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Perspectives
in Plant Ecology,
Evolution and
Systematics
Vol. 1/1, pp. 78–91
© Gustav Fischer Verlag, 1998
The phenology of growth and
reproduction in plants
Michael Fenner
Biodiversity & Ecology Division, School of Biological Sciences, University of Southampton, Bassett Crescent East, Hampshire SO16 7PX, UK; email: [email protected]
Abstract
The study of phenological aspects of plants involves the observation, recording and
interpretation of the timing of their life history events. This review considers the phenology of leafing, flowering and fruit production in a range of species and communities. The selective forces (both abiotic and biotic) that influence the timing of these
events are discussed. Within the limits imposed by phylogenetic constraints, the phenological patterns (timing, frequency, duration, degree of synchrony, etc.) of each
phase are probably the result of a compromise between a variety of selective pressures, such as seasonal climatic changes, resource availability, and the presence of
pollinators, predators and seed dispersers. Many studies on flowering times stress
the role of interactions between plant species which share pollinators or predators.
The timing of fruiting plays a key role in controlling the abundance and variety of obligate frugivores in many tropical communities. The importance of long-term recording
is stressed, particularly in species which fruit irregularly. An understanding of the phenology of plants is crucial to the understanding of community function and diversity.
Key words: Leafing, flowering, fruiting, pollination, seed predation, synchrony
Lo! Sweeten’d with the summer light,
The full-juiced apple, waxing over-mellow,
Drops in a silent autumn night.
All its allotted length of days,
The flower ripens in its place,
Ripens and fades, and falls, and hath no toil,
Fast-rooted in the fruitful soil.
– Tennyson, The Lotus Eaters
Introduction
One of the most familiar of all natural phenomena is the cycle of events associated
with the passage of the seasons. This is
especially so in temperate and polar regions
where annual changes in temperature are
great and are accompanied by corresponding
cycles in the growth and reproduction of the
flora. In tropical regions, seasons are often
marked by differences in rainfall, with life-his-
tory events occurring in response to water
availability.
Phenology (from the Greek phainein, to
show or appear) is the study of the timing of
these life-history events. In plants, bud-burst,
leaf-expansion, abscission, flowering, fertilisation, seedset, fruiting, seed dispersal and
germination all take place in due season. For
the most part, these events are too familiar to
attract any special attention. Only when the
expected pattern is broken, for example by
out-of-season flowering or the loss of fruit
due to a late frost, is our attention drawn to
the importance of timing of growth and reproduction in the life of plants.
Phenological studies are as important to
our understanding of species interactions and
community function as the spatial aspects are.
In Europe there is a long tradition of phenological recording, which goes back to the last
century, with an international network of phe-
Phenology of growth and reproduction in plants 79
nological gardens. The information gathered
has mainly been used as a kind of bioindicator
of climatic patterns (Schnelle 1965–1986,
1977). However, data about recurring life-history events are still relatively scarce for most
communities. Some of the reasons for this are
pointed out by Lechowicz & Koike (1995).
Firstly, the data are hard won. They can only
be accumulated by many years of repetitive
recording at the same site. Phenological studies need long-term planning and funding, and
so do not lend themselves to the short-term
requirements of thesis projects, grant cycles,
and the priorities of awarding bodies. Nevertheless some excellent long-term studies have
been published (e.g. Norton & Kelly 1988;
Allen & Platt 1990) and are a tribute to the persistence of their authors.
The phenology of plant communities can
be studied by dealing with particular life-history stages separately, such as leafing, flowering, fruiting, seed dispersal and germination. Each of these events occurs in its own
calendar slot, but there is clearly some interdependence between them. Fruiting must
wait upon flowering; seed dispersal cannot
preceed fruiting. Each phenomenon can be
studied at different levels of organisation. For
example, we can study the phenology of flowering in a whole plant community, or in a guild
of species sharing a pollinator, or in a population of a particular species, or in the flowers
on a single plant. Even an individual flower
undergoes a sequence of events (bud burst,
stigma ripening, pollen shedding, fertilization,
fruit swelling, etc.) whose phenology differs
between species and is presumed to be the
result of natural selection. At each level, the
constraints and selective forces which influence timing are different. This approach to
examining phenological information at successively finer levels of organisation is well
exemplified in the review of flowering patterns by Primack (1985).
For individual species it is important to distinguish between the physiological and ecological/evolutionary answers to the question of
why leafing, flowering or fruiting occurs at a
particular time. The immediate cause of a phenological event is the organism’s detection of
the environmental cues which trigger the appropriate response, e.g. a flowering response
to short or long days (Bernier et al. 1981).
Physiological responses are in principle easy
to explore experimentally, though with so
many potential cues operating simultaneously
in nature, it may not be easy to identify the relevant ones. The long-term cause of the timing
of a life-history event is the selection pressure
which has resulted in the evolution of the
plant’s idiosyncratic phenology. These pressures may range from abiotic constraints (e.g.,
seasonally unfavourable temperatures, erratic
rainfall), to biotic pressures such as seasonal
presence of predators, pollinators and dispersers. Many phenological studies are basically concerned with answering the question
‘Why now, rather than earlier or later?’ The
timing of a particular life-history event may be
the result of selection for exploiting a favourable slot sandwiched between two more
hazardous periods.
Most life-history events occur over a
period of time, and their timing can be described and quantified in terms of a number
of parameters (Newstrom et al. 1994). These
are (1) the frequency of occurrence, which is
often annual; (2) the time of occurrence,
which includes the starting date of the earliest
individuals and the date of peak activity; (3)
the duration of the event; (4) the magnitude
(both the mean and variability); and (5) the
degree of synchrony both within and between
species. In general, where the climate is
highly seasonal, as in temperate regions and
in the dry tropics, the phenology of whole
communities tends to follow a broadly similar
pattern from year to year, though modifications occur due to climatic differences between years. Leaf flushing tends to be relatively constant from year to year, but reproduction can be erratic, especially in harsh climates (Allen & Platt 1990). In the wet tropics
where annual seasons are less marked, a
great variety of phenological patterns are
seen: in different species, flowering may be
continual, sub-annual, annual or supra-annual, and may occur regularly or irregularly
(Newstrom et al. 1994). The great variety of
patterns encountered in leafing, flowering
and fruiting in any given habitat may be a reflection of diverse biotic and abiotic selective
pressures operating in all communities.
This review examines some of the interesting questions which arise in relation to the
phenology of plants, and attempts to summarize some of the answers which have been
put forward. The main questions dealt with
here are:
1. How and why do plants differ from each
other in the timing of their life history
events?
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M. Fenner
2. Why is the same stage apparently ‘staggered’ between some sympatric species?
3. Why do some stages occur on an annual
cycle while others do not?
4. What are the constraints on the timing or
frequency of a particular phase?
5. How does the phenology of the plants affect the primary consumers?
6. How might global climatic change affect
the phenology of plants and hence the
functioning of whole communities?
An excellent introduction to the broad topic
of phenological patterns in plants is provided
by Rathcke & Lacey (1985). For the flowering
phenology of tropical forests, Newstrom et al.
(1994) have successfully reduced the great
variety of patterns found to a small number of
identifiable types. Also in tropical forests, Van
Schaik et al. (1993) have synthesized a
range of data on phenological adaptation to
abiotic conditions, and discuss the community effects of phenological events. This review deals with the three major phenophases
in the life-cycle of plants (leafing, flowering
and fruiting) and attempts to identify the selective forces which may be responsible for
the patterns encountered. However, the possible influence of selective forces in determining phenological patterns must be interpreted
in the light of the phylogenetic inheritance of
the species. As with all other genetically controlled characteristics, the timing of life history
events may be largely influenced by evolutionary constraints, with selection merely
modifying a predetermined underlying pattern. The issue of phylogenetic inertia is discussed in the context of fruit characters in
Lee et al. (1991).
Temporal patterns in leafing
Community patterns
The timing and duration of bud burst, leaf expansion, maturity, senescence and fall of individual leaves are all crucial to the fitness of
plants. Rather few long-term studies have
been made of the life histories of leaves. In
aseasonal climates, such as parts of the wet
tropics, leafing is continuous on a community
scale, though a wide range of behaviour is
found between species. Lowman (1992)
monitored individual leaves of five species of
rain forest trees in Australia for up to twelve
years. He found that flushing behaviour
ranged from synchronous to continuous in
different species and that there were large
differences in longevity. In seasonal climates,
the production of new leaves tends to be concentrated for most species into a short period
of the year. This is the case both in evergreen
communities (such as the boreal conifer forest) and in deciduous forests (both temperate
and tropical). Usually leafing is linked with
some climatic feature such as rainfall (Lieberman & Lieberman 1984; Bullock & Solís-Magallanes 1990), irradiance (Wright & Van
Schaik 1994), temperature (Brooke et al.
1996), or photoperiod (Loubry 1994). Where
water is not a limiting factor, irradiance may
play a predominant role. In a major study of
eight disparate tropical forests, Wright & Van
Schaik (1994) show that leaf (and flower) production coincides with seasonal peaks of irradiance. In three cases peak irradiance occurred in the drier season. Leaf production
can be artificially induced in some cases by
irrigation during the dry season (Wright 1991;
Tissue & Wright 1995). However, in many
tropical deciduous forests, flushing takes
place during the dry season, well before the
arrival of the rains. For example in the seasonally dry forests of southern India leaf
flushing peaks in the hottest, driest month of
the year (May), greening the canopy well in
advance of the onset of the monsoon (Singh
& Singh 1992; Murali & Sukumar 1993). Dry
season leafing is also reported by Frankie et
al. (1974) for an evergreen forest in the lowlands of Costa Rica. The production of leaves
before the arrival of the rain is achieved by
drawing on internal reserves of water which
buffer the trees against the impact of seasonal drought (Borchert 1994).
Al-Mufti et al. (1977) provide one of the
few detailed studies of shoot phenology in
herbaceous communities. They show that in
productive, less disturbed, temperate communities, the biomass peaks in mid-summer.
In low-fertility sites, plants tend to be evergreen, with some species showing no detectable seasonal peak in shoot expansion.
The phenology of growth in many temperate
bulbous plants (and grasses with large cells
and high DNA content) appears to be controlled by their ability to grow at low temperatures in early spring by expanding cells which
have been pre-formed in the preceding summer. This contrasts with other herbaceous
plants which have small cells and genomes,
and delayed (summer) growth because they
Phenology of growth and reproduction in plants 81
need higher temperatures for cell division
(Grime & Mowforth 1982). The link between
nuclear DNA and rate of shoot expansion in
spring has been shown in a limestone grassland community by Grime et al. (1985).
Herbivory as a selective force in
leaf flushing
A major selective force in determining the timing of leafing may be the effect of herbivory.
Young leaves are especially vulnerable to
attack by insects (Lieberman & Lieberman
1984; Lowman 1992), with the majority of lifetime damage being suffered during the first
month (Aide 1993). Highest damage may
occur on early-expanding rather than on juvenile leaves, at least in European shrubs (R.V.
Jackson, J. Kollmann & P.J. Grubb, unpubl.
data). A number of life history traits seem to
have resulted from selection due to herbivory.
One is the production of new leaves at a
period when the herbivores (mainly insects)
are at their least abundant. This is the supposed advantage of dry season flushing. Observations by Murali & Sukumar (1993) show
that late flushing individual trees in the Indian
monsoon forest suffered significantly higher
damage from insects compared with those
that flushed earlier because the late-flushing
trees were damaged by the herbivorous insects which emerged with the rains.
The temporal escape from herbivory by
means of flushing in the dry season was investigated experimentally by Aide (1992)
using populations of the understorey shrub
Hybanthus prunifolius (Violaceae) in Panama. Individuals of this species respond to dry
season rain by producing leaves. Some individuals were experimentally prevented from
flushing until the wet season. A comparison of
cohorts of dry-season and wet-season leaves
showed that wet season leaves suffered
three times as much herbivore damage.
In temperate communities, individuals
which flush either earlier or later than the
mean of the population can find themselves
at risk of herbivory. For example, in Picea
glauca damage by the bud moth Zeiraphera
canadensis has been shown to be greatest
amongst early leafing individuals (Quiring
1994). In contrast, late flushing individuals of
Quercus geminata were found to be most
susceptible to a leaf miner moth, Stilbosis
quadricustatella (Mopper & Simberloff 1995).
Clearly, selection will favour the survival of
the individuals which conform to the least
dangerous calendar slot.
A second possible strategy for reducing
herbivory is the synchronous production of
leaves throughout a population, thereby satiating the herbivores. This was investigated in
the Central American sub-canopy tree Gustavia superba (Lecythidaceae) by Aide (1991).
Most individuals produce their leaves
synchronously with the rest of the population.
Some individuals, however, are found to be
out of synchrony with their conspecifics, and
suffered significantly more herbivore damage.
Another phenological feature seen in
many tropical evergreen trees is the delay in
greening of the leaves after expansion. A
study by Kursar & Coley (1992) using data
from 175 species on Barro Colorado Island,
Panama, indicates that delayed greening is
most common in shade species and rare in
light-demanding gap species. This was interpreted as a possible anti-herbivore defence
mechanism. By delaying the input of chlorophyll, nitrogen and other valuable resources
until after the leaves have acquired their
structural defences, the plants limit their
losses to herbivory. The benefit presumably
outweighs the disadvantage of the temporary
absence of photosynthetic activity, and the
balance of advantage is reckoned to be especially favourable in shade leaves.
Therefore, the timing of leafing seems to
be a compromise between exploiting the
most favourable environmental conditions
and the avoidance of herbivory. In many
cases, herbivory may simply be avoided by
the satiation effect of synchronous flushing.
Leaf fall
For deciduous species, the seasonal loss of
leaves brings about a period of dormancy
during which photosynthesis is generally suspended. The cost of shedding the leaves is
usually mitigated by the reabsorption of minerals preceding abscission (Delarco et al.
1991; Chidumayo 1994). The timing of leaf
fall is often linked with some change in environmental conditions such as water availability (Williams et al. 1997), temperature (Rusch
1993) or photoperiod (Loubry 1994). For example, in an Australian tropical savanna,
Williams et al. (1997) recorded a wide degree
of deciduousness, but in each species leaf
fall was coincident with the attainment of seasonal minima in leaf water potential. In con-
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M. Fenner
trast, Loubry (1994) found that individual
trees in a tropical rain forest had their own
periodicity with respect to leaf fall, and that it
was not linked with a dry season. Leaf fall in
this case was more closely correlated with
variations in daylength, even though these
variations are small at 5° latitude. Although
leaf fall is broadly linked to external conditions, a number of studies indicate that there
is also an endogenous component to its timing (Porras 1991; Loubry 1994; Williams et al.
1997).
Flowering phenology
Community patterns
The timing of flowering is one of the most
widely investigated aspects of the phenology
of plant life-cycles, and has been studied on
every scale, from the level of the community
(Murali & Sukumar 1994) to that of the individual flower (Herrera 1995a). In most plant
communities, although at least some species
will be in flower throughout the growing season, there is a tendency for peaks of flowering to occur. In wet tropical forests flower production may coincide with peaks of irradiance
(Wright & Van Schaik 1994). In the seasonally dry tropical forests flowering is often concentrated in the transition from the late dry to
the early wet season (Murali & Sukumar
1994). A particularly marked example of the
concentration of community-wide flowering is
found in the ground flora of temperate deciduous woodlands, where a pronounced peak
of flowering occcurs in spring before the tree
canopy closes (Heinrich 1976). Flower production and maintenance requires the expenditure of energy to form non-photosynthetic
tissue and nectar, the cost of which is considerable (Ashman & Schoen 1997). In many
cases its timing may be largely determined by
seasonal changes in resource availability. In
some studies, climatic factors (such as some
measure of cumulative heat sum) are the
best predictors of flowering (Diekmann 1996;
White 1995). Abiotic control of flowering time
may be strongest in harsh environments with
a short growing season. For example, in
alpine plant communities there may be a high
level of selection in favour of early flowering
in most species because of the restricted
time available subsequently for seed maturation (Totland 1993). Smith-Ramírez & Armesto (1994) concluded from an investiga-
tion of a temperate rain forest in Chile that
flowering (and fruiting) was largely constrained by seasonal variables.
Species patterns
The pattern of flowering of individual species
varies widely. In some species it is staggered
over a long period; in others there is a much
more pronounced peak with relatively few individuals occurring in the early and late parts
of the flowering period. The various types are
well exemplified in a study of eight sympatric
species in the Myrtaceae family in Central
Brazil by Proença & Gibbs (1994). These
ranged from mass-flowering (synchronous
over a short period), pulsed flowering (repeated flushes), to steady-state flowering (a
few per day over a long period). Each pattern
may be a response to a different set of selective pressures. A strong peak of flowering
suggests a disadvantage to out-of-season individuals, possibly due to pollination reduction in an out-crossing species. In the massflowering Andean shrub Befaria resinosa
Melampy (1987) showed that the proportion
of flowers that set fruit was positively correlated with flower abundance. Augspurger
(1981) induced individuals of the shrub Hybanthus prunifolius to flower out of synchrony
with the general population, and found that
these plants had a lower seed set and greater
seed loss to predation than the general population. In a situation in which out-of-season
individuals are at a disadvantage, there
would be a strong stabilizing selective pressure in favour of synchrony.
Where flowering periods are more staggered, other selective pressures may be operating. Variation in weather from year to year
or changes in pollinator or seed predator
abundance may result in inconsistent selective pressures on flowering times, favouring
early, average or late individuals in different
years. In the tropical shrub Erythroxylum havanense selection pressure on flowering time
varies in direction from year to year (Dominguez & Dirzo 1995). Brody (1997) also points
out that the net effect of pollinators and seed
predators varies both in time and space.
Even in any one year the advantage of an individual having a particular flowering time in
relation to the general population may be
finely balanced. Zimmerman (1988) for example notes that late-flowering plants of
Polemonium foliosissimum were more likely
Phenology of growth and reproduction in plants 83
to outcross than the general population. The
potential benefit of this may be counterbalanced by the possible disadvantages of late
blooming (less time for seed ripening, etc.).
Rathcke & Lacey (1985) point out that at least
some degree of asynchronous flowering in a
population would have the benefit of promoting outcrossing by forcing pollinators to move
between individuals. The highest levels of
outcrossing of a mass-flowering species probably occurs at the beginning and end of the
blooming season (Carpenter 1976). Asynchrony within individuals would have the
same effect (Rathcke & Lacey 1985).
If selection has long-term evolutionary effects, flowering times would have to be under
genetic control. The fact that differences in
flowering time between individuals in natural
populations are often maintained from year to
year (e.g. in Polemonium foliosissimum, Zimmerman & Gross 1984) suggests genetic
control. Various studies show that these differences are maintained in cultivation, for example, in Rumex crispus (Akeroyd & Briggs
1983), Solidago canadensis (Pors & Werner
1989) and Centaurea species (Lack 1982).
Widén (1991) went one stage further by
showing that rank order of flowering in individuals of the perennial herb Senecio integrifolius was significantly correlated with that of
their progeny. Waser (1983) cites a number
of examples of the genetic control of flowering time, and even suggests it to be a relatively flexible character.
Environmental cues for flowering
The immediate cause of flowering is the development of flowering initials in the appropriate meristematic tissues. In some cases flowering may simply result from the plant having
reached a critical size or developmental
stage, though this usually depends on a
cumulative heat-sum, such as degree-days
above a threshold (Diekmann 1996). In other
cases, flowering may be a physiological response to a very specific environmental cue.
Examples of such cues are short or long
days, warm or cold temperatures, or an
episode of rain or drought (Bernier et al.
1981). A shared response in a population to a
specific cue has the advantage of resulting in
synchronous flowering. In temperate regions
where daylength varies markedly with the
seasons, a photoperiodic response may be a
major determinant of flowering time for indi-
vidual species, though rather few records
have been made for wild plants. Even in the
tropics, a response to changes in daylength
are not unknown. For example, Njoku (1958)
reports that daylength variations of 15 minutes (as at Ibadan, 7°26′N), is sufficient to initiate flowering in many Nigerian herbs and
shrubs. A bout of cool temperature in tropical
rainforest can induce flowering in Dipterocarpaceae in Malaysia (Ashton et al. 1988)
and in a range of trees in Gabon (Tutin & Fernandez 1993). In temperate climates, warm
temperatures often act as flowering triggers,
especially in mast seeding trees (Allen & Platt
1990). Rain triggers flowering in the shrub
Erythroxylum havanense in Mexico (Dominguez & Dirzo 1995), and in the shrub Hybanthus prunifolius in Panama (Augspurger
1981). Experiments with desert ephemerals
in Namaqualand show that drought can bring
forward the flowering date in late sown
species (Steyn et al. 1996).
Competition for pollinators and
interference between species
The extent to which flowering times of sympatric species are influenced by competition
for pollinators has been much debated over
the years. It is hypothesized that competition
could be reduced by avoiding overlap in flowering times. This might be expected to result
in character displacement between coexisting species sharing the same pollinators. A
number of studies indicate that inter-specific
exploitative competition for pollinators does
occur (see examples cited in Rathcke 1983).
Another form of competition between plants
sharing a pollinator is the interference which
occurs when pollen from one species is deposited on the stigma of another. Reduced
seed set in the field as a result of heterospecific pollen transfer by shared pollinators
is well established in a number of cases
(Galen & Gregory 1989; Waser 1978a,b). Its
existence would provide a selection pressure
for the separation of the flowering times of
two sympatric species. There is some evidence for this. Carpenter (1976) describes
the case of two trees in Hawaii (Metrosideros
collina and Sophora chrysophylla) which
share a pollinator (honeycreepers). The two
species grow together at some elevations
and separately at others. Where they are
sympatric their flowering times are sequential; where they grow separately their flower-
84
M. Fenner
ing periods overlap. This is at least circumstantial evidence of local character displacement. Another intriguing case in which a
coexisting species pair shares a pollinator is
reported by Waser (1983). Ipomopsis aggregata and Penstemon barbatus grow together
on isolated mountains in south-west USA.
They are both pollinated by hummingbirds
and always flower sequentially. The hypothesis that their separate flowering times may be
due to character displacement is supported
by Waser’s discovery that the order of flowering ‘flip-flops’ from place to place. This variation in the sequence of flowering may be due
to the genetic characteristics of the founding
populations, but the consistency of the divergence in flowering time strongly suggests
local character displacement.
Another interaction between plants which
may provide a selection pressure affecting
flowering times is the advantage conferred on
one species by the presence of another
species in flower at the same time. The joint
floral display may result in increased visitation rates, leading to enhanced seed set for
one or both species. There is some evidence
that this may occur (Thompson 1978, 1981;
1982; Schemske 1981), but it is difficult to
standardize all other factors that affect seed
set. Facilitation, if effective, would provide a
selective force to converge flowering times
between species. An interesting form of this
‘facilitation’ is the benefit that early flowering
plants confer on those flowering later in the
season, by supporting the initial pollinators
(which survive to pollinate the later species).
This ‘sequential mutualism’ was nicely
demonstrated by Waser & Real (1979) in Delphinium nelsonii and Ipomopsis aggregata.
The complexity of these interactions is indicated by the fact that these two species were
also shown to compete for pollination.
Many studies in which the flowering times
of species within communities are recorded
show that there is often a temporal sequence
of flowering, with each species peaking in
turn. When presented graphically, with the
species placed in order of mean flowering
date, the sequence often appears to be nonrandom (that is, more evenly spaced and with
less overlap than would be expected in a random arrangement). Stiles (1977) gives a
much-quoted example of a guild of hummingbird-pollinated plants in a Costa Rican rain
forest which show an orderly sequence of
flowering peaks. Sympatric Dipterocarp
species also appear to have a staggered sequence (Ashton et al. 1988), as do meadow
plant communities in the Rocky Mountains
(Pleasants 1980). However, there are difficult
statistical problems involved in testing the
significance of these sequences. A common
approach is to compare the data with a random sequence. When this is done, few if any
examples can be distinguihed from a random
sequence statistically. This was the case, for
example, with the analysis of Stiles’s data by
Poole & Rathcke (1979), though this is robustly challenged by Stiles (1979). The tests
applied in these cases may not always be appropriate. Cole (1981) and Gleeson (1981)
modified the test and obtained different results. Useful accounts of the technicalities of
applying tests to detect orderly sequences in
flowering are given by Gleeson (1981), Estabrook et al. (1982) and Pleasants (1990).
Rathcke (1984) also did a random model test
on the flowering phenologies of plants from a
swamp in Rhode Island, but again found that
an apparently ‘promising’ sequence could not
be distinguished from random.
The present position with regard to character displacement due to competition for pollinators is that it is unproven, at least for long
sequences, but that some cases certainly
suggest a tendency towards it. It is probably
rare in any case for a large group of sympatric
plants to share exactly the same pollinators,
and since so many other forces influence
flowering times, it would probably be difficult
to identify any tendency which did exist.
Cases involving pairs of species (Carpenter
1976; Waser 1983) seem quite well established. The phenomenon would be most convincing if shown in a guild of related plants.
However, it should be borne in mind that a
group of sequentially pollinated species may
be the consequence of what Janzen calls
‘ecological fitting’ (Janzen 1985), resulting
from the arrival of widespread species whose
local survival is due to their ‘fitting in’ to the existing community. They were fortuitously preadapted, therefore, character displacement
due to competition for pollinators is unnecessary to account for their flowering time. It is
possible that many, if not most, pollination
guilds arise in this way.
Predispersal seed predation
Another important potential biotic influence
on flowering time is pre-dispersal seed pre-
Phenology of growth and reproduction in plants 85
dation. It can provide a selective pressure if it
is concentrated at a particular time within the
flowering period. A concentration of flowerhead or seed predation in early flowering individuals has been reported for Polemonium
foliosissimum (Zimmerman 1980; Brody
1997), Ipomopsis aggregata (Brody 1997), Silene vulgaris (Pettersson 1991), and Actaea
spicata (Eriksson 1995). In some cases early
and late season individuals suffer most damage. Fenner (1985) found that in a population
of Centaurea nigra, early and late capitula
were much more prone to seed predation
than those which flowered in mid-season.
This may have been due simply to a saturation effect at the peak of abundance, but the
effect would be to stabilize flowering times
around the mid-season date. In Baptisia australis Evans et al. (1989) recorded greater
flower damage early and late in the season,
giving a narrow window in time for flowering
to occur. Significantly, however, the timing of
this window shifts from year to year, probably
selecting for the maintenance of a range of
flowering times within the population. The opposite pattern has been recorded in Bartsia
alpina (Molau et al. 1989) and Erigeron glaucus (English-Loeb & Karban 1992), those
early and late flowers suffer less damage
from predators. This would favour a prolonged period of blooming. In addition to selection for flowering time, predation may impose other selective pressures. In Bartsia
alpina (Molau et al. 1989) and Tripleurospermum inodorum (Fenner 1985) the larger inflorescences have been shown to be preferentially attacked.
Ideally, predation and pollination data
should be combined in the same study (as in
Pettersson 1991; English-Loeb & Karban
1992; Brody 1997), so that the net effect of
these two forces can be assessed. Zimmerman (1980) gives an interesting example of a
trade-off between pollination and predation in
Polemonium foliosissimum in which the predators (fly larvae) preferentially attack those
plants which receive highest numbers of pollination visits. The balance of advantage to the
plant shifts during the season. Another complicating factor which needs to be considered
in all these studies is the effect of the presence of other plant species which share the
same seed predator. In Brody’s (1997) study
of two species which share a common
dipteran seed predator, Ipomopsis aggregata
suffered much more damage in sites where it
occurred alone than when it was accompanied by Polemonium foliosissimum. The complexities of the interactions between plants
sharing common pollinators and common
predators, combined with the effects of annual variations in climate on each of these organisms separately, make it particularly difficult to assess long-term net selective pressures on flowering time.
Inherent constraints on flowering
Each life-history stage of a plant is to some
extent dependent upon or constrained by the
preceeding and succeeding stages. For most
species, the time of flowering may be constrained by the timing of other phenophases
such as growth, seed dispersal or seed germination (Johnson 1993). An important constraint occurs at the end of the season when
late flowering individuals may not have
enough time for fruit maturation (Helenurm &
Barrett 1987; Rathcke 1988; Kudo 1993).
Dieringer (1991) showed that late flowers of
Agalinis strictifolia, a hemiparasitic grassland
annual herb, produced fewer fruits than early
or middle-flowering individuals. Seed size
was found to decline in late-flowering plants
of Ranunculus adoneus (Galen & Stanton
1991). Primack (1985) neatly demonstrated
the apparent constraint on flowering time imposed by the need to allow a sufficient period
for fruit to ripen. He found a significant negative correlation between flowering date and
volume of fruit amongst 115 insect-pollinated
species in the British flora. That is, species
with larger fruit flowered earlier. Since larger
fruit are assumed to require a longer period to
mature, the implication of the data is that fruit
size imposes at least some influence on flowering time.
An important constraint on the flowering
phenology of a species may be its taxonomic
affinities. Related plants share similar inherent design constraints which would limit their
potential evolutionary response to selection.
Analyses of various floras confirm that this
phylogenetic effect on flowering time is
strong. Its influence has been demonstrated
in the floras of South West Australia (Bell &
Stephens 1984), North America and Japan
(Kochmer & Handel 1986) and the Cape
(Johnson 1993). Coexisting congenerics
sometimes show rather similar phenologies,
as for example, Commiphora species in East
African dry forest vegetation (Fenner 1982).
86
M. Fenner
Clearly, the results of all studies in which the
influence of various putative selective pressures is tested, should be interpreted in the
light of these phylogenetic limitations.
Fruiting phenology
Selective pressures on timing
As with flowering, the phenology of fruiting is
governed by its own set of constraints. Jordano (1992) has compiled a summary of fruiting phenology in a wide range of ecosystems,
which indicated that fruiting peaks generally
occur during periods of low photosynthetic
activity or after periods of high rates of reserve accumulation. There is a broad divide
between temperate and tropical fruiting patterns. In temperate regions fruiting has a unimodal peak in late summer or autumn, with a
mean duration of less than 1.5 months. In
tropical communities there are usually some
species in fruit at any given time of the year,
and individual species tend to have longer
fruiting periods, with a mean of more than 4.0
months (Jordano 1992). These differences
probably reflect the nature of the contraints
on fruit timing in the two regions. The highly
seasonal occurence of favourable temperatures and irradiance in the middle latitudes
confines the necessary resource build-up for
fruit production and ripening to a restricted
period. In most cases it has to be squeezed in
between flowering time and the onset of winter. In a temperate Australian community,
French (1992) suggests that fruit production
is largely controlled by the accumulation of
enough photosynthate, which can only occur
towards the end of the growing season. In individual cases, flowering time may further restrict the fruiting calendar slot. Late-flowering
Rhododendron aureum in northern Japan
fails to set fruits because of the onset of
autumn frost and snow, preventing fruit ripening (Kudo 1993). Physical limitations on fruiting time are probably less acute in the tropics,
though seasonal rainfall is probably the single
most important abiotic factor controlling resource availability there (Borchert 1994). Timing of fruiting may also be under some selective pressure to disperse seeds at the start of
the rainy season to facilitate germination
(Garwood 1983). However, in at least some
tropical rain forests fruiting has virtually no
seasonal pattern when viewed from the community level (Putz 1979; Hilty 1980).
Since seed dissemination is the major
function of the fruit, we might expect its phenology to be influenced by selective pressures which would favour successful dispersal. A number of studies have sought to test
the hypothesis that wind-dispersed species
release their disseminules (whether fruits or
individual seeds) at the most appropriate
season. There is a general tendency, at least
in the case of seasonally dry tropical forests,
for wind dispersed species to shed their
seeds during the dry season (Ibarra-Manríquez et al. 1991; De Lampe et al. 1992;
Morellato & Leitao 1996). Dry season dispersal may be more effective as it coincides with
leaflessness. The timing of shedding of these
wind-dispersed fruits contrasts with that of
fleshy or dry heavy fruits which are produced
throughout the year (De Lampe et al. 1992).
For fleshy fruits which attract dispersal
agents, the timing of ripening would be expected to coincide with the presence of the
dispersers. In the tropics there are numerous
specialised frugivores which eat fruit throughout the year. The continuous availability of
the fruit is a necessary part of the mutualism
between plant and disseminator. In contrast,
in temperate dispersers (mainly birds), frugivory is highly seasonal. In many temperate
regions the abundance of frugivorous birds
varies seasonally, reaching a peak in autumn
during migration to winter quarters. A number
of studies record the concentration of fruiting
in bird-dispersed species at this time: in
forests of eastern USA (Stiles 1980), in Illinois (Thompson & Willson 1979) and in
northern and southern Europe (Snow 1971;
Herrera 1984). Snow (1971) points out that
fruits of bird-dispersed species ripen later at
increasingly southerly latitudes in Europe, in
conformity with the southerly migration of frugivorous birds in autumn. The phenology of
fleshy fruit production in the Mediterranean
closely matches that of the seasonal abundance of frugivorous avian dispersers (Herrera 1995b).
Mast fruiting
The production of fruits by an individual plant
is often irregular. For many species, fruit
crops appear only once every few years in an
unpredictable pattern, with several barren
seasons in between. There is a tendency for
all the plants in a population to produce fruit
in the same year. This phenomenon, called
Phenology of growth and reproduction in plants 87
‘masting’, is seen in a range of long-lived
species, and is characteristic of many temperate broadleaved trees (Hilton & Packham
1986; Allen & Platt 1990) and conifers (Norton & Kelly 1988). Irregular supra-annual
fruiting also occurs in the tropical Dipterocarpaceae, montane grasses and perennial
herbs (Primack 1985). Mast fruiting is linked
to the formation of flowering initials in response to environmental cues which occur
only at irregular intervals (Fenner 1991). Several hypotheses which attribute an adaptive
significance to mast behaviour have been put
forward. It is often seen as a mechanism of
seed predator deterence, in which the predators are alternately starved and satiated (Silvertown 1980). The fact that species which
share a common seed predator tend to mast
in the same year provides some support for
this hypothesis, since those which do not
conform to the mass fruiting would attract the
predators (Ashton et al. 1988). An alternative
(or possibly additional) advantage would be
more effective pollination by massed flowering (Norton & Kelly 1988). A further consideration is that supra-annual fruiting may just be
a consequence of the need to build up reserves between crops. The cost of fruiting is
high and known to have a depressive effect
on growth in subsequent years (Haase
1986).
Keystone fruit providers
The phenology of fruiting has very important
consequences for community diversity because of the dependence of frugivores on a
constant supply of food. Many tropical forests
support a range of specialist fruit-eating
species, such as birds, primates, bats and insects. The availability of fruit in most communities varies considerably through the year
(Friedel et al. 1993), and many frugivores can
tide themselves over a period of scarcity by
various behavioural devices, such as dietary
switching (to leaves, nectar, etc.), a change in
range, migration and seasonal breeding (Van
Schaik et al. 1993). It is probable that the carrying capacity for frugivores is set by the narrowness of these ‘bottle necks’ or ‘pinch
points’ in fruit availability. For example, the
Urucu terra firme forest in Brazil has a remarkably low density of frugivores compared
with comparable forests elsewhere. Peres
(1994) suggests that this may be linked to the
strongly seasonal production of fruit there,
giving rise to severe shortages which few frugivores can survive. Those species which
fruit in the season of general scarcity therefore have a central role in the maintenance of
community function and diversity. They are
true ‘keystone species’ in the sense that their
removal would cause major community impoverishment. Howe (1984) and Terborgh
(1986) give examples of providers of ‘keystone plant resources’. In many tropical
forests this role falls to members of the fig
genus (Ficus) whose continuous fruiting may
be partly a consequence of its obligate mutualism with wasp pollinators (Lambert & Marshall 1991; Milton 1991). A knowledge of fruiting phenology is of central importance for
conservation management generally, but is of
special value in tropical forests which support
a diversity of fruit-dependent species.
Conclusions
From the current literature on phenological
patterns in plant communities it is possible to
draw a few tentative conclusions and to indicate certain useful directions for future work.
One point which stands out is the need for
long-term research in this area. For example,
a single-year study showing that early and
late flowers suffer more predation than midseason flowers would suggest that selection
would result in syncronous flowering. However, if several years are recorded and it is
found that the timing of the ‘window’ of reduced predation shifts from year to year (as
in Baptisia australis, Evans et al. 1989) our
conclusion would be that selection favours
asynchrony. With masting species, few conclusions at all can be drawn for at least a couple of decades. One very good reason for collecting long-term masting data is to monitor
the biological effect (if any) of global climate
change. Masting species are likely to be particularly sensitive to changes in the frequency
of the climatic cues which trigger flowering.
An increase in mean temperature would increase the frequency of fruit production in
some species (possibly having deleterious
effects of exhaustion), and would decrease
fruiting in those species which require a coldtemperature cue, such as Dacrydium cupressinum (Norton & Kelly 1988). As major
economic species (e.g. most softwoods)
would be affected, as well as many species of
ecological importance, this aspect of repro-
88
M. Fenner
ductive phenology would seem worthy of
more extensive investigation (Fenner 1991;
Lechowicz 1995). The reproductive phenology of whole communities may be markedly
affected by climate change, e.g. montane
grasslands (McKone et al. in press) and
tropical forests (Reich 1995).
A number of studies illustrate the complexity of the interacting forces which may collectively influence flowering times. The effect of
competition between plants for pollinators
must be seen in the context of possible facilitation occurring at the same time (Waser &
Real 1979). The effect of seed predators
should take into account other plant species
sharing those predators (Brody 1997). Superimposed on these biotic influences are the
abiotic constraints, chiefly the timing of resource availability. Since we cannot expect
every investigation to be comprehensive, future work might profitably be concentrated on
systems in which we already have a good
grounding. Investigations which are too narrowly focussed are in danger of missing
some unconsidered influence which may be
of over-riding importance.
The results of most phenological investigations have been expressed in some quantitative way, such as percent reduction in seed
set due to competition for pollinators, or percent seed loss by predation. Rather few have
looked at the qualitative consequences of the
differential survival of certain genotypes. In
some cases the disadvantages of a lower
rate of survival in early or late individuals may
be more than compensated by the long-term
genetic advantages of higher rates of outcrossing. For example, Zimmerman (1988)
demonstrated increased outcrossing in late
flowering Polemonium foliosissimum individuals. In Bartsia alpina seed predation is concentrated on the self-pollinated flowers,
thereby selecting in favour of the outcrossed
individuals which then form a larger proportion of the seed pool (Molau et al. 1989). An
understanding of how these genetic differences in the surviving progeny affect their relative fitness is central to assessing the effects of the various mortality agents on flowering times. The importance of considering
the long-term evolutionary consequences of
ecological processes is stressed by Bradshaw (1984).
Finally, one must emphasize again that in
our search for selective forces, which shape
the phenology of plants, we must always
keep in mind the contraints imposed by their
phylogenetic inheritance. The flowers that
bloom in spring may do so largely because
their ancestors have bequeathed to them a
genetic constitution for doing so. It is highly
probable that these phylogenetic constraints
severely limit the ‘room for manoeuvre’ available for selection and hence adaptation
(Bradshaw 1984). The selective forces which
we investigate (seasonal availability of resources, competition for pollinators, avoidance of loss to seed predators) may have
only marginal effects on highly conservative
genomes.
Lo! In the middle of the wood,
The folded leaf is woo’d from out the bud
With winds upon the branch, and there
Grows green and broad, and takes no care,
Sun-steep’d at noon, and in the moon
Nightly dew-fed; and turning yellow
Falls, and floats adown the air.
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Received 19 January 1998
Revised version accepted 6 April 1998