Vol. 1/1, pp. 78–91 Perspectives © Gustav Fischer Verlag, 1998 in Plant Ecology, Evolution and Systematics The phenology of growth and reproduction in plants Michael Fenner Biodiversity & Ecology Division, School of Biological Sciences, University of Southampton, Bassett Cres- cent 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 phe- nology of leafing, flowering and fruit production in a range of species and communi- ties. The selective forces (both abiotic and biotic) that influence the timing of these events are discussed. Within the limits imposed by phylogenetic constraints, the phe- nological patterns (timing, frequency, duration, degree of synchrony, etc.) of each phase are probably the result of a compromise between a variety of selective pres- sures, 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 obli- gate frugivores in many tropical communities. The importance of long-term recording is stressed, particularly in species which fruit irregularly. An understanding of the phe- nology 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, tory events occurring in response to water The full-juiced apple, waxing over-mellow, availability. Drops in a silent autumn night. Phenology (from the Greek phainein, to All its allotted length of days, show or appear) is the study of the timing of The flower ripens in its place, these life-history events. In plants, bud-burst, Ripens and fades, and falls, and hath no toil, leaf-expansion, abscission, flowering, fertili- Fast-rooted in the fruitful soil. sation, seedset, fruiting, seed dispersal and – Tennyson, The Lotus Eaters germination all take place in due season. For the most part, these events are too familiar to attract any special attention. Only when the Introduction expected pattern is broken, for example by out-of-season flowering or the loss of fruit One of the most familiar of all natural phe- due to a late frost, is our attention drawn to nomena is the cycle of events associated the importance of timing of growth and repro- with the passage of the seasons. This is duction in the life of plants. especially so in temperate and polar regions Phenological studies are as important to where annual changes in temperature are our understanding of species interactions and great and are accompanied by corresponding community function as the spatial aspects are. cycles in the growth and reproduction of the In Europe there is a long tradition of phenolog- flora. In tropical regions, seasons are often ical recording, which goes back to the last marked by differences in rainfall, with life-his- century, with an international network of phe- Phenology of growth and reproduction in plants 79 nological gardens. The information gathered in nature, it may not be easy to identify the rel- has mainly been used as a kind of bioindicator evant ones. The long-term cause of the timing of climatic patterns (Schnelle 1965–1986, of a life-history event is the selection pressure 1977). However, data about recurring life-his- which has resulted in the evolution of the tory events are still relatively scarce for most plant’s idiosyncratic phenology. These pres- communities. Some of the reasons for this are sures may range from abiotic constraints (e.g., pointed out by Lechowicz & Koike (1995). seasonally unfavourable temperatures, erratic Firstly, the data are hard won. They can only rainfall), to biotic pressures such as seasonal be accumulated by many years of repetitive presence of predators, pollinators and dis- recording at the same site. Phenological stud- persers. Many phenological studies are basi- ies need long-term planning and funding, and cally concerned with answering the question so do not lend themselves to the short-term ‘Why now, rather than earlier or later?’ The requirements of thesis projects, grant cycles, timing of a particular life-history event may be and the priorities of awarding bodies. Never- the result of selection for exploiting a favo- theless some excellent long-term studies have urable slot sandwiched between two more been published (e.g. Norton & Kelly 1988; hazardous periods. Allen & Platt 1990) and are a tribute to the per- Most life-history events occur over a sistence of their authors. period of time, and their timing can be de- The phenology of plant communities can scribed and quantified in terms of a number be studied by dealing with particular life-his- of parameters (Newstrom et al. 1994). These tory stages separately, such as leafing, flow- are (1) the frequency of occurrence, which is ering, fruiting, seed dispersal and germina- often annual; (2) the time of occurrence, tion. Each of these events occurs in its own which includes the starting date of the earliest calendar slot, but there is clearly some inter- individuals and the date of peak activity; (3) dependence between them. Fruiting must the duration of the event; (4) the magnitude wait upon flowering; seed dispersal cannot (both the mean and variability); and (5) the preceed fruiting. Each phenomenon can be degree of synchrony both within and between studied at different levels of organisation. For species. In general, where the climate is example, we can study the phenology of flow- highly seasonal, as in temperate regions and ering in a whole plant community, or in a guild in the dry tropics, the phenology of whole of species sharing a pollinator, or in a popula- communities tends to follow a broadly similar tion of a particular species, or in the flowers pattern from year to year, though modifica- on a single plant. Even an individual flower tions occur due to climatic differences be- undergoes a sequence of events (bud burst, tween years. Leaf flushing tends to be rela- stigma ripening, pollen shedding, fertilization, tively constant from year to year, but repro- fruit swelling, etc.) whose phenology differs duction can be erratic, especially in harsh cli- between species and is presumed to be the mates (Allen & Platt 1990). In the wet tropics result of natural selection. At each level, the where annual seasons are less marked, a constraints and selective forces which influ- great variety of phenological patterns are ence timing are different. This approach to seen: in different species, flowering may be examining phenological information at suc- continual, sub-annual, annual or supra-an- cessively finer levels of organisation is well nual, and may occur regularly or irregularly exemplified in the review of flowering pat- (Newstrom et al. 1994). The great variety of terns by Primack (1985). patterns encountered in leafing, flowering For individual species it is important to dis- and fruiting in any given habitat may be a re- tinguish between the physiological and eco- flection of diverse biotic and abiotic selective logical/evolutionary answers to the question of pressures operating in all communities. why leafing, flowering or fruiting occurs at a This review examines some of the inter- particular time. The immediate cause of a phe- esting questions which arise in relation to the nological event is the organism’s detection of phenology of plants, and attempts to summa- the environmental cues which trigger the ap- rize some of the answers which have been propriate response, e.g. a flowering response put forward. The main questions dealt with to short or long days (Bernier et al. 1981). here are: Physiological responses are in principle easy 1. How and why do plants differ from each to explore experimentally, though with so other in the timing of their life history many potential cues operating simultaneously events? 80 M. Fenner 2. Why is the same stage apparently ‘stag- ranged from synchronous to continuous in gered’ between some sympatric species? different species and that there were large 3. Why do some stages occur on an annual differences in longevity. In seasonal climates, cycle while others do not? the production of new leaves tends to be con- 4. What are the constraints on the timing or centrated for most species into a short period frequency of a particular phase? of the year. This is the case both in evergreen 5. How does the phenology of the plants af- communities (such as the boreal conifer for- fect the primary consumers? est) and in deciduous forests (both temperate 6. How might global climatic change affect and tropical). Usually leafing is linked with the phenology of plants and hence the some climatic feature such as rainfall (Lieber- functioning of whole communities? man & Lieberman 1984; Bullock & Solís-Ma- gallanes 1990), irradiance (Wright & Van An excellent introduction to the broad topic Schaik 1994), temperature (Brooke et al. of phenological patterns in plants is provided 1996), or photoperiod (Loubry 1994). Where by Rathcke & Lacey (1985). For the flowering water is not a limiting factor, irradiance may phenology of tropical forests, Newstrom et al. play a predominant role. In a major study of (1994) have successfully reduced the great eight disparate tropical forests, Wright & Van variety of patterns found to a small number of Schaik (1994) show that leaf (and flower) pro- identifiable types. Also in tropical forests, Van duction coincides with seasonal peaks of irra- Schaik et al. (1993) have synthesized a diance. In three cases peak irradiance oc- range of data on phenological adaptation to curred in the drier season. Leaf production abiotic conditions, and discuss the commu- can be artificially induced in some cases by nity effects of phenological events.