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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? 80 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- 82 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. References Aide, T.M. 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