Botanical journal of the Linnean Sociedy (1990), 104: 175-186. With 4 figures
Bryophytes and plant strategy theory
J. P. GRIME, E. R. RINCON AND B. E. WICKERSON
Unit of Comparative Plant Ecology (N.E.R.C.),Department of Plant Sciences,
The University, Shefield SIO 2TN
GRIME, J . P., RINCON, E. R. & WICKERSON, E. B., 1990. Bryophytes and plant strategy
theory. In this paper reference will be made to three widely recurrent types of functional
specialization. These correspond to (1) .strategies* apparent in the established (adult) phase of the
life history, (2) strategies of the regenerative (juvenile) phase and (3) strategies ofgrowth response to
seasonal variation in temperature and moisture supply. In each case a comparison will be drawn
between the range af strategies displayed by bryophytes and that already described for vascular
plants. Reference will be made also to some of the implications of these strategy theories for the role
of bryophytes in the structure and dynamics of plant communities.
ADDITIONAL KEY WORDS:-Life
~
history - regeneration strategies.
CONTENIS
Introduction . . . . . . . . . . . . . . . . . .
Established strategies . . . . . . . . . . . . . . . .
Regenerative strategies.
. . . . . . . . . . . . . . .
Strategies of growth response to seasonal variation in temperature and moisture supply
Conclusions . . . . . . . . . . . . . . . . . .
References
. . . . . . . . . . . . . . . . . .
.
.
.
.
.
.
175
176
181
182
184
184
INTRODUCI‘ION
As the science of ecology matures, two rather different sets of activities and
objectives have captured the attention of research workers. The first, motivated
primarily by the curiosity and ingenuity of specialists, consists of the attempt to
identify the processes (demographic, genetic and biochemical) which influence
the behaviour of individual populations; two recent symposia (Dirzo &
Sarukhan, 1984; Gottlieb & Jain, 1988) reveal the extent to which this line of
enquiry is now committed to paths of increasingly refined analysis and narrowed
perspective. Some have argued strongly (e.g. Woolhouse, 1981; Harper, 1982)
that this very detailed research agenda represents the only reliable way to
achieve a satisfying explanation for ecological phenomena. It is doubtful whether
the time scale of this type of scholarship is compatible with the pressing demands
upon ecology for enlightened management of the biosphere.
The second set of activities and objectives, now evident within ecological
research, refers to the same sources of information as the first but seeks to
*In this paper stratrgies are defined (Grime, 1979) as ‘‘groupings of similar or analogous genrtic
characteristics which recur widely among species or populations and cause thrm t o rxhihit similaritirs i n
ecology”.
0024-4074/90/090175
+ 12 SOS.OO/O
175
01990 The Linnean Society of London
J. P. GRIME ET AL.
176
preserve a broader perspective. Crucial to this philosophy is the assertion that we
can introduce priorities into ecological thinking by recognizing that, at a
fundamental level, patterns of evolutionary and ecological specialization are
constrained such that organisms can be classified within a common framework of
basic functional types. Where this approach proves to be valid, it will provide
opportunities for extrapolation from the few intensively studied organisms and
habitats to the much larger number which have been neglected. In addition, the
ability to classify organisms into functional types has major applications in
community ecology and ecosystem theory.
ESTABLISHED STRATEGIES
With respect to both autotrophs and heterotrophs, a general functional
classification has been proposed which coincides with variation in the quality
and durational stability of the habitat or niche to which the organism has been
attuned by natural selection (Ramenskii, 1938; Grime, 1974; Southwood, 1977;
Greenslade, 1983; Pugh, 1980; Cooke & Rayner, 1984; Reynolds, 1987).
According to this theory there are three extremes of evolutionary specialization
(ruderals, competitors and stress-tolerators) which recur widely in many taxa
and in all major biomes and correspond to particular conditions of resource
supply (Table 1). The extreme conditions favouring either ruderals, competitors
or stress-tolerators form only part of the range of available environments. The
full spectrum of conditions occurring in nature and their associated strategies can
be described as an equilateral triangle in which the relative importance of
competition, stress and disturbance is represented by three sets of contours (Fig.
IA). This model recognizes not only the three categories of Table 1, but also a
range of intermediate strategies capable of exploiting less extreme equilibria
between stress, disturbance and competition. A detailed description of this
model, its implications and the measures necessary to test it, is available
elsewhere (Grime, 1979, 1988), and discussions of its applicability to bryophytes
are included in During (1979) and Longton (1988). Here attention will be
confined to aspects of plant strategy theory of particular relevance to bryophytes.
In Table 2, plant attributes associated with the three primary strategies are
summarized and those which appear to be especially relevant to the classification
of bryophytes are indicated in bold type. From this table it is immediately
apparent that numerous bryophytes can be found which conform either to the
ruderal (e.g. Pleuridium acuminatum, Leptobyum pyriforme, Pottia truncata) or to the
stress-tolerant (e.g. Grimmia puluinata, Andreaea rupestris, Racomitrium lanuginosum)
categories, but none corresponds to the competitive strategy. On first inspection
this may seem anomalous since it is well known that some bryophyte genera
(Sphagnum, Polytrichum, Pleurocium, Brachthecium, Pseudoscleropodium) are capable of
TABLE
1 . Conditions of resource supply associated with three primary strategies
I . Ruderal (ephemeral)
2. Competitor
3. Stress-tolerator
Temporarily abundant
Continuously abundant but subject to local and/or progressive depletion as
resources are exploited
Continuously scarce
BRYOPHYTES AND PLANT STRATEGY
I77
Figure 1. A. Model describing the various equilibria between competition, stress and disturbance in
vegetation and the location of primary and secondary strategies. C, competitor; S, stress tolerator;
R, ruderal; C-R, competitive-ruderal; S-R, stress tolerant ruderal; C-S, stress tolerant competitor;
C-S-R, ‘C-S-R-strategist’. I,, intensity of competition (
); intensity of stress ( . -); I,,
intensity of disturbance ( - -- ). B-E. The strategic range of four life forms: B, herbs; C, trees and
shrubs; D, bryophytes; E lichens.
dominating the plant biomass in various habitats and, at least on a local scale,
are often able to suppress the establishment and growth of vascular plants. Here
it is of vital importance to draw a distinction between the ability of a plant to
compete for resources and its capacity for dominance. Thus, many of the
bryophytes (and small herbs and shrubs) which eventually dominate
unproductive habitats of low biomass, have achieved their status not through
any exceptional ability to monopolize resource capture in competition with
neighbours; rather they have assumed dominance slowly through the capacity to
retain and protect captured resources in conditions where stronger competitors
suffer greater losses through higher rates of tissue turnover and ineffective
defences against herbivory (Grime, 1979; Chapin, 1980; Coley, 1983; Coley,
Bryant & Chapin, 1985).
Although competitors s m u strict0 are not represented among bryophytes
(Grime, 1977; Longton, 1988), certain species such as Brachythecium rutabulum,
have growth characteristics which allow them to be classified as stronger
competitors for resources relative to bryophytes of more oligotrophic conditions.
Support for this conclusion is provided in Fig. 2, which compares the light
‘foraging ability’ of six bryophytes. Essentially, the experiment measures the
capacity of each species to exploit beams of spatially predictable, unfiltered light
projected into shaded containers over a period of 3 months. The results are
expressed as a concentration index (dry weight of thallus per unit area in
unfiltered light divided by dry weight of thallus per unit area in adjacent shade
light) which for each species is plotted against the mean relative growth rate of
control plants grown in uniformly unfiltered light of low intensity over the
experimental period. Marked differences in concentration index are apparent
and it is evident that the four species of higher potential relative growth rate and
characteristic of mesic habitats (Brachythecium rutabulum, Eurynchium praelongum,
Pseodoscleropodium purum and Thuidium tamariscinum) were more effective colonists
J. P. G R I M E E l AL.
I78
TABLE
2. Some characteristics of competitive, stress-tolerant and ruderal plants
(i) Morphology
1. Life forms
2. Morphology of shoot
3. Leaf form
4. Canopy structure
(ii) Life-history
5. Longevity of
established phase
6. Longevity of leaves
and roots
7. Leaf phenology
Competitive
Stress-tolerant
Ruderal
Herbs, shrubs and trees
Lichens, bryophytes,
herbs, shrubs and trees
Extremely wide range of
growth forms
Herbs, bryophytes
High dense canopy of
leaves. Extensive lateral
spread above and below
ground
Robust, often
mesomorphic
Rapidly-elevating
monolayer
12. Regenerative
strategies*
Often small or
Various, often
leathery, or needlelike mesomorphic
Often multilayered. If
Various
monolayer, not rapidlyelevating
Long or relatively short
Long-very long
Very short
Relatively short
Long
Short
Well-defined peaks of leaf
production coinciding
with periods of maximum
potential productivity
Produced after (or, more
8. Phenology of seed
or spore production rarely, before) periods of
maximum potential
productivity
9. Frequency of seed
Established plants usually
or spore production reproduce earh year
10. Proportion of
annual production
devoted to seeds or
spores
11. Perennation
Small stature, shoot
limited lateral spread
Small
Dormant buds and sceds
or spores
Evergreens, with various Short phase of leaf
patterns of leaf
production in period of
production
high potential
productivity
No general relationship
Reproduction occurs
between time of flowering early in the lifeand season
history
Intermittent
reproduction over a
long life-history
Small
Stress-tolerant leaves
Large
Dormant seeds or
spores
s, w, B,
V, S, W, B,
(iii) Physiology
13. Maximum potential Rapid
relative gowthrate
14. Response to stress Rapid morphogenetic
responses (root-shoot
ratio, leaf area, root
surface area) maximizing
vegetative growth
15. Photosynthesis and Strongly seasonal,
uptake of mineral
coinciding with long
nutrients
continuous period of
vegetative growth
16. Acclimation of
Weakly developed
photosynthesis,
mineral nutrition
and tissue
hardiness to
seasonal change in
High frequency of
reproduction
Slow
Rapid
Morphogenetic
responses slow and
small in magnitude
Opportunistic, often
uncoupled from
vegetative growth
Rapid curtailment of
vegetative growth,
diversion of
resources into seed
or spore production
Opportunistic,
coinciding with
vegetative growth
Strongly developed
Weakly developed
BRYOPHYTES AND PLANT STRATEGY
179
TABLE
2.-continued
Competitive
temperature, light
and moisture
eupplY
17. Storage of
photosynthate and
minerd nutrients
(iv) Miscellaneous
18. Litter
19. Palatability to
Ruderal
Stress-tolerant
confinrd to d
Most photosynthate and
Storage systems in
mineral nutrients are
leaves, stems and/or
rapidly incorporated into roots
vegetative structure but a
proportion is stored and
forms the capital for
expansion of growth in
the following growing
season
s or
spores
Copious, not usually
persistent
Various
Sparse, often
persistent
LOW
Sparse, not usually
persistent
various, ofcen high
Usually small
Various
Small - very small
WASpcd.lized
herbivorer,
20. Genome size
*Key to regenerative strategies: V, vegetative expansion; S, seasonal regeneration in vegetation gaps; W,
numerous small wind-dispersed seeds or spores; B,, persistent seed or spore bank; B,,, persistent seedling or
sporeling bank.
6-0
I
Erochvthecium rulobulufl
5-0
Thuidium tomariscinum
4-a
0
8
.-
--e
c
.-0
3-c
c
0
c
0
0
2.0
ofopecururn
1
0
0.02
1
I
I
0-04
0.06
0-08
I
0.10
I
0-12
C 4
Relatlve growth rate (mg rng-' day-')
Figure 2. Comparison of the ability of six bryophytes of contrasted ecology grown in a constant
mosaic of high (48W m-Y)and low (9 W m-Y)irradiance for 110 days to concentrate their biomass
in the areas of high irradiance. The concentration indices are plotted against the relative growth
rate of individuals of the same species grown concurrently at a uniformly high irradiance
(49 W m-') in the same environmental conditions (temperatures 18°C (day), 12°C (night),
photoperiod 12 h). 95% confidence limits are indicated by the horizontal and vertical lines. Thc
regression equation for the fitted line i s j = 0.057 3 9 . 2 2 ~(P< 0.05).
+
J. P. GRIME E l AL.
I80
1I
L S
i
Brochylhecium
rufabulum
Eurynchium
proelongum
Thuidium
lamariscinum
4
Pseudoscleropodium
purum
H L S
H L S
fissidens
crisf af us
Thamnium
ohpecwum
Figure 3. Comparison of the ability of six bryophytes of contrasted ecology to exploit artificial
sunflecks of 20 min duration and randomly distributed in space and time. The histograms describe
the mean relative growth rate (&95%confidence limits) over a period of 110 days exposure to high
irradiance (H) (48 W m-*), low irradiance (L) (9 W m-') and low irradiance+sunflecks (S).
Temperatures: 18°C (day), 12°C (night); photoperiod: 12 h.
of the local patches of unfiltered light than the two slow-growing species of
shaded limestone outcrops ( Thamnium alopecurum, Fissidens cristutus) , These data
are clearly consistent with the strategy predictions outlined in Table 2 in that
greater morphological plasticity was evident in the four species normally found
growing in closed herbaceous vegetation, whereas the two bryophytes associated
with deeply shaded conditions were relatively unresponsive.
In the same experiment the six bryophytes were compared with respect to
their capacity to exploit spatially unpredictable irradiance in the form of
artificial sunflecks each approximately 20 mm in diameter and of 20 minutes
duration and located at random by intermittent rotation of a perforated disc
filter over a honeycomb of short vertical reflective tubes (Rincon, 1985). The
histograms in Fig. 3 compare the relative growth rates of the bryophytes in the
sunfleck treatment and in two uniform levels of irradiance comparable
respectively with the shade and sunfleck components of the sunfleck treatment.
The data confirm the greater ability of the four grassland bryophytes to grow
more rapidly at both high and continuously low irradiance. In only one of these
species, Thuidium tamariscinum, is there any appreciable benefit from the
introduction of sunflecks. I n the two slow-growing bryophytes, however, there is
clear evidence that sunflecks provided a major stimulus to dry matter
production, These results support the hypothesis (Table 2) that morphological
plasticity is of reduced importance in the mechanisms of resource acquisition of
bryophytes exploiting chronically unproductive habitats.
In the slow-growing, long-lived bryophytes or unproductive biomes, habitats
or niches, growth is intermittent and the life span of individual vegetative parts is
long. The slow turnover of tissues and cells dictates that for most of the time
differentiating tissue forms a small proportion of the plant's biomass, severely
BRYOPHYTES AND PLANT STRATEGY
181
limiting the capacity to adjust to environmental fluctuations through
morphogenetic plasticity. During their long functional life, tissues are often
exposed to severe and widely different environmental conditions. It is hardly
surprising, therefore, to find that there is an extensive literature supporting the
assertion (Table 2) that plasticity in stress-tolerant bryophytes is usually
expressed physiologically and is often both rapid and reversible. Examples of this
phenomenon are available from pioneer studies of modifications in carboxylating
capacity and in the temperature optimum of photosynthesis in relation to
varying light intensity and season (Miyata 8z Hosakawa, 1961; Hicklenton &
Oechel, 1976; Oechel, 1976; Proctor, 1982).
REGENERATIVE STRATEGIES
Through the work of several ecologists and evolutionary biologists (Stebbins,
1951, 1971, 1974; Wilbur, Tinkle & Collins, 1974; Grubb, 1977; Gill, 1978;
Grime, 1979), there has been gradual recognition of the need for separate
consideration of the strategies exhibited by organisms during the regenerative
(juvenile) phase of their life histories. For plants this has resulted in the proposal
(Table 3) that there are five major types of regenerative strategies characterized
by differences in features such as parental investment, mobility and dormancy.
Each of these strategies recurs widely and appears to confer predictable
capacities and limitations upon the ecology of the organism. Moreover, as
recognized for bryophytes by During (1979), the same genotypes may be capable
of regenerating by several mechanisms; this has prompted the suggestion (Grime,
1979) that ecological amplitude is determined not only by genetic variability
and phenotypic plasticity, but also by regenerative flexibility, which is a function
of the number of’regenerative strategies exhibited by the genotype, population or
species.
A review of the regenerative strategies listed in Table 3 is provided in Grime
(1979), which contains also a discussion of their role in successional and cyclical
vegetation changes. Both for vascular plants and bryophytes there is now an
urgent need for data collection and objective analysis to seek evidence for or
against the co-occurrence of regenerative attributes in the sets corresponding to
the strategies defined in Table 3. Preliminary cluster analyses applied to a data
base for 273 common vascular plant species of the British flora (Grime, Hunt &
Krzanowski, 1987) have confirmed the existence of recurring syndromes of
morphological and physiological traits. There appear to be excellent
opportunities to apply this approach to bryophytes although, as in the case of
vascular plants, data sources remain somewhat unbalanced, with morphological
criteria (e.g. seta length, peristome structure, spore dimensions) ‘swamping’
those relating to spore longevity, germination requirements and sporeling
requirements for establishment. A particular limitation is apparent with respect
to knowledge of spore persistence in the soil. In comparison with the voluminous
literature on seed banks (Thompson, 1987), we are comparatively ignorant of
the distribution and role of bryophyte spore banks. The pioneer studies of
Furness & Hall (1981) and During & Ter Horst (1983) provide excellent models
for future investigations.
J. P. GRIME E T AL.
I82
TABLE
3. Five regenerative strategies of widespread occurrence in terrestrial vegetation
Strategy
Functional
characteristics
Conditions under
which strategy
appears to enjoy
a selective
advantage
Examples
Vascular
plants
Bryophytes
Vegetative
expansion (V)
New shoots
vegetative in origin
and remaining
attached to parent
plant until well
established
Productive or
Reynoutria
unproductive habitats juponica
subject to low
intensities of
disturbance
Pseudoscleropodium
purum
Seasonal
regeneration (S)
Independent offspring
(seeds or vegetative
propagules) produced
in a single cohort
?
Persistent seed or
spore bank (B,)
Viable but dormant
seeds or spores
present throughout
the year; some
persisting more than
12 months
Offspring numerous
and exceedingly
buoyant in air;
widely dispersed and
often of limited
persistence
Habitats subjected to Impaliens
seasonally predictable glandulifera
disturbance by
climate or biotic
factors
Habitats subjected to Calluna vulguris
temporally
unpredictable
disturbance
Numerous widely
dispersed seeds or
spores (W)
Persistent juveniles Offspring derived
from an independent
(B,)
propagule but
seedling or sporeling
capable of long-term
persistence in a
juvenile state
Physcomitrium sphaericum
Funaria hygrometrica
Habitats subjected to Salix caprea
spatially
unpredictable
disturbance or
relatively inaccessible
(cliffs, walls, tree
trunks, etc.)
Sanicula europaea ?
Unproductive
habitats subjected to
low intensities of
disturbance
STRATEGIES OF GROWTH RESPONSE T O SEASONAL VARIATION IN TEMPERATURE
AND MOISTURE SUPPLY
Although the majority of bryophytes are relatively tolerant of desiccation,
growth is usually confined to seasons which maintain the tissues in a fully
hydrated state for significant periods of time. In grasslands and tall herb
communities of the British Isles, a consequence of this restriction is the tendency
for the biomass of the bryophyte component to show a pronounced bimodal
fluctuation each year, with peaks occurring in the spring and autumn (Fig. 4).
This pattern has been confirmed by seasonal sampling of natural bryophyte
assemblages (Al-Mufti et al., 1977; Furness, 1980) and by growth analyses using
implanted cuttings of selected species maintained in small chambers in chemical
and climatic equilibrium with the turf environment (Rincon & Grime, 1988a).
These studies, in conjunction with laboratory experiments in which various
species were grown in temperature-gradient incubators (Furness & Grime,
1982a, b) confirm the widespread capacity of British bryophytes to grow
relatively rapidly at low temperatures.
BRYOPHYTES AND PLANT STRATEGY
183
Figure 4. Seasonal changes in the shoot biomass of the main vegetation components in a stand of
Filipmdula ulmaria (Meadowsweet) situated on a damp, calcareous north-facing terrace in Northern
England: A, Filipenduala ulmaria; B, Mercurialis perennis; C, Bryophytes; D, Anemone nemorosa (Al-Mufti
el al., 1977).
It is well documented (Proctor, 1982) that many bryophytes are able to
maintain photosynthesis at low temperatures. Further research seems necessary,
however, to explain how growth itself (i.e. the expansion of new tissues) is
achieved under cold conditions. In particular it may be instructive to test for the
existence in bryophytes of the strategy which appears to facilitate growth at low
temperatures in many vernal vascular plants. This proposed mechanism rests on
the suggestion (Grime & Mowforth, 1982; Grime, 1983), first, that the major
limiting factor upon spring growth is the inhibitory effect of low temperatures
upon cell division, and second, that this limitation is circumvented by plants
which confine cell division to warmer periods, store unexpanded cells in the
meristems and subsequently achieve growth at low temperatures, mainly by cell
enlargement. This hypothesis is supported by controlled environment studies
(e.g. Hartsema, 1961) which have shown the dependence of spring growth upon
preceding exposure to warm summer temperatures. Perhaps, more relevant still
to the behaviour of bryophytes, is the phenomenon of ‘stored growth’ (Salter &
Goode, 1967) whereby an acceleration of shoot growth after drought is achieved
in many cereals and grasses by rapid inflation of cells which have continued to
accumulate in an unexpanded state during periods of desiccation. The water
relations of bryophytes dictate that many species exist for considerable periods in
I84
J. P. GRIME E T AL.
a semi-dehydrated condition. There is need to determine the extent to which cell
divisions continue in desiccated bryophytes and to assess the relevance of this
process to the unusual capacities of many species to expand new shoots under
low temperatures.
CONCLUSIONS
Patterns of ecological specialization in bryophytes exhibit strong parallels with
those recognized in vascular plants. However, as in the case of pteridophytes
(Grime, 1985) and individual families of angiosperms (Grime, 1984; Hodgson,
1986), phylogenetic constraints have restricted the ability to adopt certain
strategies. The unsophisticated transport systems and water relations of
bryophytes have limited their capacity to monopolize resource capture and
dominate vegetation in productive, undisturbed habitats. Failure to achieve the
competitor strategy has relegated bryophytes to a surbordinate role in perennial
vegetation of high productivity. Despite this limitation, some bryophytes are
capable of vegetation dominance. Robust species frequently occur as the major
contributors to the plant biomass in bogs, moist grasslands and on the floor of
boreal forests, and they are also conspicuous during the early stages of primary
succession of skeletal habitats where they may facilitate (Connell & Slatyer,
1977) the establishment of vascular plants. In these circumstances, however,
dominance is related to efficient retention and conservative utilization of
captured resources rather than superior competitive ability.
Further research is required to characterize the regenerative strategies of
bryophytes. It is already evident, however, that regeneration involving the
production of numerous widely dispersed spores (W in Table 3) is of widespread
importance in epiphytic species and in bryophytes exploiting other relatively
inaccessible sites (e.g. cliffs, walls and forest clearings), Persistent spore banks in
the soil are important in the exploitation of intermittent habitats by certain
ephemerals; we suspect that this regenerative strategy is of wider ecological
significance in bryophytes than is currently appreciated. Regeneration by
vegetative expansion is important not only in slow-growing perennial bryophytes
occupying severe environments or microhabitats, but also in the faster-growing
pleurocarpous mosses which coexist with vascular plants in productive
grasslands, tall herb communities and in the ground layer of deciduous
woodlands.
Strategy concepts may also contribute to a mechanistic understanding of the
unusual ability of many bryophytes of cool temperate and continental climates
to grow at low temperatures. There is a need to determine whether bryophytes
share the capacity of vernal geophytes and grasses for 'stored growth'.
REFERENCES
AL-MUFII, M. M., SYDES, C. L., PURNESS, S. B., GRIME, J. P. Br BAND, S. R., 1977. A quantitativc
analysis of shoot phenology and dominance in herbaceous vegetation. journal n f Ecology, 65: 759-791.
CHAPIN, F. S., 1980. The mineral nutrition of wild plants. Annual Reuiew of Ecologv and Systematics, 11:
233-260.
CLAPHAM, A. R., ~ I U I I N T.
, C. & WARBURG, E. F., 1981. Excursion Flnra @'the British Isles. 3rd edition.
Cambridge: Cambridge University Prcss.
COLEY, P. D., 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forcut.
Ecological Monographs, 53: 209-233.
BRYOPHYTES AND PLANT STRATEGY
185
COLEY, P. D., BRYANT, J. P. & CHAPIN, 1<'. S., 1985. Resource availability and plant antiherbivore
defence. Science, 230: 895-899.
DIRZO, R. & SARUKHAN,J. (Eds), 1984. Perspectives on Plant Population Ecology. Sunderland, Massachusetts:
Sinauer Associates Inc.
DURING, H. J., 1979. Life strategies of bryophytes: a preliminary review. Lindbergia, 5: 2-18.
DURING, H. J. & TERHORST, B., 1983. The diaspore bank of bryophytes and ferns in chalk grassland.
Lindbergia, 9: 57-64.
FURNESS, S. B. & HALL, R. H., 1981. An explanation of the intermittent occurrence of Pkyscomitrium
sphaericum (Hedw.) Brid. Journal of Bryology, 11: 733-742.
FURNESS, S. B. & GRIME, J. P., 1982a. Growth rate and temperature responses in bryophytes. I. An
investigation of BrackYthecium rutabulum. Journal if Ecology, 70: 513-523.
FURNESS, S. B. & GRIME, J. P., 1982b. Growth rate and temperature responses in bryophytes. II. A
comparative study of species of contrasted ecology. Journal of Ecology, 70: 525-536.
GOTTLIEB, L. D. & JAIN, S. K. (Eds), 1968. Plant Evolutionary Biology. London: Chapman & Hall.
GREENSLADE, P.J. M., 1983. Adversity selection and the habitat temple!. American Naturalist, 122: 352-365.
GRIME, J. P., 1974. Vegetation classification by reference to strategies. Nature, 250: 26-31.
GRIME, J. P., 1977. Evidence for the existence of three primary strategies in plants and its rrlevancc to
ecological and evolutionary theory. American Naturalist, 111: 1169-1194.
GRIME, J. P., 1979. Plant Strategies and Vegetation Processes. Chichester: Wiley.
GRIME, J. P., 1983. Prediction of weed and crop response to climate based upon measurements of nuclear
DNA content. In Aspects of Applied Biology. 4: Influence if Environmental Factors on Herbicide Peiformance and Crop
and Weed Biology: 87-98. National Vegetable Research Station, Wellesbourne, Warwick: The Association of
Applied Biologists.
GRIME, J. P., 1988. The C-S-R model of primary plant strategies origins, implications and tests. In L. D.
Gottlieb & S. K. Jain (Eds), Plant Evolutionary Biology: 371-393. London: Chapman & Hall.
GRIME,]. P. & MOWFORTH, M.A., 1982. Variation in genome size-an ecological interpretation. Nature,
299: 151-153.
GRIME, J. P., CRICK, J. C. & RINCON, j. E., 1986. The ecological significance of plasticity. In D. H.
Jennings & A. J. Trewavas (Eds), Plasticiry in Plants: 5-29. Proceedings of the Society of Experimental
Biology 40th Symposium. Cambridge: The Society for Experimental Biology.
GRIME, J. P., HUNT, R. & KRZANOWSKI, W. J., 1987. Evolutionary physiological ecology of plants. In
P. Calow (Ed.), Evolutionary Physiological Ecology: 105-125. Cambridge: Cambridge University Press.
GRUBB, P. J., 1977. The maintenance of species-richness in plant communities: the importance of the
regeneration niche. Biological Reviews, 52: 107-145.
HARPER, J. L., 1982. After description. In E. I. Newman (Ed.), The Plant Communi!J as a Working Mechanism.
Special Publication No. I BES: 11-25. Oxford: Blackwell Scientific Publications.
HARTSEMA, A. M., 1961. Influence of temperature on flower formation and flowering of bulbous and
tuberous plants. In W. Ruhland (Ed.), Handbuch der !JlanzenpkYsiologie. 16: Aussenfaktoren in Wachstum und
Entwicklung: 123-167. Berlin: Springer.
HICKLENTON, P.R. & OECHEL, W. C., 1976. Physiological aspects of the ecology of Dicranumfuscescens in
the subarctic. I. Acclimation and acclimation potential of C0 2 exchange in relation to habitat, light and
temperature. Canadian Journal of Bola'!)', 54: 1104-1119.
HODGSON, J. G., 1986c. Commonness and rarity in plants with special reference to the Sheffield flora. 3.
Taxonomic aspects. Biological Conservation, 36: 275-296.
HOFFMAN, G. R., 1966. Ecological studies of Funaria kYgrometrica (Hedw.) in eastern Washington and
Northern Idaho. Ecological Monographs, 36(2): 157-180.
LONGTON, R. E., 1988. The Biology if Polar Bryophytes and Lichens. Cambridge: Cambridge University Press.
MIYATA, I. & HOSAKAWA, T., 1961. Seasonal variations of the photosynthetic efficiency and chlorophyll
content of epiphytic mosses. Ecology, 42: 766-775.
OECHEL, W. C., 1976. Seasonal patterns of temperature response of C0 2 flux and acclimation in Arctic
mosses growing in situ. PhotoV~nthetica, 10: 44 7-456.
PROCTOR, M. C. F., 1982. Physiological ecology: water relations, light and temperature responses, carbon
balance. In A. J. E. Smith (Ed.), BryopkYte Ecology: 333-381. London: Chapman & Hall.
PUGH, G. J. F., 1980. Strategies in fungal ecology. Transactions of the British Mycological Sociery, 75: 1-14.
RAMENSKII, L. G., 1938. Introduction to the Geobotanical Stut[y if Complex Vegetations. Moscow: Selkhozgiz.
REYNOLDS, C. S., 1984. The ecology of freshwater phytoplankton. Cambridge: Cambridge University Press.
RINCON, E., 1986. Experimental investigations if the ecology ifbryopkYtes in calcareous grassland in Northern England.
Unpublished PhD thesis of the University of Sheffield.
RINCON, E. & GRIME, J. P., 1988a. An analysis of seasonal patterns of bryophyte growth in a natural
habitat. Journal if Ecology, 77: 447-455.
RINCON, E. & GRIME, J. P., 1988b. Plasticity and light interception by six bryophytes of contrasted
ecology. Journal of Ecology, 77: 439-446.
SALTER, P. J. & GOODE, J. E., 1967. Crop responses to water at different stages of growth. Research
Review, 2. East Mailing, Kent: Commonwealth Bureau of Horticulture and Plantation Crops.
SMITH, A. J. E., 1978. The Moss Flora of Britain and Ireland. Cambridge: Cambridge University Press.
186
J. P. GRIME ET AL.
SOUTHWOOD, T. R. E., 1977. Habitat, the template for ecological strategies? Journal of Animal Ecology, 46:
337-365.
STEARNS, S. C., 1976. Life-history tactics: a review of the ideas. Q.uarterry Review of Biology, 51: 3--47.
THOMPSON, K., 1987. Seeds and seed banks. In I. H. Rorison, J.P. Grime, R. Hunt, G. A. F. Hendry &
D. H. Lewis (Eds), Frontiers qf Comparative Plant Ecology: 23-34. London: Academic Press.
WOOLHOUSE, H. W., 1981. Aspects of the carbon and energy requirements of photosynthesis considered in
relation to environmental constraints. In C. R. Townsend & P. Calow (Eds), Physiological Ecology: an
Evolutionary Approach to Resource Use: 51-85. Oxford: Blackwell Scientific Publications.