 30kPa
([C0 2 ] 8 = 10 mmol m- 3 ), internal C0 2 partial pressure of 20 kPa
([C0 2 ] 1 = 6.7 mmol m- 3 ), equation (3) shows that
Tr
(1270-640)
-p = 1.6
= 302 mol H 2 0 lost per mol C0 2 fixed
net
( 10- 617)
For a plant with 50% C in the dry weight (Westlake, 1963), I mol C0 2 is
equivalent to 24 g dry weight, while 302 mol H 2 0 has a mass of 5463 kg, so
227 g H 2 0 must be lost in gaining I g dry weight of photosynthate. Since dark
respiration (see Raven, 1976) amounts to some 0.33 C lost as C0 2 per C
assimilated into cell material in a C 3 herb, this brings the H 2 0 transpired per
dry weight gain to 302 g H 2 0/g dry weight gain. In practice, C 3 plants lose at
least 400 g H 2 0/g dry weight gain (e.g. Black, 1973).
APPENDIX 3: THE SIGNIFICANCE OF EXPOSING A LARGE AREA OF CELL SURFACE TO THE
GAS PHASE IN RELATION TO THE PLANT'S INVESTMENT IN RUBISCO AND IN STRUCTURE
RUBISCO has a high Mr (5.5.10 5 ), a low solubility ( ~5 mol m- 3 ), a low
specific reaction rate at C0 2 saturation at 25°C ( <20 mol C0 2 (mol
enzyme)-' s-') and a Kt which is higher than the air-equilibrium C0 2
concentration in solution at 25°C (Kt> 10 mol m- 3, air-equilibrium
solution= 10 mol m - 3 ) and, in addition to its carboxylase activity, it has an
oxygenase activity which, in air-equilibrated solution, gives an oxygenase
118
J. A. RAVEN
activity which consumes RuBP at about 0.25 of its rate of consumption by the
carboxylase activity (Bird, Cornelius & Keys, 1981; Hall, Pierce & Tolbert,
1981; Lorimer, 1981; Raven, 1981a; Raven & Glidewell, 1981). The enzyme is
conservative kinetically; within the eukaryotes the rate of CO, fixation in airquilibrated solution at 25°C varies (on a unit protein basis) only about two-fold
between algae, bryophytes, pteridophytes, gynmosperms and angiosperms, with
C,, C,, CAM or ‘CO, concentrating mechanism’ metabolism (see Cornelius &
Keys, 1981; Jordan & Ogren, 1981; Lorimer, 1981; Raven & Beardall, 1981;
Yeoh, Badger & Watson, 1981). Up to 25% of the protein (soluble and
insoluble) in a photosynthetic cell is RUBISCO. Accordingly, economy in N and
energy used for RUBISCO synthesis demands that the CO, and 0,
concentrations at the site of RUBISCO activity should be as near the airequilibrated values as possible. Photosynthetic activity decreases CO, and
increase 0, at the site of the enzyme (by almost equal absolute amounts), the
changes increasing with increasing diffusive resistance to gas exchange between
bulk air and RUBISCO (Raven, 1977a, 1981a; Raven & Glidewell, 1981;
Samish, 1975). Since D,
in water is only some lo-’ of DCO2in air, the
adverse effect of 1 pm diffusive pathway in water on RUBISCO activity is
equivalent to that of a 10 mm gas-phase diffusion path; the large M, and low
solubility of RUBISCO means that RUBSICO added to a constant area of cellgas phase interface would be disadvantaged, in that the added RUBSICO
would be further from the interface and thus be exposed to a lower absolute
[CO,] and to a lower [CO,]/[O,]. At the other extreme, a minimal transport
resistance (a monolayer of RUBISCO molecules at the water-gas interface,
with optimal gas exchange between the interface and bulk air) would involve a
large input of material (organic C) and energy into structures. Several lines of
evidence (O’Leary, 1981; Wong, Cowan & Farquhar, 1979) suggest that, in
extant C, plants, the diffusive resistance (a long gas-phase path through a
medium with a high DCO,and a short liquid-phase path through a medium
accounts for 0.2-0.5 of the total (lifecycle integrated)
with a low D,,)
limitation on photosynthesis; the remaining 0.5-0.8 of the limitation is related to
biochemical processes (with RUBISCO a major contributor), This range may
reflect a number of ‘local’ optima of the diffusive and biochemical limiting
processes, granted various additional constraints of N supply, H,O availability,
and the extent of respiratory losses (cf. Jones, 1976).
In the context of early vascular plants, we may note particularly the following
points:
The enzyme RUBSICO was probably similar kinetically to the extant
eukaryote enzymes, which, as has been pointed out above, are kinetically
similar despite the substantial range of in vivo CO, and 0, concentrations
which they encounter Uordan & Ogren, 1981; Lorimer, 1981; Yeoh et al.,
1981).
The absolute atmospheric CO, levels have been rather above the current
levels, while the 0, level may have been 0.1-0.5 of the present atmospheric
level, i.e. the ratio of carboxylase to oxygenase activity would have been
higher than it is now for an enzyme with similar kinetic properties.
Palaeozoic vascular plants were anatomically C, (rather than C,) plants; if
we can take the carbon isotope ratio (6’,C) of Palaeozoic organic remains
PHYSIOLOGY AND FOSSIL PLANTS
119
at face value (i.e. ignore diagenetic effects), then they were also
physiologically C, plants (see O'Leary, 1981; Troughton, 1971).
Some recent work on photosynthesis and transpiration in liverworts with
(Murchunliu foliuceu Mitt.) and without (Moncleu forsteri Hook.)
intercellular air spaces showed that the rate of photosynthesis on the basis
of the external thallus area was no greater in Murchunliu than in Monoclea,
but that the H,O loss per unit net photosynthesis was lower, under
identical conditions, in Marchunliu than in Monoclea (Green & Snelgar,
1982). These findings suggest that economy of water use rather than
enhanced net photosynthesis (on an external area basis) was a major early
selective advantage of intercellular air spaces in terrestrial plants
(cf. Pickard, 1982). however, other marchantiaceous species studied
(Bjorkman & Gauhl, 1968; Fock, Krotkov & Canvin, 1969) have up to five
times the light-saturated rate of photosynthesis in air than was reported for
Marchantia foliuceu (all rates on an external area basis), thus suggesting that
the increased area of photosynthetic cells exposed to the gas phase as a
result of the occurrence of intercellular spaces in the Marchantiales can
lead to rates of photosynthesis higher than could be achieved with a solid
thallus.
While the area of photosynthetic cell surface in contact with the gas phase is a
very significant factor in determining the photosynthetic capacity of an
organ in air at light saturation, the view (e.g. Nobel, 1977) that genotypic
and phenotypic (e.g. in response to photon flux density for growth)
variations in the photosynthetic rates of leaves (on an external area basis)
disappear when the data are expressed on the basis of internal leaf area is
clearly an over-simplification (e.g. Harvey, 1980; Raven & Glidewell,
1975). Accordingly, the area of (putatively) photosynthetic cells exposed to
intercellular air spaces in fossil plants is probably not directly related to the
capacity for photosynthesis, although it probably does indicate an upper
limit (1-2 pmol CO, (m2 internal area)-' S K I ) ,
APPENDIX 4: THE SIGNIFICANCE OF XYLEM WATER TRANSPORT FOR SUPPLYING WATER
TO CELLS PHOTOSYNTHESIZING WITH AIR AS THE CO, SOURCE
For a plant with the dimensions of Eohostimella or Cooksoniu (i.e. an aerial axis
100 mm long and 1 mm in diameter) photosynthesizing at 1 pmol CO,
(m2 aerial axis surface area)-' s-' (Nobel, 1977; Raven & Glidewell, 1981), the
analysis of Appendix 2 shows that, with 227 g H,O lost per g dry weight gain,
some 428 ng H,O s-' is lost by the photosynthesizing axis. If a linear gradient
of water potential along the axis is assumed, a xylem-less plant such as
Eohostimellu with a specific H,O conductance of lo-" m2 s-' Pa-' (Appendix 1)
must have a $, at the apex of 27.3 MPa more negative than the $, at the
base. For Cooksoniu, assuming a central xylem cylinder occupying 0.01 of the
transverse areas of the axis (Raven, 1977a), and a xylem H,O conductance of
lo-' m2 s-' Pa-', involves a JI, at the apex only 2.73 kPa more negative than
that at the base. Since a $, of -27.3 MPa has a substantial inhibitory effect on
the biochemistry of photosynthesis (Hsaio, 1973), there is very restricted scope
;,
for Eohostimellu to extract H,O from a soil with a significant negative $
J. A. RAVEN
120
Cooksoniu could, by contrast, maintain its axis #w at a relatively high (not very
negative) value, and thus permit photosynthesis, even when extracting H,O
from a soil with a relatively negative #w.
We may note that this rate of net CO, fixation, with a growth-associated rate
of respiration equal to 0.25 of gross photosynthesis (Raven, 1976), 1/3 of the
axis (50 mm length) underground, and a fresh weight/dry weight ratio of 10,
gives a relative growth rate of 0.01 d-', i.e. an accumulation of dry matter
which is only about twice the minimal maintenance respiration rate quoted by
Penning de Vries (1975a). A ratio of internal to external exposed area of 10
would give, for a plant with intercellular air spaces and stomata, and the same
dimensions as our idealized Eohostimella or Cooksoniu, a relative growth rate of
0.1 d-' if the photosynthetic rate on the basis of internal exposed area were
1 pmol CO, m-' s-I, i.e. a 20-fold excess of relative growth rate over specific
maintenance rate. The enhanced rate of photosynthesis would imply an H,O
loss in transpiration some ten times that for the Cooksoniu example (without
intercellular air spaces) used earlier; with the same xylem dimensions and xylem
specific conductance as in the earlier example the water flux would require a qW
at the apex some 27.3 kPa more negative than that at the base.
Woodhouse & Nobel (1982) present pertinent data on the xylem conductivity
of extant leptosporangiate ferns.
APPENDIX 5: T H E COSTS OF HOMOIOHYDRY AND DESICCATION-RESISTANCE
Table 1 shows the degree of desiccation-tolerance of vegetative nonvascular
and vascular plants. Intuitively, there could be costs (in terms of resource
diversion) associated with both the homoiohydric and the desiccation-resistant
mechanisms of surviving water shortage as vegetative plants. The
xylem/cuticle/stomata/intercellular space system of the homoiohydric plant must
divert resources from the production of more resource-acquiring machinery:
data reviewed by Penning de Vries (1975b) show that lignin and lipids are
intrinsically costly (energy per unit weight of product) to synthesize. The
additional costs for a plant to be desiccation-resistant rather than desiccationsensitive are less readily quantifiable, but may involve cell compositions and
Table 1. Taxonomic distribution of tolerance of desiccation in the vegetative state in extant non-vascular and
vascular plants
~~~~
Tolerance of desiccation
in the vegetative state
Intolerant
Tolerant
Non-vascular plants
Vascular plants
Most of the algae which normally live
fully submerged; many bryophytes
and vascular plant free-living
gametophytes of moist habitats.
Many algae which are exposed to air
for prolonged periods; most lichens;
many bryophytes.
Sporophytes (except those of
resurrection plants)
Sporophytes of a small fraction of
herbaceous plants (resurrection
plants)
Data drawn from reviews by Bewley (l979), Gaff (l980), Hsaio (1973) and Levitt (1972). The extent to
which the ability to withstand desiccation in the vegetative state correlates with the ability to withstand
freezing (which can also act by desiccating cells) is not clear.
PHYSIOLOGY AND FOSSIL PLANTS
121
architectures (e.g. a smaller degree of vacuolation) which are sub-optimal for
resource acquisition, e.g. in terms of surface/volume relationship (Walter &
Stadelmann, 1968), as well as the presence of repair mechanisms absent from
desiccation-sensitive plants.
The expression of these additional costs may be sought in the relative growth
rate of the organisms, in that resources used for the homoiohydric mechanism or
the desiccation-resistance mechanism cannot be used to produce more resourceacquisition apparatus. Comparisons here are very difficult: clearly organisms of
similar size must be compared, in view of the lower relative growth rates found
for larger organisms (see Blasco, Packard & Garfield, 1982). Comparing young
ruderal or competitive strategy plants (see Grime, 1979; Raven, 1981b; Raven,
Smith & Glidewell, 1979) we find that the highest reported relative growth rates
are about 0.4 d-' for both marine algae (Jackson, 1980: table 111) and terrestrial
vascular plants (Grime & Hunt, 1975). The data were obtained for light and
nutrient saturation, natural inorganic carbon levels, and with the temperature
for the land plant measurements higher than those for the algae. This latter
difference would tend to underestimate the potential growth rate for the algae
since, even if the lower temperatures were near optimal for the algae, there is a
clear tendency for an increase in maximum relative growth rates with
temperature for genotypes adapted to various temperatures (see Eppley, 1972).
The consideration notwithstanding, the available data suggest that the
maximum specific growth rate for the algae does not greatly exceed that of the
vascular plants, despite the vascular plants having to bear the costs of
homoiohydry while the algae (species of Laminaria and of Porphyra) with the
highest growth rates are relatively desiccation-sensitive and so do not have to
bear the (unquantified) cost of desiccation-resistance (cf. Fork & Oquist, 1981,
who discuss the relative desiccation resistance of species of Porphyru). The
relative growth rate of desiccation-tolerant poikilohydric plants which are
otherwise comparable with the vascular plants and the desiccation-sensitive
algae has not, to my knowledge, been shown to be as high as 0.4 d - '. We may
note that the use of 'natural' inorganic carbon levels does not greatly
disadvantage the terrestrial plant (with the stomata1 resistance between the
source CO, and RUBISCO: Raven, 1981a) relative to the aquatic plants
(where the greater diffusive resistance of water than of air tends to decrease the
CO, availability to RUBISCO: Raven, 1970, 1981a; Raven, Beardall &
Johnston, 1981; Smith & Walker, 1980).
The growth rate data are inconclusive with respect to costs associated with
the survival of water deficits in the vegetative state; further work aimed directly
at this problem is needed to overcome the difficulties inherent in the
promiscuous comparison of data in the analysis given above. The comparison is
both possible and worthwhile. Analysis of the data in terms of the plants
resistant to desiccation in their vegetative phase should certainly consider the
costs of the sort of anti-photoinhibition mechanisms descussed by Sigfidsson &
Oquist (1980) and Fork & Oquist (1981) (cf. Raven, 1981a), while it must be
borne in mind with respect to vascular plants that even those which are not
resurrection plants (i.e. able to tolerate vegetative dehydration) must have the
genetic capacity for desiccation tolerance in their seeds. T h e analysis of data of
this sort should not, of course, assume that the capacity for rapid growth is the
only, or even the major, criterion of plant fitness!
5
J. A. RAVEN
122
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