the maintenance of species-richness in plant communities

Biol. Rev. (1977), 52, pp. 107-145
BRC PAH 52-4
THE MAINTENANCE OF SPECIES-RICHNESS
IN PLANT COMMUNITIES: THE IMPORTANCE OF THE
REGENERATION NICHE
BY P. J. GRUBB
Botany School, University of Cambridge
(Received 7 September 1976)
CONTENTS
I. Introduction . .
11. Mechanisms not involving the process of regeneration
(a) Variation in life-form . .
(b) Phenological spread . .
(c) Fluctuations in the environment .
(d) Balancedmixturea .
(e) Variation in competitive ability with physiological age
111. Induction to the involvement of regeneration .
IV. Definition of a plant’s niche . . . . .
V. Patterns of regeneration in different plant communities
VI. Examples of differentiation in the regeneration niche .
(a) Production of viable seed .
(a) Dispersal .
(c) Germination . . . . . .
(d) Establishment of seedlings .
(e) Further development of the immature plant
.
VII. Discussion .
VIII. summary .
IX. References . . .
.
I. INTRODUCTION
. 107
. 108
. 108
. 111
. I11
. 113
. 114
. 116
. I19
. 119
. . . I21
. I21
. 125
. 126
. 128
. 130
. I31
. . . I34
. 136
According to ‘ Gause’s hypothesis ’ a corollary of the process of evolution by natural
selection is that in a community at equilibrium every species must occupy a different
niche. This idea is generally accepted by zoologists (Krebs, 1g72), but most botanists
find difficulty in understanding how all the species in a species-rich plant community
can possibly occupy different niches. Although many different factors are involved in
the full definition of an animal’s niche, one can fairly readily imagine sufficient niches
for all the animal species known, using food-requirements alone; the million or so
animal species can easily be ‘explained’ in terms of the 300000 species of plants
(so many of which have markedly different parts such as leaves, bark, wood, roots,
etc.) and the existence of three to four tiers of carnivores (Hutchinson, 1959). There is
no comparable ‘explanation’ for autotrophic plants ; they all need light, carbon dioxide,
water and the same mineral nutrients.
Many ideas have been put forward to explain the indefinite co-existenceof numerous
species in particular communities, but it is the author’s contention that most of these go

108 P. J. GRUBB
only a very little way toward explaining the persistence of numerous species in the more
species-rich communities. One reason for the lack of understanding on the part of
most botanists results from their failure to take into account the phenomenon of
regeneration in plant communities, which was first discussed in general terms by
A. S. Watt in 1947. Most communities that are not successional are longer-lived than
their constituent individual plants. When any one plant individual dies, a gap is
created and a new individual ultimately takes its place. It may or may not be of the
same species and this is the crucial point. Heterogeneity of the environment (physicochemical
and biotic) does in fact ensure that the replacement plant (or plants) is
sometimes of the same species as died and sometimes not. It is suggested in this review
that this replacement stage is of great importance not only for understanding speciesrichness
as such but also for understanding the basic processes of evolutionary
divergence in plants and for the management of plant communities in conservation.
In order to view the problem as a whole, ideas not involving regeneration are
considered briefly in the first part of the review (Section 11), and ideas that do involve
regeneration are covered in more detail in the second part (Sections 111-VII). The
nomenclature follows that used in the papers quoted except where otherwise indicated.
11. MECHANISMS NOT INVOLVING THE PROCESS OF REGENERATION
(u) Vuriation in life-form
It is useful to consider initially the various dominance-structures found in plant
communities. The findings of many ecologists on the structures of natural communities
are reflected in the dominance-diversity ideas of Whittaker (1965), who concluded
that plant communities could be represented by a spectrum of curves relating the
importance values of species and the number of species (Fig. I). In the communities
poorest in species, represented by type (u) curves, one species has a much greater
productivity (or cover-abundance or standing crop) than any others and there is a
short series of successively less productive species. At the other extreme (type (c)
curves) there is no clear single dominant, but a group of most productive species
followed by a larger group of moderately productive species and a final group of rare
species contributing little to the productivity of the community. Many communities
are intermediate in nature (type (b) curves).
The co-existence of species in type (u) communities can largely be explained in
terms of complementarity of life-form. Very few, if any, dominant species are able to
utilize the resources of an area totally or block off with complete success those they do
not use themselves. Thus it is very likely that epiphytes (often cryptogamic) will be
found on the mature dominant. Almost always one or a few species of shade-tolerant
herbs or subshrubs can co-exist - their shoots receiving just enough light for persistence
if not for flowering and their roots enough mineral nutrients and water.
A tolerant species of climber may similarly co-exist with the dominant. The different
productivities of the species in such systems are determined more by inherent differences
in potential than by simple competition from the dominant. If the latter is

100
- 10
al
$ 1
>
8
Y rn
b,
0
a
- E
0.1 0.01
Maintenance of species-richness in plant communities 109
0.001 0 10 C 10 20
Species numbers
Fig. I. The three major types of dominance-diversity curves presented by Whittaker (1965):
(a) species-poor communities, (b, c) species-rich.
Fig. 2. A section of a model of a species-poor community with only one species in each major
life-form; the resources are represented by a space of finite volume and the requirements of the
three species by incompressible spheres. The larger spheres are seen to be unable to exclude
the smaller ones. The arrangement of the spheres would be different if their sizes were kept
constant and the space representing the resources were made bigger or smaller. e.g. if it were
made the size of one of the four unit-spaces drawn in the figure.

I I0
P. J. GRUBB
Fig. 3. A section of the central part of a model of a species-poor community with dependencerelationships
as well as the exclusion-relationship; the cylinders and cones cannot fit into each
other’s holes and the larger of the small spheres are also excluded.
removed, and no species is artificially introduced, none of the remaining species may
be able to take over the role of dominant either in terms of standing crop or in
dominating the others in a more general sense. The long-term co-existence of several
species in these simple communities can largely be ‘explained’ in terms of a model in
which they fit in the gaps between each other. Thus, if the available resources are
represented by a cube of finite size and the plants by incompressible spheres, the size
of which is proportional to the resources utilized or blocked off, then the larger
spheres are not able to occupy all the space that encloses them (Fig. 2). Such a model
represents only part of the truth because the plants in such a system do not grow
independently and the spheres ought to be conceived of as capable of denting each
other to some extent, just as the circles can overlap in the model of Putwain & Harper
(1970). Thus the trees in forest systems of this type reduce the yield of the few species
of herb beneath them (Watt & Fraser, 1933 ; Karpov, 1961) while the yield of the trees
may be reduced by the herbs-after all, the grass sward in an orchard can reduce
the fruit crop above it (Bedford & Pickering, 1919).
The model represented in Fig. z is also inadequate in that it fails to include the
dependence-relationship which, together with competition and complementarity,
characterizes the integrated plant community. Dependence is most clearly demonstrated
by the epiphytes already mentioned, by the parasites and hemi-parasites and by

Maintenance of species-richness in plant communities
the epi-parasites (‘saprophytes’) often found growing in very dense shade where few
autototrophic plants can persist. The dependence-relationship can be incorporated, as
in Fig. 3, by conceiving the requirements of the host species as represented by large
spheres with hollows of different shapes and sizes on their outsides and by representing
the dependent species as cylinders or cones that fit these hollows exactly.
I11
(b) Phenological spread
The second major way in which species are complementary to each other is in
their seasonal development. A useful simple example comes from the persistence of
certain weeds in crops. Quite often the crop, during its own active period of growth,
very strongly suppresses a particular species of weed, as in the case of barley and white
persicaria (Aspinall & Milthorpe, 1959; Aspinall, 1960), but the weed is not eliminated
from the field because it combines an ability to persist in a suppressed state with an
ability to develop rapidly to the stage of ripe seed production before harvest, starting
as soon as the crop begins to divert its photosynthate into production of its own seed
rather than into vegetative organs directly active in competition. At this time the crop
may actually leak out nutrients of value to the weed, as potassium escapes from the
grass Phalaris tuberosa (Richardson, Trumble & Shapter, I 932). Opportunism,
coupled with persistence while suppressed, may be especially important for species
at the bottom of the rank order in a particular natural community. Differences in
seasonal development or phenology are one of the main findings of those who have
developed the analytical approach with natural communities. The vernal flora of
north temperate deciduous woodland is most often quoted but equally impressive are
the successive flushes of activity in steppe (Walter, 1968) or semi-desert (Bykov, 1974)
and the non-coincidence of flushing in trees of tropical rain-forest (Medway, 1972;
Frankie, Baker & Opler, 1974).
(c) Fluctuations in the environment
In most, if not all, plant communities the processes by which certain species tend to
oust others as a result of competition in the vegetative stage are greatly hindered by
temporal fluctuations in the environment. The effects of short-term changes in the
environment on species-balance can be very considerable. If a mature plant community
is ‘in equilibrium’, then the equilibrium is highly dynamic. Thus, in certain seminatural
meadows in the U.S.S.R. the grasses Agropyron repens and Bromus inermis are
particularly prominent in dry years while Alopecurus patensis tends to dominate in
wet years (Rabotnov, 1974). In the same general area temporary blockage of drainage,
which can occur naturally, leads to an increase in Ranunculus repens and release of the
blockage returns the balance in favour of Alopecurus patensis (Rabotnov, 1974).
Fluctuation in temperature is probably equally important, especially where species
with a northern distribution and greater resistance to winter-killing are mixed naturally
with those of southern distribution and lesser hardiness, e.g. Elymus canadensis and
Sorghastrum (Andropogon) nutans in some North American prairies (Clements,
Weaver & Hanson, 1929). Fluctuations with a period of 2-3 years grade into those

I12
P. J. GRUBB
lasting a decade, e.g. the long drought of the 1930s in the prairies of the U.S.A. and
the wetter than average 1950s (Coupland, 1974). Since individuals of some grasses and
plants of the woodland door possibly persist for a thousand years or more (Harberd,
1961; Ohenen, 1967a, b), climatic fluctuations on the scale of centuries may be
important in determining an inconstant balance between the vegetative, plants of some
species.
The biotic environment also fluctuates. Chilvers & Brittain (1972) have tried to
explain co-existence of similar plant species in terms of a negative feed-back involving
fluctuations in the numbers of host-specific parasites or herbivores. However, fluctuations
in the severity of pests determined by climatic influences or by predators rather
than by the abundance of the host will also play a role. So also will fluctuations in pests
that are not host-specific but still selective, e.g. leatherjackets (TZpula spp.) eating
roots of clover more than those of grass in a ley (White & French, 1968). Several
observations suggest indirectly that pests may be important in limiting the abundance
of plant species under natural conditions, e.g. the better growth of certain Eucalyptus
spp. outside Australia but in climates very similar to those of their natural range
(Gillett, 1962; Harper, 1969). The effectiveness of specific insects brought in to
control particular weeds introduced by man is also impressive, e.g. in the control of
St John’s Wort (Hypericum perforaturn) by the beetle Chrysolinu quadrigemina in
California (Huffaker & Kennet, 1959). At one typical range-land site the cover of weed
was reduced from cu. 75 yo to zero in four years. Similar effects in more nearly natural
vegetation were found by Cantlon (1969), who studied the annual herb Melumpymm
Zineare in deciduous forest in Michigan. The plant is grazed by the katydid Atlanticus
testaceus and in plots treated with a mixture of insecticides the number of seedlings
was twice as great as in the control plots after I year, three times as great after 2 years
and over three times as great after 4 years. Fluctuations in localized and roving
populations of mammals, which are generally less selective than insects (Summerhayes
1941 ; Watt, 1957; Kydd, 1964; Stewart & Stewart, I ~ I ) must , also have been an
important influence before man dominated the scene.
Temporal fluctuations in microbial pests may also be important for the control of
the abundance of particular plants in the wild but little is known about this. Theeffects
of spatial fluctuation - seen in the fairy rings of grasslands in the North Temperate
Zone - are highly suggestive. These rings have been a great source of mythology but
are still poorly understood in scientific terms (Shantz & Piemeisel, 1917; Ramsbottom
1953). Apparently a fungus spreads outwards slowly from its site of infection, suppressing
the dominant grass to a variable degree (sometimes almost completely).
Often, it seems, considerable quantities of major nutrients are liberated when the
fungus dies and these stimulate the growth of the grass to a particularly high level at
the margin of the infected area, thus forming the ‘ring’.
It has been suggested (Gillett, 1962; Janzen, 1970; Connell, 1971) that host-specific
parasites and herbivores may have a rather special role to play in maintaining speciesrichness
through their activities being concentrated on adult plants and inflicting
especially heavy mortality on any offspring in the immediate neighbourhood of the
parents. This idea will be further discussed on page 125.

Maintenance of species-richness in plant communities 113
0' I
Time
Fig. 4. The two major kinds of result found when two species (x and y) are grown in mixture,
starting with contrasted proportions of x (90 % and 10 %) : (a) x always replaces y, (b) a balance
between x and y is set up. The shape of the time course of the ratio may vary appreciably
depending on the species tested, and there are likely to be fluctuations about the mean line of
the time course depending on the season, as shown (discontinuous line) for one of the mixtures
in (a).
(d) Balanced mixtures
Many experiments on competition have been made in recent years using even-aged
mixtures of pairs of species, and with the two species sown in varying proportions as
suggested by de Wit (1960, 1961). In most cases one species of the pair tends to oust
the other, whatever the proportions at the start of the experiment (Fig. 4 a), but in
a few cases there is evidence for a position of balance, which could persist indefinitely
and toward which mixtures in all proportions tend to change (Fig. 4b). In the first case
there is eventually complete replacement of one species by the other. If the advantage
of A over B is relatively small, as is often the case, replacement will take a very long
time. However, such replacement can occur in quite short periods in annual species
as is shown by the experiment of Harlan & Martini (1938). They sowed I I varieties of
barley in equal proportions at several different sites, harvested grain at random at the
end of each season for sowing the next year, and found that less suitable varieties were
completely eliminated within 4-1 I years at any given site.
The maintenance of a balanced mixture, as in Fig. 4b, is dependent on both the
growing conditions (van der Bergh & de Wit, 1960) and the density of the plants
(Marshall & Jain, 1969). It can be explained in general terms of either a balance of
intraspecific versus interspecific competition (Harper, 1967) or limitation of the two
species by different factors (Harper, Clatworthy, McNaughton & Sagar, 1961). The
exact mechanisms involved in the first explanation are obscure, but may possibly
involve the production of autotoxins, i.e. materials more toxic to the producer species
than to the other species. Newman & Rovira (1975) have recently obtained evidence
that production of materials that are more autoxic than allotoxic may be characteristic
of those species that occur as isolated individuals, whereas the reverse may be true of
species that naturally form long-lasting and continuous swards. Limitation by different
factors can be illustrated tentatively with respect to mineral requirements. For example,
on some soils nitrogen is the primary limiting mineral for grasses, but phosphorus and
potassium limit the growth of legumes (Thurston, 1969); on other soils phosphorus
a BRE 52

1’4 P. J. GRUBB
may be the primary limiting mineral for grasses and nitrogen for sedges (Willis, 1963).
Similarly the root growth of one species may be best in soil pores of a certain size and
that of another species best in adjacent pores of a different size (Sheikh & Rutter, 1969).
It is often forgotten that the growth of most plants is limited by several or many
factors simultaneously. In the cases just cited climatic and biotic factors limit as well
as soil factors. It has to be emphasized that the persistence of mixtures of the species
can only be accounted for in terms of different limiting minerals or pore sizes if these
are of overwhelming importance in the limitation of growth.
The significance under natural conditions of the type of balance shown in Fig. 4b is
not at all clear. The strong dependence on growing conditions and density must be
emphasized. Thus two species of Avena were proven to have the appropriate combining
ability in certain artificial experiments, but, in the field, more than half the populations
within the geographical range of both species in California were found to contain only
one of the species (Marshall & Jain, 1969). No experiments yielding evidence of
stability in even-aged mixtures of three or more species have been reported. However,
some highly relevant experimentson mixtures of four or more species have been made.
In two sets of experiments on mixtures of four species the different species were all
sown in the same proportion (Bornkamm, 1961a, b). The results show that a fairly
clear rank order (‘pecking order’) was established (Table I a). The same result emerged
(Table I b) when five grass and four legume species were grown in all possible pairs
(Caputa, 1948; Jacquard, 1968). Similar results were obtained when I I different
weeds were tested against two different crops (Welbank, 1963); experiments with only
three species tested against each other are clearly much less likely to yield a definite
rank order (Haizel & Harper, 1973). The rank order was certainly not completely
constant in Caputa’s experiment and one species, Dactylis glomerata, behaved very
erratically (Table I b). It seems improbable that in mixtures involving three or more
species many of the encounters between one species and its neighbours will lead to
a self-balancing equilibrium. However, there may be very many occasions when a nearbalance
is struck (the equivalent of a small shift in Fig. 4a) and this may be extremely
important, as becomes clear later (see page I 18).
(e) Variation in competitive ability with physiological age
The relevance of all the experiments mentioned in subsection II(d) is limited by the
fact that most natural and semi-natural plant communities are of uneven age. The
uneven age-structure is, in turn, important because success in competition depends on
which developmental stage of one species is pitted against which stage of the other.
A. S. Watt (1955) first illustrated this idea with an analysis of a semi-natural mixture
of heather (Calluna vulgaris) and the bracken fern (Pteridium aquilinum) on acid,
nutrient-poor sands in eastern England. He divided the life-history of each species
into four successive phases on the basis of morphology alone though these phases
plainly reflected physiological age (pioneer, building, mature, degenerate). He then
observed which species succeeded when one invaded the other, and, in particular, how
this depended on the growth phase of the species invaded. The pioneer phase of one

Maintwnce of species-richness in plant communities 115
Table I. The results of two experiments in which all possible pairs of species within
certain groups of species were grown together and a rank order establkhed
Species
affected
(a) From Bomkamm (1961 a)
Decreasingly strong
competitors
S S A>VaT
A S A TaV
V S ABV T
T S A V T
S = Simpis alba, A = Avena sativa, V = Vicia sativa, T = Triticum aestivum.
Species affected
L
A
D
P
F
M
X
C
H
(b) From Caputa (1948) - results of 1944
Species decreasingly aggressive to test species
M L H X F P C A D
L M A X F P C H D
L M=X A=F D P C H
L D F A X M P H C
L M=A P X F C H D
L X M C H A P D F
L D A X P F M = C H
L M X A D F H P C
L M X A D P F H C
strongly aggressive (in top two places for 719 species) :
L = Lolium italicurn
M = Medicago sativa
Moderately aggressive (in third, fourth or fifth places for 7/9 species):
A = Arrhenatherum elatius
X = Trifolium pratense
Slightly aggressive (in fifth, sixth or seventh places for 719 species):
F = Festucapratensis
P = Phleumpratense
Not aggressive (in seventh, eighth or ninth places for 719 species) :
C = Lotus corniculatus
H = T7Z~ObII hybridurn
Very variable (from second to ninth place) :
D = Dactyl& glomerata
species only succeeded if it invaded the pioneer or degenerate phase of the other. Such
a relationship provides a possible basis for the indefinite persistence of two such
species in mixture.
These various approaches to the analysis of plant communities that do not involve
a consideration of regeneration - or only a minimal study of it - provide several
distinct ways of explaining long-term co-existence of some plant species, but they do
not convincingly ‘explain’ the long-term co-existence of the numerous species with
essentially the same life-form, adult phenology and habitat-range, that are characteristic
of so many species-rich communities.

I 16
P. J. GRUBB
111. INTRODUCTION TO THE INVOLVEMENT OF REGENERATION
The idea of two species with much the same life-form, phenology and habitat-range
differing in requirements for regeneration is most easily grasped for tree species.
Gaps arising in a forest are of different sizes. When a whole large tree is blown over,
the gap produced is large; when an individual limb falls off a diseased tree, the gap
formed is small. If the gap is large, an individual tree of some light-demanding species
is most likely to be the next dominant on the spot. If the gap is small, a tree of some
shade-tolerant species is likely to grow through and dominate the spot. Thus the
light-demanding Betula pendula can persist with shade-tolerant Fagus sylvatica in
semi-natural woodland on acid soils in Britain (Watt, 1934; 1947). One can easily
envisage other factors that might swing the balance between colonizing species in the
gap or in different parts of it. Such factors include the particular species which happen
to be present at the right time as seed, seedlings, saplings or poles; the presence of the
crown of the fallen tree (and its smothering effect) or just the tall bole; presence or
absence of leaves on the fallen tree (and the green-manuring effect); the degree of
disturbance to the litter and topsoil: the presence or absence of sunflecks in sunny
weather depending on the side of the gap concerned (north or south) in a forest far
away from the equator (Coombe, 1966); the adult trees left standing and the ground
flora - both compete for light, water and mineral nutrients, and may exert allelopathic
effects or harbour particular pests and diseases.
Table 2. Processes involved in the successful invasion of a gap by a given
plant species and characters of the gap that may be important
Processes
Production of viable seed
Flowering
Pollination
Setting of seed
Dispersal of seed
Through space
Through time
Germination
Establishment
Onward growth
Characters
Time of formation
Size and shape
Orientation
Nature of soil surface
Litter present
Other plants present
Animals present
Fungi, bacteria and viruses present
The possibilities seem almost limitless. The processes involved in the successful
invasion of a gap by a given plant species and characters of the gap that may be important
are summarized in Table 2. Similar considerations apply when invasion of a gap
is by vegetative means rather than by seed.
It becomes apparent that species-richness may be maintained by a heterogeneous
environment acting on all of aseries of stages in the reproduction of the plants present.
The variable environment determines whether there is or is not at a particular place
and time for a particular species an abundance of flower-formation, pollination, good
seed-set, dispersal, germination, establishment of the juvenile plant and passage of the
juvenile to the adult. The idea that all these stages are important in the maintenance of
species-richness has been all too often ignored. It was not a matter of chance that the

Maintenance of species-richness in plant communities 117
example given above to illustrate the reality of differences in requirements for regeneration
concerned trees. The examples that we now find easiest to comprehend and most
convincing were also historically the first to be appreciated, It was the foresters who
first realized the importance of differences in regeneration-requirements. Heyer (1852)
seems to have been the first to publish an explicit account of differences in ‘tolerance’
of tree seedlings; as Tourney & Korstian (1937) pointed out, the original emphasis
was on degrees of tolerance of shade, but in the present century differences in the
ability to tolerate root competition have been increasingly emphasized. In the 1950s
the importance of differences between species at all the stages in the regeneration
cycle came to be appreciated particularly in relation to tropical rain-forest and tropical
deciduous forest (Jones, 1955-6; Hewetson, 1956; Steenis, 1956). More recently the
question has been discussed and illustrated for tropical rain-forest by Budowski (1965),
Poore (1967,1968), Ashton (1969), Richards (1969), Rollet (1969), Janzen (1970) and
Whitmore (1974, 1975) and for a subtropical rain-forest by Webb,Tracey & Williams
(1972). A particular idea that attracted much attention at the time was that of Aubreville
(1938), who suggested that any one tree species never regenerated under itself;
later workers, however, have shown that this generalization was not true (Jones, 1955-6;
Foggie, 1960; Schulz, 1960; Rollet, 1969). Most recently emphasis among writers
concerned with species-richness in tropical forests has been concentrated on differences
in flowering phenology (Gentry, 1974, 1976; Stiles, 1975). There seems to have been
much less explicit discussion of maintenance of species-richness in temperate forests,
although more interest has been shown in the last two years - see, for example, the
papers of Forcier (1975), Horn (1975), Pigott (1975) and Ash & Barkham (1976).
Many earlier studies of regeneration showed implicitly that the same principles
apply as in tropical forests, e.g. those of Watt (1934, 1947), Graham (1941), Jones
(1945), Bray (1956), Curtis (1959), Franklyn & Dyrness (1969), Auclair & Cottam
(1971), Williamson (1975), Sprugel (1976) and of various Continental authors as
summarized by Ellenberg (1963). Whittaker (1969) mentioned the ‘successional
niche’ and appeared to refer to the parts played by different species in the natural
regeneration of eastern deciduous forest in the U.S.A. after sheet destruction by fire;
in a later paper (Whittaker, 1972, pp. 239-40) he seemed to broaden his concept of the
successional niche but he considered it only briefly. Loucks (1970), in a general treatment
of diversity, also started from a forestry background; he emphasized the importance
of species reacting differently to periodic perturbations, notably fires and cyclones.
In treatments generally detached from the discussion of particular communities
Skellam (1951) has shown the importance of differences in dispersability, and Harper
and colleagues have repeatedly emphasized the potential importance of different
requirements for germination and establishment, and the nature of ‘safe sites’ for
particular species (Harper, 1961, 1965 ; Harper et al. 1961 ; Harper, Williams & Sagar,
1965; Cavers & Harper, 1967; Sheldon, 1974).
Most recent discussions on diversity in grasslands have been notable for a failure to
appreciate the relevance of regeneration processes - see, for example, the articles of
McNaughton (1967, 1968b), Grime (1937a, b) and Newman (1973). They have
concentrated on the negative correlation often found between species-richness and

I I8
P. J. GRUBB
grassland productivity, i.e. the yield of new plant matter per unit area and time. This
situation illustrates a point of great importance for the present discussion. Differences
in requirements for regeneration can only be effective in maintaining species-richness
if the adult plants of the many species are reasonably evenly balanced in competition.
In some kinds of vegetation this is less likely to be the case if the growing conditions are
generally very favourable to plant growth; under such conditions a few potentially
vigorous and tall-growing species generally eliminate many species which could
persist in the absence of competition. The grassland vegetation of N.W. Europe is
a useful example; here there is a strikiig contrast between the species-richness of the
grasslands on shallow calcareous soils (short of nitrogen, phosphorus and other
mineral nutrients) and the species-paucity of much grassland on deeper soils at pH 5-6
(with a better supply of N and P). The potential for continued co-existence by differentiation
in requirements for regeneration is very great in the calcareous grassland but
much reduced in the grassland at pH 5-6. When species-rich, nutrient-poor grasslands
are fertilized, the standing crop is increased and the species-richness sooner or later
declines. This has been shown for calcareous fixed dunes by Willis (1963), for wet
heaths by Sougnez (1966), and for montane calcareous pasture by Jeffrey & Pigott
(1973). Whether there is a similar effect to be found generally in forests seems doubtful.
Thus Watt (1934) recorded only 47 species in the herb-layer in 23 samples of escarpment
beechwoods on calcareous soils in the Chiltern Hills compared with 64 species in
10 samples of plateau woods on clay-derived soils of pH 4-7-6.0 in the same area; ash,
beech and oak all grow taller on the clay-soils than on the chalk soils (e.g. 25-32 m versus
20-23 m tall for beech) and the fertility for most plants is greater on the clay-soils. The
data from Watt’s two samples are not strictly comparable because the list for the escarpment
beechwoods is incomplete. However, this fact is counter-balanced by the inclusion
in the lists of many species not typical of mature woods and suggesting a more recent
origin for at least parts of the woodlands on the scarp. Watt’s data cannot be taken to
prove that the field-layer is more species-rich on the more fertile soil, but they illustrate
a general finding in central and northern Europe that beechwoods on deeper
soils of pH 5-6 (Asperulo-Fagion) are generally more species-rich than those on
shallow calcareous soils (Cephalanthero-Fagion), as documented by Ellenberg (I 963).
The contrast with grasslands in the same region in the trend in species-richness
reflects the much smaller number of strictly calcicolous species found in woodlands,
i.e. species strictly confined to calcareous soils (Fenner, 1975). The fact that many
species able to grow on soils of pH < 5 can also grow at pH 5-6, but not on calcareous
soils, is also important.
Despite the considerable history of discussion of regeneration processes, it is not
only the students of grassland diversity who have ignored them. Several distinguished
authors, who have written recently about co-existence of plant species in general, have
failed even to mention the possibilities of differentiation in requirements for successful
regeneration, e.g. Goodall (I970), Walter (1971) and Whittaker (1975).

Maintenance of species-richness in plant communities 119
IV. DEFINITION OF A PLANT’S NICHE
The niche of a plant is taken here to be the definition of its total relationship with
its environment, both physico-chemical and biotic; such a definition necessarily
includes a statement of the role played by the plant as well as a statement of its tolerance.
The present author sees no advantage in replacing the term ‘niche’, used in this sense
by ‘ecotope’, as suggested elsewhere (Whittaker, Levin & Root, 1973). My usage of
‘niche’ is essentially in agreement with that of Richards (1969) and Wuenscher
(1969, 1974). Four component niches have to be recognized in a complete definition
of a plant’s niche.
(i) The habitat niche, i.e. the physical and chemical limits tolerated by the mature
plant in nature. The definition should include an expression of the kinds of fluctuations
from the mean climatic conditions which favour the plant’s vegetative development.
(ii) The life-form niche, including an expression of size and annual productivity as
well as three-dimensional pattern.
(iii) The phenological niche, i.e. the pattern of seasonal development.
(iv) The regeneration niche, i.e. an expression of the requirements for a high chance
of success in the replacement of one mature individual by a new mature individual of
the next generation, concerning all the processes and characters indicated in Table 2.
The habitat niche is the plant’s address. The life-form and phenological niches are
the plant’s profession. The regeneration niche includes elements of both address and
profession.
Hutchinson’s (1957) idea of recognizing a ‘potential niche’ (that effective in the
absence of competitors and predators) and a ‘realized niche’ (that effective in the
presence of competitors and predators) can be applied to all four aspects of the niche
but is particularly important for the habitat niche.
Before considering examples of differentiation in the regeneration niche, it is
necessary to recapitulate briefly what is known of the process of regeneration in the
different major types of plant community.
V. PATTERNS OF REGENERATION IN DIFFERENT PLANT COMMUNITIES
Four major types of vegetation may be recognized in this context, determined by the
dominant life-forms present: forests and woodlands, shrub-dominated communities,
grasslands and associations of ephemeral herbs.
In most natural forests regeneration involves clearings of some kind, but the size of
the clearings varies enormously. The two extremes are represented by forests suffering
occasional sheet-destruction by fire and those with gaps created by the fall of single
trees or branches. Intermediate types include those in which gaps of 0.1-1-0 ha are
caused by cyclone damage (Webb, 1958; Whitmore, 1974) and those with strips of
dead and dying trees somehow related to strong and constant winds (Oshima, Kimura,
Iwaki & Kuroiwa, 1958; Iwaki & Totsuka, 1959; Sprugel, 1976). In many areas
occasional regeneration in sheets after fire alternates with a patchwork regeneration

I20
P. J. GRUBB
pattern during fire-free periods, e.g. in the Nothofqus forests of Tasmania where
Eucalyptus regnans colonizes after fire (Gilbert, 1959; Jackson, 1968), or in the Piceu-
Tmgu forests of western North America where Pseudotsuga mxiesii invades after
fire (Franklyn & Dyrness, 1969). In most forests some trees die ‘on their feet’ and new
trees grow up in their place without the formation of an obvious gap in the canopy;
this pattern is probably very widespread in low-stature forests (e.g. many subalpine
and upper montane tropical forests), in which the individual trees rarely develop large
trunks and appear to collapse after death without making gaps (Grubb & Stevens, 1976;
Tanner, 1977). Regeneration of trees in all these forest-types is primarily by seed, but
regeneration from burnt stumps may be important in mediterranean climates;
a valuable summary of the relevant findings in California is given by Mooney & DUM
(1970) and some basic information for the European Mediterranean zone by Trabaud
(1970). For shrubs and herbs, vegetative spread into clearings is relatively more
important (Kujala, 1926; Whitford, 1949; Flower-Ellis, 1971 ; Korchagin & Karpov,
1974), but there are certainly many forest herbs for which regeneration is mainly by
seed (Curtis, 1959; Wilson, 1959; Knight, 1964). Regeneration of climbers, epiphytes
and parasites appears to occur most often by seed in a patchwork pattern, broadly
analogous to that for most trees, though invasion of new gaps by vegetative spread is
no doubt important for some climbers and scramblers, e.g. many bamboos.
In shrub-dominated communities regeneration is sometimes chiefly by seed as in
the species-poor Callunetum of eastern England (Watt, 1947, 1955) and in semideserts
(Bykov, 1974; Davies, 1976), but in many wetter communities with creeping
Ericaceae or Epacridaceae (e.g. many subalpine heaths of both hemispheres) invasion
of gaps by vegetative spread is more common (Burges, 1951; Chambers, 1959;
Barrow, Costin & Lake, 1968; Keatinge, 1975).
In closed grassland, i.e. grassland with a continuous cover, the extent of regeneration
by seed is not clear. Vegetative regeneration in a kaleidoscopic pattern is certainly
important in a variety of grasslands, e.g. in meadows in Sweden (Tamm, 1956,1972u,
b) and Russia (Rabotnov 1969b), in hill pasture in Scotland and Wales (Harberd, 1961 ;
Chadwick, 1961), and in lowland grassland on chalk in England (Austin, 1968). The
rates of vegetative spread vary greatly but have been estimated at 2-6 cm per year for
certain dominant grasses (Harberd, 1961 ; Chadwick, 1961 ; Austin, 1968). However,
the half-lives of adult plants of the perennial species commonly vary from 1-2 years up
to more than 50 years (Harper, 1967; Tamm, 1972u, b; Sarukhhn & Harper, 1973),
and for some species may be of the order of several hundred years (Harberd, 1961 ;
Oinenen, 1967u, b). The short-lived perennials as well as the annuals and biennials,
found in continuous turf with gaps only 1-5 cm across must regenerate by seed
(Sarukhhn & Harper, 1973 ; Grubb, 1976), but for many grassland species creation of
larger gaps by animals (e.g. soil-heaps of moles or gophers, or scratchings by rabbits
or badgers) may be necessary for regeneration by seed (Watt, 1971, 1974; Miles, 1973 ;
Platt, 1975). The pattern of regeneration is particularly obscure in closed grassland
dominated by large tussocks such as those of Moliniu in western Europe (Godwin,
1941 ; Rutter, 1955), Dunthonia and Poa in New Zealand (Cockayne, 1928) or Deyeuxiu
(Culumugrostis) in the high Andes (Cuatrecasas, 1934; Diels, 1937).

Maintenance of species-richness in plant communities
In open grassland, developed in situations deficient in mineral nutrients and/or
water and consisting of isolated plants, the latter may have quite short half-lives of
5 7 years (SarukhQn & Harper, 1973) and probably regenerate chiefly by seed.
However, the huge tussocks of Triodia and Plectrachne (‘spinifex’) in the semi-deserts
of central Australia (Winkworth, 1967; Beard, 1969) appear to be much longer-lived.
Natural associations of ephemeral herbs (plants represented only by bulbs, corms or
seeds in the unfavourable season) usually exist as sub-systems of more extensive
communities, e.g. in semi-deserts, on cliffs or in successional stages on dunes. Little
is known about the regeneration of plants with bulbs and corms, but the others, by
definition, regenerate only by seed.
In summary, it is apparent that very various patterns are involved in regeneration
and that much remains to be discovered about the process. However, it is clear that
regeneration involves both seed and vegetative organs and that the relative importance
of these two depends on the community concerned.
It is necessary to comment here on the relation between regeneration and succession,
two distinct processes which have often been confused, especially in the U.S.A., where
much attention has been paid to the successions of species found after fire. Succession,
as a term, is best reserved for non-cyclic series of vegetation types, either in primary
seres (e.g. on moraines left by glaciers, in lakes or on sand dunes) or in secondary seres
(e.g. on abandoned farm land). Confusion is bound to arise where man-made secondary
successions merge with natural regeneration processes, as in the post-fire situation in
much of the U.S.A. but it is still worth while to distinguish the processes in general.
For most species the ‘successional niche’ is best treated as part of the definition of the
habitat niche, but in the case of species in certain secondary seres (notably post-fire
sere) it may be more useful to include it in the definition of the regeneration niche.
Regeneration in a gap of any kind usually involves a succession of species - the
serule of Daubenmire (1968~). An obvious kind of differentiation in the regeneration
niche concerns time of appearance in this serule (G6mez-Pompa, 1971). However,
since several or many species are usually present at each stage, niche differentiation
must concern gap quality as well.
I21
VI. EXAMPLES OF DIFFERENTIATION IN THE REGENERATION NICHE
(a) Production of viable seed
It is a commonplace that in a particular region certain years are ‘good years’ for
some crops andnot for others and variation of this type for species cultivated in fields and
orchards has been documented the world over. There is plenty of information too for
forest trees in many parts of the world: Central Europe (Schwappach, 1895; Seeger,
1913), North America (Morris, 1951; Boe, 1954; Fowells & Schubert, 1956;
Daubenmire, 1960; Baron, 1969; Clark, 1970), the U.S.S.R. (MolEanoq, 1967)~
Japan (Tagawa, 1969,1971) and New Zealand (Beveridge, 1964,1973; Wardle, 1970).
However, there is only a little information of this type for shrubs, e.g. that of Davies
(1976) on Australian semi-desert species, or for perennial grassland herbs, e.g. that
of Rabotnov (1950) and Golubeva (1968) for selected plants in meadows and pastures

I22
P. J. GRUBB
74 76 78 ao a2 a4 a6 aa 90 92
Years
Fig. 5. Numbers of seed produced by three tree species in Prussia in the years 1874-93 (after
Schwappach, 1895) : (a) Pinur sylvestris, (b) Quercus robur (open columns) and Fagus sylvatica
(filled columns).
r (a) 3442
1000 -
1
n
TI x
L al
n
el
0,
V c
3
v) 0
800
600
400
200
-
-
-
-
-
-
-
-
-
-
O U
Fig. 6. Numbers of sound seed per unit area produced in the years 1961-7 by marked trees of
five species of Podocarpaceae in New Zealand: (a) Dacrydium cupressinunz, (b) Podocarpus
ferrugineus, (c) P. spicatus, (d) P. totara and (e) P. dacrydioides (after Beveridge, 1973).

Maintenance of species-richness in plant communities 123
1960 1961 1964 1965 1966 1967 1960 1969 1970 1971
Scaevo/a spinescens 0. ..OOO..
Acacia aneura 0 ~ O . ~ . , .
Acacia pruinocarpa
0
O....0.
Acacia tetragonophylla 0 0 . 0 . O 0.
Cassia desolata 0 0 . 0 0.0 0.
Cassia helrnsii 0 . 0 0 . ~ ~ .
Erernophila fraseri ..........
Acacia victoriae O ~ O O ~ O O
Hakea lorea 0 O o....o
Santalum spicatum o OOO..OO
0 0
0 1-25 26-50
51-75 76-100
Fig. 7. The crops of fruit produced by ten species of trees and shrubs over 10 years in an arid
region of Western Australia (from Davies, 1976). The results are expressed as percentages of the
best year’s production. Blanks indicate that nu recoras were kept in those years. Reproduced
from the Journal of Ecology with permission.
in the U.S.S.R. and of Sarukhh & Harper (1973) for plants in a Welsh pasture.
There are also very few data for annuals, e.g. those of Newman (1964) for certain
winter annuals in eastern England.
In each of the forest communities that have been studied, three main patterns of
seed production have emerged: (a) moderate production in most years, (b) fruiting
rather irregular, and (c) abundant fruiting strongly periodic (see Figs. 5 and 6). The
same patterns have been found in a sample of species of semi-desert scrub (Fig. 7).
Different species in group (b) are favoured by different years. It is important to
realize that the variability in the supply of viable seed to different gaps will be greater
than that suggested by the mean differences between species, not only because of
differences in dispersal, etc., but also because of differences between individuals of
each species - at least those in groups (a) and (b). In any one year some individuals
fruit abundantly and others less SO.
It is virtually certain that the three main patterns of seed production reflect three
corresponding patterns of flowering, although there is little published evidence to
prove the point. The three patterns have been shown clearly in herbs in Europe
(Fig. 8) and trees in Malaya (Medway, 1972). However, no exact correspondence
between the numbers of flowers and of viable seeds can be expected because of wide
variations in the success of pollination and the ‘setting’ or ripening of the seed.

c
46 47 4% 49 50 51 52 53 54 55 56 57 50 59 60 61 62 63
124 P. J. GRUBB
Years
Fig. 8. (a) The flowering in 1946-56 of mapped individuals of Annnone hepatica (-) and
Sanicula europaea (---) that flowered in 1946 in certain quadrats in Sweden and were still
alive in 1956 (data from Tamm, 1956). (b) Total numbers of plants flowering in a small colony
of Senecio integrifolius in England (data from Morgan, 1965).
Unfortunately little is known about year-to-year variation in either of these processes.
Circumstantial evidence exists for massive failure of pollination in some species in
some years in communities as widely separated as the lowland tropics (Medway, 1972)
and the Arctic (Kevan, 1972) and it seems virtually certain that less-dramatic fluctuations
in the success of pollination also occur, e.g. in relation to the incidence of high
winds or rain. As for the ripening of fruit the optimum conditions are known for only
a very few wild species. Examples are the Douglas fir, Pseudotsuga menziesii (Lowry,
1966), the perennial thistle, Cirsium acaulon (Pigott, 1968), and the winter annual
Teesdalia nudicaulis (Newman, 1964, 1965). For crop plants it is known that both
optimum conditions and susceptibility to damaging conditions vary with the stage of
development. For example, the yield of maize seeds was shown to suffer a 50%
reduction as a result of a standardized drought treatment lasting 6-8 days at the stage
when the primordia were growing most actively, but negligible reduction if the same
stress was applied a little later in development (Robbins & Domingo, 1953). Similar
results were obtained for barley by Aspinall, Nicholls & May (1964). Very high daytime
temperatures (32-35 "C) cause flowers of the bean to abort if they occur on the
day of opening or one day before or after that, but they cause much less damage if they
occur at a later stage in development (Smith & Pryor, 1962). High night temperatures
are especially damaging to seeds of peas about 5 days after flowering (Lambert &
Linck, 1958; Karr, Linck & Swanson, 1959) and similar results have been obtained
for cherries (Tukey, 1952), apples (Tukey, 1955) and grapes (Tukey, 1958). The
incidence of short periods of drought and high temperatures in relation to the flowering
periods of wild plants certainly varies from year to year and such periods must
account for some of the year-to-year variation in seed-set. Much more investigation
of this topic is needed. The losses due to seed-eating insects and birds, and to fungal
and bacterial pathogens, also need to be quantified, for very little information is at
present available (Rabotnov, 1969a; Janzen, 1971 ; Bohart & Koeber, 1972).
Great interest attaches to the physiological processes involved in the production

Maintenance of species-richness in plant communities 125
of viable seed and to the evolution of the variety of flowering and fruiting 'strategies'
(not least the variation in phenology), but attention is concentrated here on the fact
that in any one species-rich community the proportions of viable seeds of different
species falling on any one area are certain to vary appreciably from year to year.
(b) Dispersal
First, we are concerned with dispersal in space. In every species-rich community
that has been studied a great variety of dispersal mechanisms has been found (van der
Pijl, 1971). There can be little doubt that seeds of some species are, in general,
dispersed further afield than those of others and it has long been appreciated that wide
dispersal is important in species less fit in a competitive struggle between vegetative
plants (Skellam, 1951). In addition the relative effectiveness of different types of
dispersal in space will vary from year to year in response to variations in wind speed,
wind direction, abundance of particular animal vectors, incidence of flooding, etc.
The size of an individual gap in the community can also be important, e.g. in a large
forest-clearing few seeds of a heavy-fruited tree like Fagus reach the centre of the gap,
but large numbers of light seeds such as those of Bet& may land there; so Bet& is
helped to persist in a forest dominated by Fagus (Watt, 1934).
Secondly, we are concerned with dispersal in time. It is well established that the seeds
of the various species in particular communities vary in the length of time for which
they remain viable and that this variability is reflected in the seed bank of the soil.
Information on which species in particular communities are most abundant in the seed
bank is available for temperate grasslands (Chippindale & Milton, 1934; Champness
& Morris, 1948; Major & Pyott, 1966), and for temperate and tropical forests (Guyot,
1960; Guevara & G6mez-Pompa, 1972; Marks, 1974). It is probably extremely
important for many subsidiary species that they can regenerate from seed that has been
in the soil for decades, whenever and wherever a gap arises in the community.
Examples are species of Agrostis, H o h and Poa in grasslands in western Europe able
to benefit from gaps made by animals, and species of Hypen'cum, Juncus and Verbascum
in forests in the same area able to benefit from gaps made by tree-falls.
It is certain that seeds of different species vary inherently in longevity but differences
in survival under natural conditions may be more closely related to palatability,
digestibility and the incidence of predators (animals and microbes) than to inherent
differences in longevity. Seeds certainly differ in palatability (Janzen, 1969) and the
fact that the loss to predators is tremendous has been documented not only for forest
trees with relatively large seeds (Watt, 1919, 1923; Curtis, 1959; Janzen, 1970;
Medway, 1972) but also for herbs with quite small seeds (Tevis, 1958; Bohart &
Koeber, 1972; Sarukhhn, 1974). However, there are still very few data available on the
absolute losses to microbes as opposed to animals (Sarukhhn, 1974).
Variability in predation in time and space is bound to contribute to the variation in
the numbers of viable seeds present at the time of formation of a particular gap.
Janzen (1970) has placed great stress on losses to animals at this stage as critical to the
maintenance of diversity in tropical rain-forests, arguing that more or less host-specific
predators, accumulating on the parent tree, can destroy most seeds falling under it,

I 26
P. J. GRUBB
so that any one tree will rarely be replaced on that site by another of the same species.
However, the observations of Connell (1971) suggest that the effects of animals with
respect to the maintenance of species-richness are generally more important at a later
(seedling) stage.
(c) Germination
There is a vast literature on this topic. The chief point to be made here is that very
many of the differences between species are effective in ensuring that their seeds
germinate in sites that differ in time and space. Some seeds germinate in shade but
others only in the light (Koller, 1972; King, 1975). Most seeds germinate most rapidly
in protected micro-sites, e.g. in small gaps, but some benefit from the alternating cycles
of drying and rewetting suffered in more exposed sites, e.g. large gaps (Miles, 1974).
Many seeds are destroyed by the high temperatures suffered in the litter and topsoil
during a fire, but others are stimulated to germinate by such an event (Beadle, 1940;
Gratkowski, I 961). Seed-form varies appreciably within most communities and it
has been shown that the shape and size (Harper, Love11 & Moore, 1970) as well as the
behaviour of hygroscopic pappus hairs (Sheldon, 1974) or awns (Kerner von Marilaun,
1902), are important in determining the degree of burial of a seed on a particular type
of soil surface and the chance of its being able to take up enough water for enough time
to germinate. Differences in soil chemistry also affect germination, for example the
levels of nitrate (Williams & Harper, 1965; Williams, 1969), calcium (Parham, 1970),
and ethylene (Olatoye & Hall, 1973). A special case is that of allelopathic inhibition,
as seen in certain scrub communities (Deleuil, 1951; McPherson & Muller, 1969);
particularly interesting for the maintenance of diversity is the inhibition of germination
by the parents of the same species (Webb, Tracey & Haydock, 1967; McNaughton,
1968a; Friedman & Orshan, 1975). There can be little doubt that in most communities
gaps of differing quality arise and that the proportions of the different species able to
germinate differ from gap to gap.
Gaps differ not only in their quality at any one time but also in their timing. That
this is important for maintenance of species mixtures can be shown by two examples.
First, it is known that gaps on river-banks in eastern England caused by scour in
autumn usually become occupied by Epilobium hirsutum and those formed in spring
by Lythrum sulkaria (Whitehead, 1971). The Epilobium excludes the Lythrum from
autumn gaps by its earlier development. The Epilobium is unable to become established
as late as the spring so that Lythrum succeeds at that time. The physiological
basis of the distinction is fairly well understood (Shamsi & Whitehead, 1974).
Secondly, it is known that Avena ludoviciana, which germinates in the winter,
is a serious weed of winter cereals but it is almost totally destroyed by ploughing in
early spring. A. fatua, which germinates in the spring, is a severe pest of spring-sown
cereals (Thurston, 1951). In more general terms the periods of germination of
different species in a particular community are spread throughout the year in such
a way that species A has the maximum chance of success in a gap if it is formed by
such-and-such a date and no catastrophe follows, but species B has the best chance if
there is a catastrophe and it germinates afterward. Thus an autumn-germinating herb

Maintenance of species-richness in plant communities 127
in temperate grassland may succeed in regenerating an adult in a certain gap if there
is no heavy frost-heaving (and subsequent drought risk) and plenty of rain in winter,
but if there is plenty of frost-heaving and/or no rain, then a spring germinating
species is at an advantage. An example was observed by Salisbury (1929, p. 222);
all the seedlings of the autumn-germinating Ranumulus parviJeonCs were destroyed
during severe and prolonged winter frosts whereas seedlings of ‘ Helianthemum brewmi’
(Tuberaria guttata (L.) Fourr.) germinating in spring escaped the hazard. In fact the
year can be partitioned by the germination periods of different species into shorter
spells than autumn or spring, as shown for weed species in Central Europe in Fig. 9.
Some species spread the risk, germinating in autumn and spring or discontinuously
throughout the year. Certain species with this ‘strategy’ show an obvious seed
dimorphism related to the maintenance of at least two germination periods (Harper
et al. 1970).
Much is known about the physiological control of the timing of germination in the
kind of succession shown in Fig. 9, based on temperature-responses (Went, 1949;
Lauer, 1953 ; Newman, 1963 ; Mott, 1972), breakdown of hard coats (Salisbury, 1929),
leaching of inhibitors (Went, 1957; Koller, 1969), differences in the degree of
hydration necessary for germination (McWilliam, Clements & Dowling, 1970;
Mott, 1974) and the changes that occur during after-ripening (Newman, 1963;
Villiers, 1972) or as a result of burial (Wesson & Wareing, 1969). It is particularly
significant that appreciable differences in the temperature-responses of germination
have been found in groups of species with very similar habitat-tolerances and reproductive
‘strategies’, e.g. among the winter annuals found on cliffs and sand-dunes in
Europe and North America (Ratcliffe, 1961; Newman, 1963; Baskin & Baskin,
19714 b).
A further potentially important variable is the speed of germination under a given
set of conditions. Species in chalk grassland in England, for example, vary greatly in
this respect (J. B. Dickie, unpublished). Rapid germhators gain a competitive advantage
if subsequent conditions remain favourable, but slow germinators, which may fail
to germinate in short favourable periods, could benefit in the long run, provided they
remain viable while the rapid germinators are killed in a subsequent catastrophe.
Whereas there is now available an impressive body of knowledge concerning seed
behaviour in the laboratory, there is extremely little information available on germination
as such in the field - nearly all the apparently relevant reports concern the establishment
of seedlings and the optimum conditions for this stage of the life-cycle can be
quite different from those for germination. Thus in temperate grasslands with distinct
tussocks many seeds that come to rest beneath or within the tussocks germinate freely
in the autumn and spring but their chances of establishment in the dense shade are
negligible. Similarly those that germinate in more open microsites on deep litter are
generally killed by desiccation before their roots reach the mineral soil below.
Differences in requirements for germination and establishment have also been reported
for plants in simple experimental systems (Harper et al. 1965 ; Sheldon, 1974).

I 28
P. J. GRUBB
Bromus secalinus
Arenaria serpyllifolia
Delphinium consolida
100 r
Sonchus oleraceus
100
F 50.
100 r
u
t 50 o =
1 00
L
Galium aparine
Capsella bursa-pastoris
Myosotis arvensis
5oE 0
100
5oE 0
100
L
Odontites rubra
Sagina procumbens
5oE 0
'N'D' J ' F'M'A'M' J '
Solanum nigrurn
Fig. 9. Emergence of seedlings of various weeds from November to June in central Europe
(data of Salzmann, quoted by Ellenberg (1963), p. 797).
(d) Establishment of seedlings
Most of the information on the establishment of seedlings concerns the surfacetypes
favoured by certain species, but some of it concerns variation from year to year
at particular sites. Many species are known to have specific requirements for establishment,
e.g. Picea sitchensis is found mainly on fallen trunks whereas the accompanying
Thuja plicata and Tsuga heterophylla in the cool temperate rain-forest of the Olympic

Maintenance of species-richness in plant communities 129
1000 r n
I \
I
800 t
I
T
I
L
I
I
! 600 I
n
I
I
f
I
v
I
0 400
I
C
I
.-
-0
a8
v)
200
0
Fig. 10. The numbers of emerged seedlings of Artemisia terrae-albae (-) and Alyssum
desertorurn (---) in quadrats in the Turanian Desert in 1965-9 (data from Bykov, 1974).
Peninsula in the U.S.A. commonly become established on the ground (Franklyn &
Dyrness, I 969). Seedlings of the dicotyledonous tree Weinmannia racemosa most often
become established on the trunks of tree-ferns in the warm temperate rain-forest of
New Zealand (Beveridge, 1973), but this is not true of the other species of tree present.
Published records show that some years favour establishment of certain seedlings
and other years other species (Daubenmire, 1968a; Bykov, 1974). Thus, in one part
of the Turanian semi-desert, 1952 was good for Artemisia paucyora, Kochia prostrata
and Agropyron pectinifone, 1956 for Tanacetum achillaefolium, Festuca sulcata and
Medicago romanica, 1958 for Astragalus virgatus and Trinia hispida (Bykov, 1974).
Quantitative records for Artemisia terrae-albae and Alyssum desertmum in another area
for the years 1965-69 are shown in Fig. 10. Large differences between years have been
found for heathland in Scotland (Miles, 1974) and for forests and meadows in Finland
(Pertulla, 1941).
The passage of the young seedling to the sapling or immature vegetative phase is
only arbitrarily separated from the early seedling phase but most of the information
concerning the effects of the physical environment concern the later stage. Experiments
have shown that the effeets of irradiance (NichoIson, 1960; Grime, 1966; Hutchinson,
1967) and water supply (Jarvis, 1963; Fenner, 1975) certainly differentiate species of
the same community at this stage of the life-cycle. The ability to tolerate shade is often
correlated with large seed-size, at any rate in species that do not depend on mycorrhiza
for their organic nutrition as seedlings (Salisbury, 1941, 1974). However, there
are many exceptions to the rule and the largest-seeded trees in European deciduous
forests (Castanea, Quercm) are all light-demanding (Ellenberg, I 963). Possibly their
large seeds evolved in relation to the occupation of dry sites and the advantage of
9 BRE 52

P. J. GRUBB
rapidly developing a deep tap root; this seems to be the case in some other plants of
open habitats, e.g. the strand-line species Cakile maritima. There is little doubt that
differentiation in the regeneration niche has occurred through the function of seed
size and its effects during establishment.
Not only physical environmental factors differentiate species at the establishment
stage, but also biotic factors, notably grazing, even when the animals concerned are
not monophagous e.g. snails (Grime, MacPherson-Stewart & Dearman, 1968) or deer
(Knapp, 1974). Probably the selective effects of microbial pests and of allelopathic
relations with plants of the same or other species are important in the field but there
is very little proof (Webb et al., 1967). Particular interest arises from the idea that the
risks of pests and allelopathic effects may be significantly greater near the parent
plant so that invading species are at an advantage. Connell (1971) has provided
evidence that seedlings of certain rain-forest trees in eastern Australia may suffer a
greater mortality risk (at a given density) if under a tree of the parent species as
opposed to another species and it is highly desirable that tests should be made on the
applicability of this idea to other communities.
(e) Further development of the immature plant
Least of all, perhaps, is known about the conditions favouring the development of an
estabIished seedling or sapling of a given species into a mature adult. Although the
process is only arbitrarily separable from the establishment of the seedling or sapling,
it is well known that the optimum conditions for several forest trees are different in the
two stages. Thus the Kauri, Agathis australis, needs a light cover (e.g. of Leptospermum)
for survival as a seedling but requires a lack of overhead cover for development in the
sapling and pole stages (Beveridge, 1973). Similar differences are recorded for certain
species in the deciduous and coniferous forests of the U.S.A. (Curtis, 1959; Franklyn
& Dyrness, 1969) and in the rain-forests of the Solomon Islands (Whitmore, 1974).
Such considerations also apply to grasslands and heaths. It has been found that small
clearings (5 x 5 cm) in heathland are most favourable to the early establishment of
of most seedlings, but that after two years larger clearings (50 x 50 cm, less overgrown
than the smaller) have many more surviving plants per unit area (Miles, 1974).
In many studies on successions it has been found that certain species effectively
make possible the invasion of species of a later stage, e.g. Jun$erus spp. acting as
nurses for Taxus (Watt, 1926) or Fugus (Watt, 1934) during invasion of ungrazed
grassland in Britain or for Quercus spp. on sand dunes in the Lake States (Yarranton &
Morrison, 1974). This sort of relationship is also found in the regeneration serule
(Daubenmire, 1968 a). The presence of certain gap-invaders cantip the balance between
two species that might succeed on the site. One commercially important illustration
of this point is the suppression of young Picea sitchensis, but not Larix leptolepis, by
Calhnu vulgaris (Weatherell, 1957). If the Picea and Larix are planted in mixture, the
Larix may suppress the Calluna and, in due course, the Picea the Larix. Such relationships
are often dependent on the weather at a particular time. Thus in most years
a carpet of the herb Mercurialisperennis will inhibit growth of invading seedlings of the

Maintenance of species-richness in plant communities 131
tree Fraxinus excelsior in woodlands on boulder clay in eastern England (Wade, 1g59),
but in an unusually wet spring the Mercurialis dies back on marginal sites (Martin,
1968) and Fram‘nw, which is tolerant of waterlogging, can then grow through. The
many relationships of this kind, which must contribute to the maintenance of diversity,
have hardly begun to be explored.
VII. DISCUSSION
There can be no serious doubt that the kinds of differences between species in
regeneration requirements considered in this review contribute a finite amount to the
maintenance of species-richness in plant communities. The examples given all concern
the regeneration of seed plants, but a parallel case could be made out for the pteridophytes,
bryophytes, attached algae or fungi and indeed for corals and other attached
animals. The really difficult problem is to establish that any two species may co-exist
indefinitely on the basis of differences in the regeneration niche. If species A always
tends to oust species B over a period of years in a particular part of the world, when
individuals of the same physiological age are matched against each other, what are the
conditions necessary for differentiation in the regeneration niche to be a basis of
indefinite co-existence? There are two major conditions. The first is that B must be
able to persist in the community as long as the mean time between those events which
cause either the creation of a gap of a kind which favours the establishment of B more
than A or the creation of a gap at a place where B has propagules and A has not. The
second condition is that sufficient ‘B gaps’ must continue to arise as well as ‘A gaps’
in the area concerned; the exact proportion will be a major determinant of the
relative abundance of species B and A in the community. Intuitively it seems reasonable
that, in a temperate forest, large gaps should occur often enough to make possible the
persistence of birch as well as beech. It is less clear that the hoof-marks of sheep or deer
in a grassland should occur sufficiently often in places where species B has seed present
and species A has not. Clearly the question can be settled for any one plant community
only on the basis of detailed long-term studies of the gaps that arise, the differences
there are between species in their responses to gaps of different kinds and of the
differences there are in practice in terms of propagules of different species being
present on the site. The results of any such study are bound to be so complex as to
necessitate the building of a computer model of the situation, broadly speaking of the
kind developed for temperate deciduous forest by Botkin, Janak & Wallis (1972).
Persistence of species B in the presence of species A between the times of gap formation
may not necessarily be in the form of seed-producing adults; it may be as dormant seed
in the soil or as plants in an adjacent community, e.g. on river gravels or rock outcrops
next to the forest or grassland in question.
The idea that species-richness in plant communities is maintained in part as a
result of recurrent perturbations by outside forces is shared with the theory of Loucks
(1970). However, in the present account emphasis is also placed on the importance of
gaps in the community that arise through the senescence and death of individuals more
or less irrespective of outside forces and on the importance of a wide range of responses
9-2

132 P. J. GRUBB
to external factors in the plants of a species-rich community. Furthermore, external
factors are seen as very important not only in creating some of the gaps in the community
but also in determining which species are represented in any particular gap by
propagules (a function of recent seed-set, dispersal, etc.).
If differences in the regeneration niche can account for the long-term co-existence
of different species, just how different do species need to be? Particular interest
attaches to those genera where the most obvious differences are in phenology, e.g.
Miconia with nineteen species in Trinidad (Snow, 1965, 1968) or less remarkably
Guarea with four species in the rain-forest of part of Costa Rica (Frankie et al., 1974)
or Neolitsea with two species in the rain-forest of Japan (Ohwi, 1965). It is widely
accepted that there is competition between plants for pollinators (Free, 1968 ; Hocking,
1968; Heinrich & Raven, 1972; Kevan, 1972; Gentry, 1974) and animal vectors
of the seed (Snow, 1965, 1968) and the evolution of phenological spread is generally
seen to be a result of this competition (Richards, 1969; Mosquin, 1971 ; Stiles, 1975).
It is less often pointed out that such spread is also seen in species pollinated and
dispersed by wind, e.g. the annual grasses studied by Pemadasa & Love11 (1974).
The groups of species concerned may well differ in their exact requirements for
seed-set, as appears to be the case with six New Zealand species of Podocarpus (Fig. 6).
However, even if they have the same essential requirements for seed-set, the fact that
the weather fluctuates through the year, coupled with their different times of flowering
and fruiting, ensures (unless the plants are very tolerant) that no two years are exactly
similar in terms of the relative numbers of seeds produced per plant by different
species. Other things being equal, this must tend to perpetuate ail the species
indefinitely.
For most communities it seems unlikely that similar species will be found
ultimately to differ in only a single characteristic in the regeneration niche but it is
possible that this is the case in the astoundingly long series of species in certain genera
in some rain-forests, e.g. Eugenia and Shorea in south-east Asia or Diospyros and
Rinorea in Africa (Richards, 1969).
It is fashionable to emphasize the possible roles of predation by animals and
intraspecific allelopathy in the context of the most species-rich communities and
especially in the case of the long series of species in certain genera, but the general
importance of these two mechanisms has yet to be proven. Critical evidence is needed
to show that species are indeed unable to regenerate beneath their parents (though in
a comparable degree of shade under other species) and that the lack of regeneration is
specifically caused by predation or allelopathy.
The emphasis on differentiation in the regeneration niche is highly relevant to the
contentious issue of continua in vegetation. Whittaker (1965, 1967, 1969, 1972) has
repeatedly emphasized that gradient analysis leads to the conclusion that, while species
are clumped in their habitat-tolerances, no two species are quite the same in this
respect. He has suggested (Whittaker, 1969) that diversity in plant communities is
made possible by a partitioning of the habitat, and indeed his emphasis is almost
wholly on diversification in the habitat niche. In a popular text (Whittaker, 1975) he
gives the student the impression that groups of species with strongly similar habitat

Maintenance of species-richness in plant communities
I33
niches are not a general feature of vegetation. In fact most ecologists find that they are,
whether they are working in the deciduous forests, grasslands or weed communities of
Europe (Ellenberg, 1954, 1963 ; Duchaufour, 1960), the conifer forests and steppes of
the western United States (Daubenmire, 1968 b, 1970), the forests of eastern Australia
(Webb, Tracey, Williams & Lance, 1970) or those on tropical mountains (Wade &
McVean, 1969; Grubb & Stevens, 1976; Grubb & Tanner, 1976). This grouping of
species in habitat niches is very often accompanied by a striking conformation in
life-form, leaf-form, etc., and clearly many physiological characteristics in the
vegetative adult are similar in all the species within each group. Just why the species
involved should have ‘partitioned’ the physical environment into just so many
sections and not more is a very deep question, e.g. why are there four main forest
formations on most high tropical mountains and not two or six or twenty? Presumably
patterns of vegetational history are partly involved here. Within most habitat-groups
of species differentiation in the regeneration niche is almost certainly considerable.
Emphasis on the regeneration niche is also relevant to the many ordination studies
made on vegetation in the last decade. Some of the axes of variation detected are
bound to reflect regeneration characteristics rather than the features of the physical
environment that those who ordinate usually seek to identify; in the case of the
tropical rain-forest on one of the Solomon Islands some of the variation first found by
an ordination analysis (Greig-Smith, Austin & Whitmore, 1967) is now known to
reflect vegetation history (Whitmore, 1974).
The conclusion that species diversity has more to do with requirements for regeneration
than with partitioning of the habitat niche of the adult fits well with the growing
conviction of some evolutionists, e.g. Grant (1949), Stebbins (1951, 1970, 1g71),
Baker (1959, 1963, 1970) and van der Pijl(1960, 1961), that speciation and ultimately
the differentiation of genera and families of plants have primarily to do with adaptive
changes in reproductive characteristics, even though there are still many characters of
taxonomic importance that are hard to explain functionally (Ehrendorfer, I 973). It
seems that at all taxonomic levels evolutionary divergence may concern any aspect of the
niche. Thus several families have evolved in certain narrow and well-defined habitat
niches, while others have tremendously wide ranges. An inspection of any modern
northern European flora will show that the ecological separation of species in
most genera in that region is mainly through the habitat niche and the ecological
picture is primarily one of each habitat niche being filled by a single species from
several to many genera. Each genus is almost certain to be different from the next in
several aspects of the regeneration niche. There are, of course, cases of species with
virtually the same or very strongly overlapping habitat niches in certain genera, e.g.
Carex, Cephalanthera, Orchis, Ophrys, Rosa, Trifolium. Such cases are particularly
common in man-made communities and differences in the regeneration niche are
presumably very important in the maintenance of co-existence there, e.g. of Plantago
media and P. lanceolata in basic grassland (Sagar & Harper, 1964) or Ranuncuhs acris,
R. bulbosus and R. repens in certain pastures (Sarukhhn & Harper, 1973).
In regions of greater floristic richness than northern Europe differentiation in the
regeneration niche separating species in a genus appears to be generally more impor-
9-3

‘34 P. J. GRUBB
tant. This is true not only of tropical regions but also of certain temperate regions,
e.g. parts of northern China where the primary forests contained eight species of
Acer, nine of Betula, five of Tilia and five of Ulmus (Wang, 1961).
The evolution of diversity is here envisaged as an inevitable process whereby the
possible regeneration niches in the community are partitioned. There is no need to
involve the idea that there are selective advantages in evolution arising from greater
stability in systems of greater diversity, as suggested by MacArthur (1955) and
Hutchinson (1959). This supposed increased stability is, in any case, very much
questioned at the present time (May, 1975).
One of the central aims of much conservation is the preservation of diversity
(Westhoff, 1971 ; van der Maarel, 1971) and the theme of this review is therefore
highly relevant. It places an emphasis on the dynamic relations of plant communities,
relations which have been repeatedly overlooked in an age when classical phytosociology,
numerical analysis of vegetation and productivity studies have sapped the
energies of those who might otherwise have provided a sounder basis for positive
management in the conservation field. The need now is for proper attention to be paid
to each stage in the regeneration cycle. The most sophisticated studies will require
teams of research workers, long-term programmes and expertise in realistic modelling;
however, in the recording of many of the processes involved, e.g. annual flowering and
fruiting, amateur naturalists could play a vital role in the accumulation of valuable
information.
VIII. SUMMARY
I. According to ‘Gause’s hypothesis’ a corollary of the process of evolution by
natural selection is that in a community at equilibrium every species must occupy a
different niche. Many botanists have found this idea improbable because they have
ignored the processes of regeneration in plant communities.
2. Most plant communities are longer-lived than their constituent individual
plants. When an individual dies, it may or may not be replaced by an individual of the
same species. It is this replacement stage which is all-important to the argument
presented.
3. Several mechanisms not involving regeneration also contribute to the maintenance
of species-richness :
(a) differences in life-form coupled with the inability of larger plants to exhaust or
cut off all resources, also the development of dependence-relationships,
(b) differences in phenology coupled with tolerance of suppression,
(c) fluctuations in the environment coupled with relatively small differences in
competitive ability between many species,
(d) the ability of certain species-pairs to form stable mixtures because of a balance
of intraspecific competition against interspecific competition,
(e) the production of substances more toxic to the producer-species than to the
other species,
(f) differences in the primary limiting mineral nutrients or pore-sizes in the soil for
neighbouring plants of different soecies. and

Maintenance of species-richness in plant communities I3 5
(g) differences in the competitive abilities of species dependent on their physiological
age coupled with the uneven-age structure of many populations.
4. The mechanisms listed above do not go far to explain the indefinite persistence
in mixture of the many species in the most species-rich communities known.
5. In contrast there seem to be almost limitless possibilities for differences between
species in their requirements for regeneration, i.e. the replacement of the individual
plants of one generation by those of the next. This idea is illustrated for tree species
and it is emphasized that foresters were the first by a wide margin to appreciate its
importance.
6. The processes involved in the successful invasion of a gap by a given plant
species and some characters of the gap that may be important are summarized in
Table 2.
7. The definition of a plant’s niche requires recognition of four components:
(a) the habitat niche,
(b) the life-form niche,
(c) the phenological niche, and
(d) the regeneration niche.
8. A brief account is given of the patterns of regeneration in different kinds of
plant community to provide a background for studies of differentiation in the regeneration
niche.
9. All stages in the regeneration-cycle are potentially important and examples of
differentiation between species are given for each of the following stages:
(a) Production of viable seed (including the sub-stages of flowering, pollination and
seed-set),
(b) dispersal, in space and time,
(c) germination,
(d) establishment, and
(e) further development of the immature plant.
10. In the concluding discussion emphasis is placed on the following themes:
(a) the kinds of work needed in future to prove or disprove that differentiation in
the regeneration niche is the major explanation of the maintenance of species-richness
in plant communities,
(b) the relation of the present thesis to published ideas on the origin of phenological
spread,
(c) the relevance of the present thesis to the discussion on the presence of continua
in vegetation,
(d) the co-incidence of the present thesis and the emerging ideas of evolutionists
about differentiation of angiosperm taxa, and
(e) the importance of regeneration-studies for conservation.
I am grateful to Dr A. S. Watt for inspiring my interest in the regeneration of vegetation, to Dr E. W.
Jones for references on the fruiting of forest trees, and to Drs R. S. Clymo, E. I. Newman and R. W.
Snaydon for criticizing a first draft of this paper. Miss S. M. Bishop drew Figs. 1-6 and 8-10.

P. J. GRUBB
IX. REFERENCES
ASH, J. E. & BARKHAM, J. P. (1976). Changes and variability in the field layer of a coppiced woodland in
Norfolk, England. Journal of Ecology 64, 697-712.
ASHTON, P. S. (1969). Speciation among tropical forest trees: some deductions in the light of recent
evidence. Biological Journal of the Linnean Society I, 155-96.
ASPINALL, D. (1960). An analysis of competition between barley and white persicaria. 11. Factors
determining the course of competition. Annals of Applied Biology 48, 637-54.
ASPINALL, D. & MILTHORPE, F. L. (1959). An analysis of the competition between barley and white
persicaria. I. The effects of growth. Annals of Applied Biology 47, 156-72.
ASPINALL, D., NICHOLLS, P. B. & MAY, L. H. (1964). The effects of soil moisture stress on the growth
of barley. I. Vegetative development and grain yield. AustralianJournal of Agricultural Research IS,
729-45.
AUBREVILLE, A. (1938). La for& coloniale: les for&ts de l'Afrique occidentale fraqaise. Annales
Acadkmie des sciences coloniales, Paris, 9, 1-245.
AUCLAIR, A. N. & COTTAM, G. (1971). Dynamics of Black Cherry, Prunus serotina Erhr., in southern
Wisconsin oak forests. Ecological Monographs 41, I 53-77.
AUSTIN, M. P. (1968). Pattern in a Zerna erecta dominated community.Journa1 of Ecology 56, 197-218.
BAKER, H. G. (1959). Reproductive methods as factors in speciation in flowering plants. Cold Spring
Harbour Symposia on Quantitative Biology 24, 177-91.
BAKER, H. G. (1963). Evolutionary mechanisms in pollination biology. Science 139, 877-83.
BAKER, H. G. (1970). Evolution in the tropics. Biotropica 2, 101-111.
BARON, J. F. (1969). Ten years of forest seed crops in California. Journal of Forestry 67, 490-2.
BARROW, M. D., COSTIN, A. B. & LAKE, P. (1968). Cyclical changes in an Australian fjaeldmark
community. Journal of Ecology 56, 89-96.
BASKIN, J. M. & BASKIN, C. C. (1971 a). Germination ecology and adaptation to habitat in Leavenworthia
spp. (Cruciferae). American Midland Naturalist 85, 22-35.
BASKIN, J. M. & BASKIN, C. C. (1971 b). Germination ecology of Phacelia dubia var. dubia in Tennessee
glades. American Journal of Botany 58, 98-104.
BEADLE, N. C. W. (I 940). Soil temperaturesduring forest fires and their effect on the survival of vegetation.
Journal of Ecology 28, 18-92.
BEARD, J. S. (1969). The natural regions of the deserts of Western Australia. Journal of Ecology 57,
677-7 I I.
BEDFORD, THE DUKE OF, & PICKERING, S. U. (1919). Science and Fruit Growing. Macmillan, London.
BERGH, J. P. VAN DER & WIT, C. G. DE (1960). Concurrentie tussen Timothen en Reukgras. Mededelingen
Instituut voor biologisch en scheikundig onderzoek van landbouwgewassen IZI, I 55-65.
BEVERIDGE, A. E. (1964). Dispersal and destruction of seed in central North Island podocarp forests.
Proceedings of the New Zealand Ecological Society 11, 48-55.
BEVERIDGE, A. E. (1973). Regeneration of podocarps in central North Island forest. New ZeaZandJournal
of Forestry 18, 23-35.
BOE, K. N. (1954). Periodicity of cone crops for five Montana conifers. Proceedings of the Montana
Academy of Sciences 14, 5-9.
BOHART, G. E. & KOEBER, T. W. (1972). Insects and seed production. In Seed Biology, vol. 3 (ed. T. T.
Kozlowski), pp. 1-53. Academic Press, New York.
BORNKAMM, R. (I 96 I a). Zur quantitativen Bestimmungvon Konkurrenzkraft und Wettbewerbsspannung.
Berichte der deutschen Botanischen Geselkchaft 74, 75-83.
BORNKAMM, R. (1961 b). Zur lichtkonkurrenz von Ackerunkrautern. Flora, Jena N.F. 151, 126-43.
BOTKIN, D. B., JANAK, J. F. &WALLIS, J. R. (1972). Some ecological consequencesof acomputer model
of forest growth. Journal of Ecology 60, 849-72.
BRAY, J. R. (1956). Gap phase replacement in a maple-basswood forest. Ecology 37, 598-600.
BUDOWSI~I, G. (1965). The distribution of tropical American rain forest species in the light of successional
processes. Turrialba 15, 40-2.
BURGES, A. (1951). The ecology of the Cairngorms. 111. The Empetrum-Vaccinium zone. Journal of
Ecology 39, 271-84.
BYKOV, B. A. (1974). Fluctuations in the semidesert and desert vegetation of the Turanian plain. In
Vegetation Dynamics (ed. R. Knapp), Part 8 of Handbook of Vegetation Science, pp. 243-51. Junk,
The Hague.
CANTLON, J. E. (1969). The stability of natural populations and their sensitivity to technolog). Diversity
and Stability in Ecological Systems. Brookhaven Symposia in Biology 22, 197-203.
CAPUTA, J. (1948). Untersuchungen uber die Entwicklung einiger Grsser und Kleearten in Reinsaat und
Mischung. Landwirtschaftliches Jahrbuch der Schweiz TO (849), 1-127.

Maintenance of species-richness in plant communities
CAVE=, P. B. & HARPER, J. L. (1967). Studies in the dynamics of plant populations. I. The fate of seed
and transplants introduced into various habitats. Journal of Ecology 55, 59-71,
CHADWICK, M. J. (1961). Nardus stricta, a weed of hill grazings. In The biology of Weeds (ed. J. L.
Harper). Symposia of the British Ecological Society I, 246-56.
CHAMBERS, T. C. (1959). Pattern and process in a New Zealand subalpine plant community. Vegetatio
8, 209-14.
CHAMPNESS, S. S. & MORRIS, K. (1948). The population of buried viable seeds in relation to contrasting
pasture and soil types. Journal of Ecology 36, 1 4 ~ 3 .
CHILVERS, G. A. & BRITTAIN, E. G. (1972). Plant competition mediated by host-specific parasites - a
simple model. Australian Journal of Biological Sciences 25, 749-56.
CHIPPINDALE, H. G. & MILTON, W. E. J. (1934). On the viable seeds present in the soil beneath
pastures. Journal of Ecology 22, 508-3 I.
CLARK, M. B. (1970). Seed production of hemlock and cedar in the Interior Wet Belt Region of British
Columbia related to dispersal and regeneration. Research Notes British Columbia Forest Service (5 I),
1-11.
CLEMENTS, F.E., WEAVER, J. E. & HANSON, H. C. (1929). Plant Competition. Publications of the Carnegie
Institution, Washington (398), i-xvi, 1340.
COCKAYNE, L. (1928). The Vegetation of Nee0 Zealand, 2nd ed. Engelmann, Leipzig.
CONNELL, J. H. (1971). On the role of natural enemies in preventing competitive exclusion in some
marine animals and in rain forest trees. In Proceedings of the Advanced Study Institute on Dynamics of
Numbers in Populations, Oosterbeek, 1970 (ed. P.J. den Boer and G. R. Gradwell), pp. 298-312.
Centre for Agricultural Publishing and Documentation, Wageningen.
COOMBE, D. E. (1966). The seasonal light climate and plant growth in a Cambridgeshire wood. In Light
as an Ecological Factor (ed. R. Bainbridge, G. C. Evans and 0. Rackham). Symposia of the British
Ecological Society 6, 14846.
COUPLAND, R. T. (1974). Fluctuations in North American grassland vegetation. In Vegetation Dynamics
(ed. R. Knapp, Part 8 of Handbook of Vegetational Science, pp. 233-41. Junk, The Hague.
CUATRECASAS, J. (1934). Observaciones geobotanicas en Colombia. Trabajos del Muse0 nacional de
ciencias naturales, Madrid, serie botanica (27), 1-14.
CURTIS, J. T. (1959). The Vegetation of Wisconsin. University of Wisconsin Press, Madison.
DAUBENMIRE, R. (1960). A seven-year study of cone production as related to xylem layers and temperature
in Pinus ponderosa. American Midland Naturalist 64, 187-93.
DAUBENMIRE, R. (1968~). Plant Communities. Harper and Row, New York.
DAUBENMIRE, R. (1968 b). Forest vegetation of eastern Washington and northern Idaho. Technical
Bulletin of the Agricultural Experiment Station Washington State (60), 1-104.
DAUBENMIRE, R. (1970). Steppe vegetation of Washington. Technical Bulletin of the Agricultural Experiment
Station Washington State (62), 1-131.
DAVIES, S. J. J. F. (1976). Studies on the flowering season and fruit production of some arid zone shrubs
and trees in western Australia. Journal of Ecology 64, 665-87.
DELEUIL, G. (1951). Origine des substances toxiques du sol des associations sans thkrophytes du
Romarino-Ericion. Compte rendu hebdomadaire des shnces de Z’Acadlmie des sciences, Paris 232,2038-9.
DIELS, L. (1937). Beitrage zur Kenntnis der Vegetation und Flora von Ecuador. Bibliotheca botanica
116, 1-190.
DUCHAUFOUR, P. H. (1960). Stations, types d’humus et groupements bcologiques. Rewue forestihe
frangaise, Nancy 12, 484-94.
EHRENDORFER, F. (1973). Adaptive significance of major taxonomic characters and morphological
trends in angiosperms. In Taxonomy and Ecology (ed. V. H. Heywood), pp. 317-27. Academic Press,
London.
ELLENBERG, H. (1954). Landwirtschaftliche Pflanzensoziolcp.e, vol. I. Ulmer, Stuttgart.
ELLENFIERG, H. (1963). Vegetation Mitteleuropas mit den Alpen. Ulmer, Stuttgart.
FENNEF~, M. (1975). Factors affecting the distribution of strict calcicoles. Ph.D. dissertation, University of
Cambridge.
FLOWER-ELLIS, J. G. K. (1971). Age structure and dynamics in stands of bilberry (Vaccinium myrtillus
L.). Research Notes, Department of Forest Ecology and Forest Soils, Royal College of Forestry,
Stockholm (9), i-x, 1-108.
FOGGIE, A. (1960). Natural regeneration in the humid tropical forest. Caribbean Forester 27, 73-81.
FORCIER, L. K. (1975). Reproductive strategies and the co-occurrence of climax tree species. Science
189, 808-10.
FOWELLS, H. A. & SCHUBERT, G. H. (1956). Seed crops of forest trees in the Pine region of California.
United States Department of Agriculture Technical Bulletin ( I I~o), 1-48.
FRANKIE, G. W., BAKER, H. G. & OPLER, P. A. (1974). Comparative phenological studies of trees in
Tropical Wet and Dry forests in the lowlands of Costa Rica. Journal of Ecology 62, 881-913.
I37

P. J. GRUBB
FRANKLYN, J. F. & DYRNESS, C. T. (1969). Vegetation of Oregon and Washington. United States
Department of Agriculture Forest Service Research Paper (PWN-So), i-vi, 1-216.
FREE, J. B. (1968). Dandelion as a competitor to fruit trees for bee visits. Journal of Applied Ecology
5, 16978.
FRIEDMAN, J. & ORSHAN, G. (1975). The distribution, emergence and survival of seedlings of Artemisia
herba-alba Asso in the Negev - Desert of Israel in relation to distance from the adult plants. Yournal of
Ecology 63, 627-32.
GENTRY, A. H. (1974). Flowering phenology and diversity in tropical Bignoniaceae. Biotropica 6,
64-8.
GENTRY, A. H. (1976). Bignoniaceae of Southern Central America: distribution and ecological specificity.
Biotropica 8, I 17-3 I.
GILBERT, 1. M. (1959). Forest succession in the Florentine Valley. Proceedings of the Royal Society of
Tasmania 93, I 29-5 I.
GILLETT, J. B. (1962). Pest pressure, an underestimated factor in evolution. In Taxonomy and Geography
(ed. D. Nichols). Publications of the Systematics Assciciation 4, 37-46.
GODWIN, H. (1941). Studies in the ecology of Wicken Fen. IV. Crop-taking experiments. Journal of
Ecology 29, 83-106.
Pi. B. rony6esa (GOLUBEVA, I. V.) (1968). Amamma ceMemozl ~ ~O~~KTEBHOCTH IIOII~JIXUE~ Knesepa
ropHoro (Trifolimmontanum L.) H KOB~IJIS~ nepnmoro (Stipapennata L.)B paawrx t$moqeHoTHsecIcHx
YCJIOBH~X ~ ~ O B O memi & (The dynamics of the seed productivity of Trzfalium montanum L. and Stipa
pennata L. populations under different phytocoenotic conditions of a meadow steppe). Bornanuvecicic
wcypHan (Botanicheskii zhurnal SSSR) 53, 1604-1 I.
G~MEZ-POMPA, A. (1971). Posible papel de la vegetaci6n secundaria en la evoluci6n de la flora
tropical. Biotropica 3, 125-35.
GOODALL, D. W. (1970). Statistical plant ecology. Annual Review of Ecology and Systematics I, 99-124.
GRAHAM, S. A. (1941). Climax forests of the Upper Peninsula of Michigan. Ecology 22, 355-62.
GRANT, U. (1949). Pollination systems as isolating mechanisms in angiosperms. Evolution, Lancaster,
Pennsylvania 3, 82-97.
GRATKOWSKI, H. (1961). Brush seedlings after controlled burning of brushlands in southwestern
Oregon. Journal of Forestry 59, 885-8.
GREIG-SMITH, P., AUSTIN, M. P. & WHITMORE, T. C. (1967). The application of quantitative methods
to vegetation survey. I. Association-analysis and principal component ordination of rain forest.
Journal of Ecology 55, 483-503.
GRIME, J. P. (1966). Shade avoidance and shade tolerance in flowering plants. In Light as an Ecological
Factor (ed. R. Bainbridge, G. C. Evans and 0. Rackham). Symposia of the British Ecological Society
6, 187-207.
GRIME, J. P. (1973 a). Competitive exclusion in herbaceous vegetation. Nature 242, 344-7.
GRIME, J. P. (1973b). Competition and diversity in herbaceous vegetation. Nature 244, 3 I I.
GRIME, J. P., MACPHERSON-STEWART, S. F. & DEARMAN, R. S. (1968). An investigation of leaf palatability
using the snail Cepaea nemoralis L. Journal of Ecology 56, 405-20.
GRUBB, P. J. (1976). A theoretical background to the conservation of ecologically distinct groups of
annuals and biennials in the chalk grassland ecosystem. Biological Conservation 10, 5376.
GRUBB, P. J. & STEVENS, P. F. (1976). The forests of the Fatima basin and Mt Kerigomna and a Review of
Montane and Subalpine Forests elsewhere in Papua New Guinea. Department of Biogeography and
Geomorphology Publication (BG/5). Australian National University, Canberra. (In the press.)
GRUBB, P. J. & TANNER, E. V. J. (1976). The montane forests and soils of Jamaica: a re-assessment.
Journal of the Arnold Arboretum 57, 313-68.
GUEVARA, S. Sz G~MEZ-POMPA, A. (1972). Seeds from surface soils in a tropical region of Veracruz,
Mexico. Journal of the Arnold Arboretum 53, 312-35.
GUYOT, L. (1960). Sur la presence dans les terres cultivkes et incultes des semences dormantes des
espbces adventices. Bulletin du Service de la carte phytogkographique B 5, 197-254.
HAIZEL, K. A. & HARPER, J. L. (1973). The effects of density and the timing of removal on interference
between barley, white mustard and wild oats. Journal of Applied Ecology 10, 23-31.
HARBERD, D. J. (1961). Observations on population structure and longevity of Festuca rubra L. New
Phytologist 60, 184-206.
HARLAN, H. V. & MARTINI, M. L. (1938). The effect of natural selection in a mixture of barley varieties.
Journal of Agricultural Research 57, I 89-99.
HARPER, J. L. (1961). Approaches to the study of plant competition. In Mechanisms in Biological
Competition (ed. F. L. Milthorpe). Symposia of the Society for Experimental Biology 15, 1-39.
HARPER, J. L. (1965). Establishment, aggression and cohabitation in weedy species. In The Genetics of
Colonising Species (ed. H. G. Baker and G. L. Stebbins), pp. 243-68. Academic Press, New York.
HARPER, J. L. (1967). A Darwinian approach to plant ecology. Journal of Ecology 55, 247-70.

Maintenance of species-richness in plant communities ‘39
HARPER, J. L. (1969). The role of predation in vegetational diversity. Diversity and Stability in Ecological
Systems. Brookhaven Symposia in Biology 22, 48-61.
HARPER, J. L., CLATWORTHY, J. N., MCNAUGHTON & SAGAR, G. R. (1961). The evolution and ecology of
closely related species living in the same area. Evolution, Lancaster, Pennsylvania 15, 209-27.
WER, J. L., LOVELL, P. H. & MOORE, K. G. (1970). The shapes and sizes of seeds. Annual Review of
Ecology and Systematics I, 327-56.
~ E R J. , L.,WILLIAMS, J. T. & SAGAR, G. R. (1965). The behaviour of seeds in soil. I. The heterogeneity
of soil surfaces and its role in determining the establishment of plants from seed. Journal of
Ecology 53, 273-86.
HEINRICH, B. & RAVEN, P. H. (1972). Energetics and pollination ecology. Science 176, 597-602.
HEWETSON, C. E. (1956). A discussion on the ‘climax’ concept in relation to the tropical rain forest.
Empire Forestry Rm’ew 35, 274-1.
&m, G. (1852). Verhalten der Waldbaumegegen Licht und Schatten. Erlangen.
HOCKING, B. (1968). Insect-flower associations in the high Arctic with special reference to nectar.
Oikos 19, 359-88.
HORN, H. S. (1975). Forest succession. Scientific American 232 (s), 90-8.
HUFFAKER, C. B. & KWNET, C. E. (1959). A ten-year study of vegetational changes associated with
biological control of Klamath weed. Journal of Range Management 12,69-82.
HUTCHINSON, G. E. (1957). Concluding remarks. Population Studies: Animal Ecology and Demography.
Cold Spring Harbour Symposia on Quantitative Biology w, 415-7.
HUTCHINSON, G. E. (1959). Homage to Santa Rosalia or Why are there so many kinds of animals?
American Naturalist 93, 145-59.
HUTCHINSON, T. C. (1967). Comparative studies of the ability of species to withstand prolonged periods
of darkness. Journal of Ecology 55, 291-9.
Iwm, H. & TOTSIJKA, T. (1959). Ecological and physiological studies on the vegetation of Mt Shimagare.
11. On the crescent-shaped “Dead Trees Strips” in the Yatsugatake and the Chichibu Mountains.
Botanical Magazine, Tokyo 72, 255-60.
JACKSON, W. D. (1968). Fire, air, water and earth - an elemental ecology of Tasmania. Proceedings of the
Ecological Society of Australia 3, 9-16.
JACQUARD, P. (1968). Manifestation et nature des relations sociales chez les vggktaux superieurs.
Oecologia Plantarum 3, 137-68.
JANZEN, D. H. (1969). Seed-eaters versus seed size, number, toxicity and dispersal. Evolution, Lancaster,
Pennsylvania 23, 1-27.
JANZEN, D. H. (1970). Herbivores and the number of tree species in tropical forests. Am*can
Naturalist zoq, 501-28.
JANZEN, D.H. (1971). Seed predation by animals. Annual Review of Ecology and Systematics 2,
465-92.
JARVIS, M. S. (1963). A comparison between the water relations of species with contrasting types of
geographical distribution in the British Isles. The Water Relations of Plants (ed. A. J. Rutter and
F. H. Whitehead). Symposia of the British Ecological Society 3, 289312.
JEFFREY, D. W. & PIGOTT, C. D. (1973). The response of grasslands on sugar-limestone in Teesdale to
application of phosphorus and nitrogen. Journal of Ecology 61, 85-92.
JONES, E. W. (1945). The structure and reproduction of the virgin forest of the North Temperate
Zone. New Phytologist 4, 130-48.
JONES, E. W. (19554). Ecdogical studies on the Rain Forest of southern Nigeria. IV. The plateau
forest of the Okomu Forest Reserve. Journal of Ecology 43, 564-94, 4.83-1 17.
B. r.KapnOB(I(ARPOV,V. G.) (r96r).OB~K0a~ypeE~~KopEelt
aerrrenbmxn TaembIx TP~ B enoBm necax (On the influence of tree root competition on the
photosynthetic activity of the herb layer in spruce forest). AOKM~M AKadeMUU Hap CCCP (Dokladp
Akudemii nauk SSSR) 140, 1205-8.
KARR, E. J., LINCK, A. J. & SWANSON, C. A. (1959). The effect of short periods of high temperature
during day and night periods on pea yields. American Journal of Botany 46, 91-3.
JSEATINGE, T. H. (1975). Plant community dynamics in wet heathland. Journal of Ecology 63, 16372.
KBRNER VON ~ILAUN, A. (1902). TheNaturalHistory of Plants (trans. F. W. Oliver). Blackie, London.
KBVAN, P. G. (1972). Insect pollination of high arctic flowers. Journal of Ecology 60, 831-47.
KING, T. J. (1975). Inhibition of seed germination under leaf canopies in Arenaria serpyllifolia, Veronica
arvm‘s and Cerastium holosteoides. New Phytologist 75, 87-90.
KNAPP, R. (1974). Mutual influences between plants, allelopathy, competition and vegetation changes.
In Vegetation Dynamics (ed. R. Knapp), Part 8 of Handbook Vegetation Science, pp. 111-22. Junk,
The Hague.
KNIGHT, G. H. (1964). Some factors affecting the distribution of Endymion nonscriptlrs (L.) Garcke in
Warwickshire woods. J o m l of Ecology 42,405-zr.
JTepeSbeBHa ~~EMEJuIWOEFIyIo

P. J. GRUBB
KOLLER, D, (1969). The physiology of dormancy and survival of plants in desert environments. In
Dormancy and Surptival (ed. H. W. Woolhouse). Symposia of the Society for Experimental Biology
23,449-69.
KOLLER, D. (1972). Environmental control of seed germination. In Seed Biology, vol. 2 (ed. T. T.
Kozlowski), pp. 1-101. Academic Press, New York.
KORCHAGIN, A. A. & KARPOV, V. G. (1974). Fluctuations in coniferous taiga communities. In Vegetation
Dynamics (ed. R. Knapp), Part 8 of Handbook of Vegetation Science, pp. 225-31. Junk, The
Hague.
KREBS, C. J. (1972). Ecology: an Experimental Analysis of Distribution and Abundance. Harper and
Row, New York.
KUJALA, V. (1926). Untersuchungen uber die Waldvegetation in Sudund Mittlelfinnland. I. Zur
Kenntnis des okologisch-biologischen Charakters der Pflanzenarten unter spezieller Beriicksichtigung
der Bildung von Pflanzenverein. A. Gefasspflanzen. Metsatienteellisen Koelaitoksen Julkaisuja 10
(I), 1-140.
KYDD, D. D. (1964). The effect of different systems of cattle grazing on the botanical composition of
permanent downland pasture. Journal of Ecology 52, 139-49.
LAMBERT, R. G. & LINCK, A. J. (1958). Effects of high temperature on the yield of peas. Plant Physiclogy,
Lancaster, Pennsylvania 33, 347-50.
LAUER, E. (1953). uber die Keimtemperatur von Ackerunkrautern und deren Einfluss auf die Zusammensetzung
von Unkrautgesellschaften. Flora, Jena N.F. 140, 551-95.
LOUCKS, 0. L. (1970). Evolution of diversity, efficiency and community stability. American Zoologist
10, 17-25.
LOWRY, W. P. (1966). Apparent meteorological requirements for abundant cone crop in Douglas-Fir.
Forest Science 12, 185-92.
MAAREL, E. VAN DER (1971). Plant species diversity in relation to management. In The Scientific
Management of Animal and Plant Communities for Consematwn (ed. E. DufFey and A. S. Watt).
Symposia of the British Ecological Society 11, 45-63.
MACARTHUR, R. H. (1955). Fluctuations of animal populations, and a measure of community stability.
ECOk?Y 36, 533-6.
MCNAUGHTON, S. J. (1967). Relationships amongst functional properties of Californian grassland.
Nature 216, 168-9.
MCNAUGHTON, S. J. (1968~). Autotoxic feedback in relation to germination and seedling growth in
Typha latifolia. Ecology 49, 367-9.
MCNAUGHTON, S. J. (1968b). Structure and function of Californian grassland. Ecology 49, 86272.
MCPHERSON, J. K. & MULLER, C. H. (1969). Allelopathic effects of Adenostoma fasciculatum, Chamise’,
in the Californian chaparral. Ecological Monographs 39, 177-98.
MCWILLIAM, J. R., CLEMENTS, R. J. & DOWLING, P. M. (1970). Some factors influencing the germination
and early seedling development of pasture plants. Australian Journal of Agricultural Research
21, 19-32.
MAJOR, J. & PYOTT, W. T. (1966). Buried, viable seeds in two Californian bunchgrass sites, and their
bearing on the definition of a flora. Vegetatio 13, 253-82.
MARKS, P. L. (1974). The role of pin cherry (Prunuspensylvanica L.) in the maintenance of stability in
northern hardwood ecosystems. Ecological Monographs 4, 73-88.
MARSHALL, D. R. & JAIN, S. K. (1969). Interference in pure and mixed populations of Avenafatua and
A. barbata. Journal of Ecology 57, 251-70.
MARTIN, M. H. (1968). Conditions affecting the distribution of Mercurialis perennis L. in certain
Cambridgeshire woodlands. Journal of Ecology 56, 777-93.
MAY, R. M. (1975). Stability and Complexity in Model Ecosystems. 2nd ed. University Press, Princeton,
New Jersey.
MEDWAY, LORD (1972). Phenology of a tropical rain forest in Malaya. BiologicalJournal of the Linnean
Society 4, I 17-46.
MILES, J. (1973). Early mortality and survival of self-sown seedlings in Glenfeshie, Inverness-shire.
Journal of Ecology 61, 93-8.
MILES, J. (1974). Effects of experimental interference with stand structure on establishment of seedlings
in Callunetum. Journal of Ecology 62, 675-87.
MonwIoB A. A. (MOLEANOV, A. A.) (1967). reorpa@ari nnonoHomeHm rnameimx npesecHbrx
nopon B CCCP (Geographical Distribution of the Fruit-bearing of Main Woodland Trees in the USSR).
&i3naTenbcTeo cmayKaB (Izdatel’stvo‘ Nauka’), Moscow.
MOONEY, H. A. & DUNN, L. E. (1970). Convergent evolution of Mediterranean-climate evergreen
scleropyll shrubs. Evolution, Lancaster, Pennsylvania ~ q, 292-303.
MORGAN, G. H. (1965). A colony of Senecio integrifolius at Burham, Kent, with some notes on investigations
of the growth of the plants. Bulletin of the Kent Field Club 3, 26-49.

Maintenance of species-richness in plant communities 141
MORRIS, R. F. (1951). The effects of flowering on the foliage production and growth of balsam fir.
Forestry Chronicle 27, 40-57.
MOSQUIN, T. (1971). Competition for pollinators as a stimulus for the evolution of flowering time.
Oikos 22,398-402.
MOTT, J. J. (1972). Germination studies on some annual species from an arid region of Western
Australia. Journal of Ecology 60, 293-304.
MOTT, J. J. (1974). Factors affecting seed germination in three annual species from an arid region of
Western Australia. Journal of Ecology 62, 699709.
NEWMAN, E. I. (1963). Factors controlling the germination date of winter annuals. Journal of Ecology
51, 625-38.
NEWMAN, E. I. (1964). Factors affecting the seed production of Teesdalia nudicaulis. I. Germination date.
Journal of Ecology 52, 391-404.
NEWMAN, E. I. (1965). Factors affecting the seed production of Teesdalia nudicaulis. 11. Soil moisture
in spring. Journal of Ecology 53, 211-32.
NEWMAN, E. I. (1973). Competition and diversity in herbaceous vegetation. Nature 244, 310.
NEWMAN, E. I. & ROVIRA, A. D. (1975). Allelopathy among some British grassland species. Journal of
EcologY 63, 727-37.
NICHOLSON, D. I. (1960). Light requirements of seedlings of five speices of Dipterocarpaceae. Malayan
Forester 23, 344-56.
Om, H. (1965). Flora of Japan (English edition edited by F. G. Meyer and E. H. Walker). Smithsonian
Institution, Washington D.C.
OINENEN, E. (1967~). Sporal regeneration of bracken (Pteridium aquilinum (L.) Kuhn.) in Finland in the
light of the dimensions and the age of its clones. Acta Forestalia Fennica 83 (I), 1-96.
OINENEN, E. (19673). The correlation between the size of Finnish braken (Pteridium aquilinum (L.)
Kuhn.) clones and certain periods of site history. Acta Forestalia Fennica 83 (2), 1-51.
OLATOYE, S. L. & HALL, M. A. (1973). Interaction of ethylene and light on dormant weed seeds. In
Seed Ecology (ed. W. Heydecker), pp. 233-49. Butterworths, London.
OSHIMA, Y., KIMURA, M., IWAKI, H. & KUROIWA, S. (1958). Ecological and physiological studies on the
vegetation of Mt. Shimagare. I. Preliminary survey of the vegetation of Mt. Shimagare. Botanical
Magazine, Tokyo 71, 289-301.
PARHAM, M. R. (1970). A comparative study of the mineral nutrition of selected halophytes andglycophytes.
Ph.D. thesis, University of Norwich.
PEMADASA, M. A. & LOVELL, P. H. (1974). Factors controlling the flowering time of some dune annuals.
Journal of Ecology 52, 869-80.
PERTULLA, U. (1941). Untersuchungen iiber die generative und vegetative Vermehrung der Blutenpflanzen
in der Wald Hainwiesen und Hainfelsenvegetation. Annales Academiae scientiarum Fennicae
58, (I), 1-388.
PIGOTT, C. D. (1968). Biological Flora of the British Isles: Cirsium acaulon (L.) Scop. Journal of
Ecology 56, 597612.
PIGOTT, C. D. (1975). Natural regeneration of Tilia cordata in relation to forest-structure in the forest of
Biafowieza, Poland. Philosophical Transactions of the Royal Society B 270, I 51-79.
PIJL, L. VAN DER (1960). Ecological aspects of flower evolution. I. Phyletic evolution. Evolution,
Lancaster, Pennsylvania 14, 403-16.
PIJL, L. VAN DER (1961). Ecological aspects of flower evolution. 11. Zoophilous flower classes. Evolution,
Lancaster, Pennsylvania 15, 44-59.
PIJL, L. VAN DER (1971). Principles of Dispersal in Higher Plants. 2nd ed. Springer, Berlin.
PLATT, W. J. (1975). The colonization and formation of equilibrium plant species associations on badger
disturbances in tall-grass prairie. Ecological Monographs 45,285-305.
POORE, M. E. D. (1967). The concept of the association in tropical rain forest. Journal of Ecology 55,
46P-47P.
POORE, M. E. D. (1968). Studies in Malaysian rain forest. 1. The forest on triassic sediments in Jengka
Forest Reserve. Journal of Ecology 56, 143-96.
PUTWAIN, P. D. & HARPER, J. L. (1970). Studies in the dynamics of plant populations. 111. The influence
of associated species on populations of Rumex acetosa L. and R. acetosella L. in grassland. Journal of
Ecology 58, 251-64.
Pa60THOB T. A. (RABOTNOV, T. A.) (1950). XKH3HeHHbIfi IlHKn MHorOneTHHx TpaSHHECTbIX PaCTeHd
B nyrobIx qe~osax (Life cycles of perennial herbage plants in meadow coenoses). Tpyh
EomanuqecKozo Nncmumyma AKadeMuu Hayrc CCCP (. TruQ . Botanicheskogo institutu Akademzy nauk
SSSR, series 3) 6, 7-204.
RABOTNOV, T. A. (1969~). Plant regeneration from seed in meadows of the USSR. Herbage Abstracts

P. J. GRUBB
RABOTNOV, T. A. (1969b). On coenopopulations of perennial herbaceous plants in natural coenoses.
Vegetatio 19, 87-95.
RABOTNOV, T. A. (1974). Differences between fluctuations and seasons. In Vegetation Dynamics (ed
R. Knapp), Part 8 of Handbook of Vegetation Science, pp. 19-24. Junk, The Hague.
RAMSBOTTOM, J. (1953). Mushrooms and Toadstools. Collins, London.
RATCLIFFE, D. (1961). Adaptation to habitat in a group of annual plants.Journa1 of Ecology 49, 187-203.
RICHARDS, P. W. (1969). Speciation in the tropical rain forest and the concept of the niche. Biological
Journal of the Linnean Society I, 149-53.
RICHARDSON, A. E. U., TRUMBLE, H. C. & SHAPTER, R. E. (1932). The influence of growth stage and
frequency of cutting on the yield and composition of a perennial grass - Phalaris tuberosa. Bulletin
of the Council for Scientific and Industrial Research (Australia)(66), 1-33.
ROBBINS, J. S. & DOMINGO, C. E. (1953). Some effects of severe soil moisture deficits at specific growth
stages in corn. Agronomy Journal 45, 618-21.
ROLLET, B. (1969). La rtgtntration naturelle en for& dense humide sempervirente de plaine de la
Guyane Vtnkzutlienne. Bois et for& des tropiques I-, 19-38.
RUTTER, A. J. (1955). The composition of wet heath vegetation in relation to the water-table. Journal of
Ecology. 43, 507-43.
SAGAR, G. R. & HARPER, J. L. (1964). Biological Flora of the British Isles: Phntago mjor L., P. media L.
and P. lanceolata L. Journal of Ecology 52, 189-221.
SALISBURY, E. J. (1929). The biological equipment of species in relation to competition. Journal of
Ecology 17, 197-222.
SALISBURY, E. J. (1941). The Reproductive Capacity of Plants. Bell, London.
SALISBURY, SIR EDWARD (1974). Seed size and mass in relation to environment. Proceedings of the Royal
Society B 186, 83-8.
SARUKHAN, J. (1974). Studies on plant demography: Ranunculus repens L., R. bulbosus L. and R. acris L.
11. Reproductive strategies and seed population dynamics. Journal of Ecology 62, 151-77-
SARUKHAN, J. & HARPER, J. L. (1973). Studies on plant demography: Rammculus repens L., R. bulbosus
L. and R. acris L. I. Population flux and survivorship. Journal of Ecology 61, 675-716.
SCHULZ, J. P. (1960). Ecological studies on rain forest in northern Suriname. Verhandelingen der
Koninklijke nederlandse akademie van wetenschappen. Afdeeling natuurkunde (sectie 2) (53), 1-67.
SCHWAPPACH, A. (1895). Die Samenproduktion der Wichtigsten Waldholzarten in Preussen. Zeitschift
fur Forst- undJagdwesen 27, 14714.
SEEGER, M. (I 913). Die Samenproduktion der Waldbaume in Baden. Naturwissenschaftliche Zeitschrift
fur Forst- und Landeuirtschaft 12, 529-54.
SHAMSI, S. R. A. &WHITEHEAD, F. H. (1974). Comparative eco-physiology of Epilobium hirsutum L. and
Lythrum salicaria L. 11. Growth and development in relation to light. Journal of Ecdogy 62, 631-45.
SHANTZ, H. L. & PIEMEISEL, R. L. (1917). Fungus fairy rings in eastern Colorado and their effect on
vegetation. Journal of Agricultural Research IT, 191-245.
SHEIKH, K. H. & RUTTER, A. J. (1969). The responses of Molinia caerulea and Erica tetralix to soil
aeration and related factors. I. Root distribution in relation to soil porosity. Journal of Ecology 57,
7 I 3-26.
SHELDON, J. C. (1974). The behaviour of seeds in soil. 111. The influence of seed morphology and the
behaviour of seedlings on the establishment of plants from surface-lying seeds. Journal of Ecology
62,47-66.
SKELLAM, J. G. (1951). Random dispersal in theoretical populations. Biometrika 38, 196-218.
SMITH, F. L. & PRYOR, R. H. (1962). Effect of maximum temperature and age on flowering and seed
production in three bean varieties. Hilgardia 33, 669-88.
SNOW, D. W. (1965). A possible selective factor in the evolution of fruiting seasons in tropical forest.
Oikos 15, 274-81.
SNOW, D. W. (1968). Fruiting seasons and bird breeding seasons in the New World tropics. Journal of
Ecolcgy 56, 5P-6P.
SOUGNEZ, N. (1966). Rtactions floristiques d'une lande humide aux fumures mintrales. Oecologia
Plantarum I, 219-34.
SPRUGEL, D. G. (1976). Dynamic structure of wave-regenerated Abies balsamea forests in the northeastern
United States. Journal of Ecology 64, 889-911.
STEBBINS, G. L. (1951). Natural selection and the differentiation of angiosperm families. Evolution,
Lancaster, Pennsylvania 5, 299-323.
STEBBINS, G. L. (1970). Adaptive radiation of reproductive characteristics in angiosperms. I. Pollination
mechanisms. Annual Review of Ecology and Systematics I, 307-26.
STEBBINS, G. L. (1971). Adaptive radiation of reproductive characteristics of angiosperms. 11. Seeds and
seedlings. Amml Rm'ew of Ecology and Systematics 2, 237-60.

Maintenance of species-richness in plant communities '43
STEENIS, C. G. G. J. VAN (1956). Basic principles of rain-forest sociology. Proceedings of the Kandy
Symposium on Study of Tropical Vegetation, pp. 159-63. UNESCO, Paris.
STEWART, D. R. M. & STEWART, J. (1971). Comparative food preferences of five East African ungulates
at different seasons. In The Scientific Management of Animal and Plant Communities for Consemation
(ed. E. DutTey and A. S. Watt). Symposia of the British Ecologicat Society XI, 351-66.
STILES, F. G. (1975). Ecology, flowering phenology, and hummingbird pollination of some Costa =can
Heliconha species. Ecology 56, 285-301.
SUMMERHAYES, V. S. (1941). The effect of voles (Microtus agrestis) on vegetation. Journal of Ecology 29,
14-48.
TAGAWA, H. (1969). A preliminary investigation of seed fall in an evergreen broadleaf forest of Minamata
Special Research Area of IBP. Scientijk Reports, Kagoshima University 18, 27-41.
TAGAWA, H. (1971). Studies on the biological production of laurel-leaved forest. Japanese IBP-PT
Annunl Report pp. 39-60.
TAMM, C. 0. (1956). Further observations on the survival and flowering of some perennial herbs: I.
Oikos 7,273-92.
TAMM, C. 0. (1972~). Survival and flowering of some perennial herbs. 11. The behaviour of some
orchids on permanent plots. Oikos 23, 23-8.
TAMM, C. 0. (1g72b). Survival and flowering of perennial herbs. 111. The behaviour of Prim& om's
on permanent plots. Oikos 23, 159-66.
TANNER, E. V. J. (1977). Four montane forests of Jamaica: a quantitative characterization of the
floristics and the soils and a discussion of the interrelations. Journal of Ecology 65, (in the press).
TEVIS, L. (1958). Interrelations between the harvester ant Veromessorpergandei (Mayr) and some desert
ephemerals. Ecology 39, 695704.
THURSTON, J. M. (1951). Some experiments and field observations on the germination of wild oat
(Aoena fatua and A. luakiciana) seeds in soil and the emergence of seedlings. Annals of Applied
Biology 38, 812-32.
THURSTON, J. M. (1969). The effect of liming and fertilizers on the botanical composition of permanent
grassland, and on the yield of hay. In Ecological Aspects of the Mineral Nutrition of Plants (ed. I. H.
Rorison). Symposia of the British Ecological Society 9, 3-10.
TOUMEY, J. W. & KORSTIAN, C. F. (1937). Foundations of Silviculture upon an Ecological Basis, 2nd ed.
Wiley, New York.
TRABAUD, L. (1970). Quelques valeurs et observations sur la phyto-dynamique des surfaces incendibes
dans le Bas-Languedoc. Naturalia monrpeliensia, skie Botanique 21, 231-42.
TUKEY, L. D. (1952). Effect of night temperature on the growth of the fruit of the sour cherry. Botanical
Gazette 114, 155-65.
TUKEY, L. D. (1955). Some effects of night temperatures on the growth ofMcIntosh apples. I. Proceedings
of the American Societv - of - Horticultural Science 68, 32-43.
Tub~, L. D. (1958). Effects of controlled tempera&& foilowing bloom on berry development of the
Concord Grape (Vitis labrusca). Proceedings of the American Society of Horticultural Science 71,157-66.
VILLIERS, T. A. (1972). Environmental control of seed germination. In Seed Biology, vol. 2 (ed. T. T.
Kozlowski), pp. 220-81. Academic Press, New York.
WADE, L. K. & MCVEAN, D. N. (1969). Mt Wilhelm Studies. I. Department of Biogeography and
Geomorphology Publication (BG/I), i-wi, 1-225. Australian National University, Canberra.
WALTER, H. (1968). Die Vegetation der Erde in Gkophysiologkcher Betrachtung, vol. 2. Fischer, Jena.
WALTER, H. (1971). Ecology of Tropical and Subtropical Vegetation. Oliver & Boyd, Edinburgh.
WANG. C.-W. (1961). The Forests of China. Maria Moors Cabot Foundation (Cambridge, Massachusetts)
Publication (i5j, 1-313.
WARDLE, J. (1970). The ecology of Nothofagus solandri. 3. Regeneration. New ZealandJoumal of Botany
8, 571-608.
WARDLE, P. (1959). The regeneration of Fraxinus excelswr in woods with a field layer of Mercurialis
perennis. Journal of Ecology 47.483-97.
WATT, A. S. (1919). On the causes of failure of natural regeneration in British oakwoods. Journal of
Ecology 7, 173-203.
WATT. A. S. (1923). On the ecology of British beechwoods with special reference to their regeneration.
Journal of Ecology XI, 1-48.
WATT, A. S. (1926). Yew communitites of the South Downs. Jountal of Ecology 14, 282316.
WATT, A. S. (1934). The vegetation of the Chiltern Hills, with special reference to the beechwoods and
their sera1 relationships. Journal of Ecology 22, 23~70,
45-507.
WATT, A. S. (1947). Pattern and process in the plant community. Journal of Ecology 35, 1-22.
WATT, A. S. (1955). Bracken versus heather: a study in plant sociology. Journal of Ecology 43,490-506.
WATT, A. S. (1957). The effect of excluding rabbits from Grassland B (Mesobrometum) in Breckland.
Journal of Ecology 45, 86178.

I44
P. J. GRUBB
WATT,A. S. (1971). Factors controlling the floristic composition of some plant communities in Breckland.
In The Scientific Management of Animal and Plant Communities for Conservation (ed. E. Duffey and
A. S. Watt). Symposia of the British Ecological Society XI, 137-52.
WATT, A. S. (1974). Senescence and rejuvenation in ungrazed chalk grassland (Grassland B) in
Breckland: the significance of litter and of moles. Journal of Applied Ecology 11, I 157-71.
WATT, A. S. & FRASER, G. K. (1933). Tree roots and the field layer. Journal of Ecology 21, 404-14.
WEATHERELL, J. (1957). The use of nurse species in the afforestation of upland heaths. QwrterZy Journal
of Forestry 51, 298-304.
WEBB, L. J. (1958). Cyclones as an ecological factor in tropical lowland rain-forest, North Queensland.
Australian Journal of Botany 6, 220-8.
WEBB, L. J., TRACEY, J. G. & HAYDOCK, K. P. (1967). A factor toxic to seedlings of the same species
associated with living roots of the non-gregarious subtropical rain forest tree Grmillea robusta. Journal
of Applied Ecology 4, 13-25.
WEBB, L. J., TRACEY, J. G. & WILLIAMS, W. T. (1972). Regeneration and pattern in the subtropical rain
forest. Journal of Ecology 60, 675-95.
WEBB, L. J., TRACEY, J. G., WILLIAMS, W. T. & LANCE, G. N. (1970). Studies in the numerical analysis
of complex rain-forest communities. V. A comparison of the properties of floristic and physiognomicstructural
data. Journal of Ecology 58, 203-32.
WELBANK, P. J. (1963). A comparison of competitive effects of some common weed species. Annals of
Applied Biology 51, 107-25.
WENT, F. W. (1949). Ecology of desert plants. 11. The effect of rain and temperature on germination and
growth. Ecology 30, 1-13.
WENT, F. W. (1957). Environmental control of plant growth. Chronica Botanica (17), i-xvii, 1-343.
WESSON, G. & WAREING, P. F. (1969). The induction of light sensitivity in weed seeds by burial. Journal
of Exberimental Botany 20, 414-25.
WESTHOFF, V. (1971). The dynamic structure of plant communities in relation to the objectives of
conservation. In The ScientiJic Management of Animal and Plant Communities for Conservation (ed.
E. Duffey and A. S. Watt). Symposia of the British Ecological Society XI, 3-14.
WHITE, J. H. & FRENCH, N. (1968). Leatherjacket damage to grassland. Journal of the British Grassland
Society 23, 326-9.
WHITEHEAD, F. H. (1971). Comparative autecology as a guide to plant distribution. In T/ze Scientific
Management of Animal and Plant Communities for Conservation (ed. E. Duffey and A. S. Watt).
Symposia of the British Ecological Society XI, 16776.
WHITFORD, H. N. (1949). Distribution of woodland plants in relation to succession and clonal growth.
Ecology 30, 199-208.
WHITMORE, T. C. (1974). Change with time and the role of cyclones in tropical rain forest on Kolombangara,
Solomon Islands. Institute Paper, Commonwealth Forestry Institute, Oxford (46), 1-78.
WHITMORE, T. C. (1975). Tropical Rain Forests of the Far East. Clarendon Press, Oxford.
WHITTAKER, R. H. (1965). Dominance and diversity in land plant communities. Science 147, 25-60.
WHITTAKER, R. H. (1967). Gradient analysis of vegetation. Biological Rezkus 49, 207-64.
WHITTAKER, R. H. (1969). Evolution of diversity in plant communities. Diversity and Stability in
Ecological Systems. Brookhaven Symposia in Biology 22, 178-95.
WHITTAKER, R. H. (1972). Evolution and measurement of species diversity. Taxon 21, 213-51.
WHITTAKER, R. H. (1975). Communities and Ecosystems, 2nd. ed. Macmillan, New York.
WHITTAKER, R. H., LEVIN, S. A. &ROOT, R. B. (1973). Niche, habitat and ecotope. American Naturalist
107, 321-38.
WILLIAMS, J. T. (1969). Biological Flora of the British Isles: Chenopodium rubrum L. Journal of Ecology
57,831-41.
WILLIAMS, J. T. & HARPER, J. L. (1965). Seed polymorphism and germination. I. The influence of
nitrates and low temperatures on the germination of Chenopodium album. Weed Research 5,
141-50.
WILLIAMSON, G. B. (1975). Pattern and sera1 composition in an old-growth beech-maple forest.
Ecology 56, 727-3 I.
WILLIS, A. J. (1963). Braunton Burrows: the effects on the vegetation of the addition of mineral
nutrients to the dune soils. Journal of Ecology 51, 353-74.
WILSON, J. Y. (1959). Vegetative reproduction in the bluebell, Endymion nonscriptus (L.) Garcke.
Garcke. New Phytologist 58, 155-63.
WINKWORTH, R. E. (1967). The composition of several arid spinifex grasslands of central Australia in
relation to rainfall, soil water relations and nutrients. Australian Journal of Botany 15, 107-30.
WIT, C. T. DE (1960). On competition. Verslagen van landbouwkundige onderzoekingen, The Hague
(66.8), i-iv, 1-82.

Maintenance of species-richness in plant communities
WIT, C. T. DE (1961). Space relationships within populations of one or more species. In Mechanisms in
Biological Competith (ed. F. L. Milthorpe). Symposia of the Society of Experimental Biology 15,
314-29.
WUENSCHER, J. E. (1969). Niche specification and competition modeling. Journal of Theoretical Biology
25,436-43.
WUENSCHER, J .E. (1974). The ecological niche and vegetation dynamics. In Vegetation and Environment
(ed. B. R. Strain and W. D. Billings), Part 6 of Handbook of Vegetation Science, pp. 39-45. Junk,
The Hague.
YARRANTON, G. A. & MORRISON, R. G. (1974). Spatial dynamics of a primary succession: nucleation.
Journal of Ecology 62, 417-28.
I45