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

(Received7 September 1976)

CONTENTS
I. Introduction . . . 107
11. Mechanisms not involving the process of regeneration . 108
(a) Variation in life-form . . . . 108
(b) Phenological spread . . . 111
(c) Fluctuations in the environment . . I11
(d) Balancedmixturea . . 113
(e) Variation in competitive ability with physiological age . 114
111. I n d u c t i o n to the involvement of regeneration . . 116
IV. Definition of a plant’s niche . . . . . . I19
V. Patterns of regeneration in different plant communities . 119
VI. Examples of differentiation in the regeneration niche . . . . I21
(a) Production of viable seed . . . I21
(a) Dispersal . . 125
(c) Germination . . . . . . . 126
(d) Establishment of seedlings . . 128
(e) Further development of the immature plant . . 130
VII. Discussion . . I31
VIII. summary . . . . I34
IX. References . . . . 136

I. INTRODUCTION
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 explainingthe 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 (physico-
chemical 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 species-
richness 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 otherwiseindicated.

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 per-
sistence 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 dif-
ferences in potential than by simple competition from the dominant. If the latter is
 Maintenance of species-richness in plant communities

b,
109
100

- 10

al
$ 1
>
8
Yrn
0
a
-E
0.1
0.01

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.
II0 P. J. GRUBB

Fig. 3. A section of the central part of a model of a species-poor community with dependence-
relationships 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 demon-
strated by the epiphytes already mentioned, by the parasites and hemi-parasites and by
 Maintenance of species-richness in plant communities I11
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.

(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, I932). 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 semi-
natural 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, fluctua-
tions 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 yoto 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, sup-
pressing 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 species-
richness 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 replacesy, (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 (discontinuousline) 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).I n 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). I n 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 tentativelywith 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 B R E 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. 4 b 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 occasionswhen a near-
balance 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
(a)From Bomkamm (1961 a)
Species Decreasingly strong
affected competitors
S S A > V a T
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.

(b) From Caputa (1948) - results of 1944

Species affected Species decreasingly aggressive to test species
L M L H X F P C A D
A L M A X F P C H D
D L M = X A = F D P C H
P L D F A X M P H C
F L M=A P X F C H D
M L X M C H A P D F
X L D A X P F M = C H
C L M X A D F H P C
H 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 = T 7 Z ~ O b I Ihybridurn
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 characteri-
stic 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 Characters
Production of viable seed Time of formation
Flowering Size and shape
Pollination Orientation
Setting of seed Nature of soil surface
Dispersal of seed Litter present
Through space Other plants present
Through time Animals present
Germination Fungi, bacteria and viruses present
Establishment
Onward growth

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 impor-
tant 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 regenera-
tion 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. I n 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 Aubre-
ville (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 treat-
ment of diversity, also started from a forestry background; he emphasized the impor-
tance 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.
I n 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 differen-
tiation 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 escarp-
ment beechwoods on calcareous soils in the Chiltern Hills compared with 64 species in
10samples 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 escarp-
ment 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 illu-
strate 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 fluctua-
tions from the mean climatic conditions which favour the plant’s vegetative develop-
ment.
(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 m x i e s i i invades after
fire (Franklyn & Dyrness, 1969). I n 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.
I n shrub-dominated communities regeneration is sometimes chiefly by seed as in
the species-poor Callunetum of eastern England (Watt, 1947, 1955) and in semi-
deserts (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 regenera-
tion 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 I21
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.

VI. EXAMPLES OF DIFFERENTIATION I N 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 cultivatedin 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).

1000
r- (a) 3442
1

800 -
n
x
TI -
al
L
n
el
600 -
0,
c
V
3 -
0
v)

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..

0 ~ O . ~ . , .

..........
Acacia aneura

Acacia pruinocarpa
. .
0
. . O 0.
Acacia tetragonophylla 0 0 . 0 . O . 0

Acacia victoriae O ~ O O ~ O O
Cassia desolata 0 0 . 0 0.0 . 0

Cassia helrnsii 0 . 0 0 . ~ ~ .
Erernophila fraseri

oHakea lorea
. . 0 . .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 10years 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.
I n 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
124 P. J. GRUBB

46 47 4% 49 50 51 52 53 54 55 56 57 50 59 60 61 62 6 3
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 fluctua-
tions 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 day-
time 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 dispersalin time. It is well establishedthat 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 seedlingsof ‘Helianthemum brewmi’
(Tuberariaguttata (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-tolerancesand reproduc-
tive ‘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 advan-
tage 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 germina-
tion as such in the field - nearly all the apparently relevant reports concernthe establish-
ment 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.
Differencesin 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

Sonchus oleraceus

100 r

Galium aparine

F u
100

50
0. Capsella bursa-pastoris
100 r
o
50

100
t
= L Myosotis arvensis

50o E Odontites rubra

100

50o E

100
L Sagina procumbens

5 0o E Solanum nigrurn
' N ' D 'J ' F'M'A'M'J '
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 surface-
types 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 establish-
ment, 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
L
I
I
!600
n
I
I
I
I
f I
v I
0 400 I
-
.-
C

-0
I

a8
v)

200

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 Weinmanniaracemosa 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 mycor-
rhiza 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 B R E 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 differencesare 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, 1968a). 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 relation-
ships are often dependent on the weather at a particular time. Thus in most years
a carpet of the herb Mercurialisperenniswill 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 ( W a d e , 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 pteri-
dophytes, 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 senescenceand death of individualsmore
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 commu-
nity 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, 1968b, 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 regenera-
tion 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 divergencemay concernany 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 phyto-
sociology, 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. I t is this replacement stage which is all-important to the argument
presented.
3. Several mechanisms not involving regeneration also contribute to the main-
tenance 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 physio-
logical 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 differentiationin the regenera-
tion 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 a m 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
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