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Annu. Rev. Ecol. Syst. 1993.24:353-377 Quick links to online content
THE PHENOLOGY OF
TROPICAL FORESTS: Adaptive
Significance and Consequences for
Primary Consumers*
Annu. Rev. Ecol. Syst. 1993.24:353-377. Downloaded from www.annualreviews.org
1 2 3
Carel P. van Schaik , John W. Terborgh , S. Joseph Wright
l
Biological Anthropology and Anatomy, Duke University, Durham, NC 27705
2center for Tropical Conservation, Duke University, Durham, NC 27705
3
by Duke University on 11/17/12. For personal use only.
Abstract
Most tropical woody plants produce new leaves and flowers in bursts rather
than continuously, and most tropical forest communities display seasonal
variation in the presence of new leaves, flowers, and fruits. This patterning
suggests that phenological changes represent adaptations to either biotic or
abiotic factors. Biotic factors may select for either a staggering or a clustering
of the phenological activity of individual plant species. We review the
evidence for several hypotheses. The idea that plant species can reduce
predation by synchronizing their phenological activity has the best support.
However, because biotic factors are often arbitrary with respect to the timing
of these peaks, it is essential also to consider abiotic influences. A review of
published studies demonstrates a major role for climate. Peaks in irradiance
are accompanied by peaks in flushing and flowering except where water stress
makes this impossible. Thus, in seasonally dry forests, many plants concen
trate leafing and flowering around the start of the rainy season; they also tend
to fruit at the same time, probably to minimize seedling mortality during the
subsequent dry season. Phenological variation at the level of the forest
community affects primary consumers who respond by dietary switching,
seasonal breeding, changes in range use, or migration. During periods of
scarcity, certain plant products, keystone resources, act as mainstays of the
primary consumer community.
*The us government has the right to retain a nonexclusive, royalty-free license in and to any
copyright covering this paper.
353
354 V Al" SCHAlK, TERBORGH & WRIGHT
INTRODUCTION
Inquiries into the phenology of tropical plants mostly take one of two
approaches. The first is to examine the intrapopulational behavior of single
species, or less commonly, groups of related species, in relation to environ
mental factors (6,8). These studies focus on proximate physiological releasing
mechanisms. While daylength, or daylength in combination with rising
temperatures, often triggers the resumption of physiological activity after
winter dormancy at higher latitudes (120), the limited annual variation in these
Annu. Rev. Ecol. Syst. 1993.24:353-377. Downloaded from www.annualreviews.org
factors in the tropics has prompted a search for other kinds of environmental
signals that could serve as reliable indicators of season and/or as proximate
releasers of physiological activity (6, 8, 109).
The second approach is to document the phenology of plant guilds or
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The three phenophases (leafing, flowering, and fruiting) are not mutually
independent in individual woody plants. Can hypotheses for their timing be
considered for each phenophase separately, or should we instead consider any
given phenological pattern as a single trait?
Fruiting must obviously follow flowering, and so questions about one might
produce answers involving the other. Likewise, flowering and leafing can be
interrelated. Axillary, ramiflorous, or cauliflorous flowering may be partly or
wholly independent of leafing activity, but terminal flowering preempts the
terminal buds of a plant and requires the initiation of a new set of shoots from
lateral buds. Terminal flowering thus usually precedes leafing on the same
branch. Many deciduous species show flowering and fruiting during the
leafless phase (46, 70). In other deciduous species (19, 83, 103) and many
evergreen ones (82, 109, 110), flushing and flowering occur on the same new
shoots and therefore occur close in time. Very few studies have examined the
possible functional significance of different interrelationships of the
phenophases (or their link with tree architecture: 17). However, there is
enough variability in their timing to suggest that the developmental programs
of plants are flexible (44, 116, 125, 156). Hence, separate evaluation of
evolutionary hypotheses for the timing of leaf emergence, flowers, and ripe
fruits is warranted. However, whenever such flexibility is limited, we must
expect plants to have evolved phenological patterns reflecting the external
factor that exerted the strongest fitness effects.
Individuals and populations of tropical plants display nearly every possible
phenological behavior from nearly continuous activity to repeated brief bursts,
and from complete intraspecific synchrony to complete asynchrony (leafing:
46, flowering: 107, fruiting: 46, 98). Even in the most uniform tropical
climates, however, only a tiny fraction of individuals shows continuous
leafing, flowering, or fruiting (46, 50, 107, 110, 122, 151). Moreover, some
356 VAN SCHAlK, TERBORGH & WRIGHT
agents.
biotic agents. Second, they may attract pollinators and dispersers or satiate
predators by doing so.
phenology peaks (104). Moreover, in at least one site without migratory birds,
the timing of fruit peaks was similar to that of climatically similar areas
elsewhere (116).
Similarly, the abundance of pollinators may vary seasonally. For instance,
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it has been suggested that numbers of pollinating insects are highest during
the dry season, favoring flowering at this time (44), but the reverse causality
is equally likely (47, 117, 120).
are irregular and associated with El Nino Southern Oscillation events (74,
108), making it difficult for predators to entrain to the rhythm (6). Second,
on nutrient-poor soils, crops produced during annual fruit peaks may not be
large enough to swamp predators. It then becomes advantageous for plants to
store carbohydrate reserves in a form inaccessible to predators and to produce
larger crops at longer intervals (72).
Strong evidence for the hypothesis that masting is an adaptation to reduce
seed predation comes from Silvertown's (132) comparative analysis in the
temperate zone, showing that increased seed crop size is correlated with lower
per capita seed predation risk, and that species subject to heavier seed
predation in years of low fruit production are more prone to exhibit masting.
For Malesia, the evidence is strong but less direct. First, among dipterocarps,
fruiting is more synchronized between species than is flowering (5). Second,
dipterocarp trees fruiting out of synchrony often lose all their seeds to predators
(108, 157). Third, masting species tend to have large seeds that are only
mechanically protected, whereas nonmasting species tend to have seeds that
are small, endozoochorous, or wind-dispersed (74, 151), or are chemically
protected (P Ashton, personal communication).
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Figure 1 The months in which community-wide peaks in leafing (a) or flowering (b) are observed ,
in relation t o latitude. The lines trace solar maxima a s the sun moves toward higher latitudes.
Phenological peaks clearly cluster around these lines. The data are culled from a total of 53 studies
of tropical plant phenology (not all of which reported all three phenophases). Symbols surrounded
by circles are discussed in the text. References and details can De obtained from the authors.
the dry season disrupted pollination and subsequent fruit set, presumably
because it reduced the activity of pollinating agents. The second class of
hypothes(�s argues that flowering or fruiting should take place in weather
TROPICAL FOREST PHENOLOGY 361
windiest times of the year when canopies are bare (44, 46, 64).
However, if fruits dispersed by other means tend to peak at the same time,
this would reduce the explanatory power of the hypothesis. The evidence is
equivocal: although four studies did not show a clear difference in timing
between the fruiting of wind-dispersed species and other wood plants (3, 50,
64, 125), two studies did (24, 44).
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Table 1 Distribution of flowering-fruiting intervals of tropical forest sites (for which information on at least 20 species is available) �
46, 127). Studies reporting flower-fruit intervals for more than 20 species are
compiled in Table 1. There is some effect of the number of dry months on
aspects of the flower-fruit interval distribution; the correlation with the
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Less obvious than seasonal variation in rainfall, and to date largely ignored
by ecologists, is seasonality in solar radiation. As the solar zenith sweeps
from hemisphere to hemisphere, the variation in incident intensity can be
considerable. For example, when the sun is vertically above the Tropic of
Cancer, the radiation falling on the Tropic of Capricorn is only 68% as great.
Seasonally coupled with variation in solar radiation is cloudiness, which can
greatly reduce the available radiant energy (91).
Seasonal variation in cloud cover, daylength, and solar elevation combine
to generate substantial seasonal variation in irradiance. For sites in the wet
tropics, total radiation averages 50% greater in the sunniest than in the
cloudiest month (compiled from 105, 159). On Barro Colorado Island (at
9°N) the dry season peak in photosynthetic photon flux density is nearly
,
twice that of the minimum in the wet season (159). In general, seasonality in
cloud cover is most important near the equator, while other factors increase
in importance toward higher latitudes.
Understory plants of tropical evergreen forests are severely light-limited
(25-27, 113), but accumulating evidence indicates that even canopy trees may
be light-limited (4, 130; D. Clark personal communication). Photosynthetic
measurements show that canopy leaves generally operate below saturation
(35, 111). Several lines of evidence point to the enhancement of photosyn
thetic and reproductive productivity by forest canopies during sunny periods.
First, in everwet climates, productivity may peak in sunny, dry periods (92,
151). Second, dipterocarp masting is both more likely and heavier in years
of high insolation (108, 151, 170). Third, cloudy conditions depress the
productivity of several tropical crops, and high rainfall during fruit ripening
may hamper ripening and r(!duce crop size (141). Finally, flowering is
increased, flower-to-fruit intervals are reduced, and fruit weights are increased
in sunny years (170). These observations suggest that phenological timing
may be an adaptation to seasonality in irradiance.
TROPICAL FOREST PHENOLOGY 365
as well as intrinsic factors such as the extent and depth of the root system.
Even modest water deficits impair growth and cell expansion, and plants under
more severe water stress are unable to produce new organs (63, 150). For
these reasons, it has frequently been inferred that water availability is both
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the proximate and ultimate factor controlling the phenologies of many tropical
forest plants (121).
The water-limitation hypothesis can be tested by asking whether flushing
and flowering peaks at the 53 sites coincide with the onset of the rainiest
season for forests with> 2 dry months (mean monthly rainfall < 60 mm).
The prediction is upheld. We found that the peaks of flushing and flowering
fall within one month of the onset of the rainiest period in respectively 67%
(Gadj. = 13.44, N 18, P < .001) and 60% (Gadj.
= = 10.68, N = 20,P
< . 001) of strongly seasonal forests. In contrast, the comparable figures are
just 33% and 33% for weakly seasonal forests (N = 18 and 24 sites,
respectively) .
Several mechanisms of drought resistance occur among tropical forest plants
(37, 96, 106, 123, 127, 138, 167, 169). Reductions in leaf area, stomatal
and cuticular conductance, and absorbed radiation all reduce transpirational
water loss. Concurrently, deep roots, low resistance to xylem water flow, and
high tissue osmotic potentials serve to maintain water uptake. As a conse
quence, evergreen and wet-season deciduous species that are adapted to grow
and reproduce at the driest time of year occur in many of the driest tropical
forests (37,71). Many more species are able to maintain active growth during
the dry season in less seasonal forests. On Barro Colorado Island, large-scale
irrigation failed to influence the phenologies of most tree and liana species
(165, 166).
2. Insolation. Young leaves that have just finished expanding are most
efficient at photosynthesis (39) and at controlling transpirational water loss
(99). They also have maximum effective leaf area, undiminished by accumu
lating herbivory, epiphylls, or pathological damage. Hence, in the absence
of water limitation, it could be predicted that tropical plants should produce
crops of young leaves to coincide with periods of high assimilation potential
(cf 93, 151), i.e. high insolation.
366 VAN SCHAlK, TERBORGH & WRIGHT
(168). Twilce as many species as expected centered their leafing and flowering
around the sunniest trimester of the year in three different Neotropical everwet
forests. In four different seasonally dry forests, all species with shallow root
systems (unlikely to maintain water status during the dry season) concentrated
leaf production in the wetter season, while two thirds of the deep-rooting
species flushed and flowered in the sunny (dry) season. Observations by Opler
et al (112) also support this idea. In a dry forest, treelets and shrubs of the
uplands concentrated leaf production at the start of the rains, but those near
the river peaked just before the start of the dry season. Thus, tropical trees
tend to concentrate flushing and flowering during the sunniest time of the
year, except when prevented from doing so by water stress.
We can also test this hypothesis with community-level data from the 53
sites mentioned above. In the absence of data on photosynthetically active
radiation for most sites, we substituted information on the monthly duration
of sunshine from the original or other studies at the same site, or from general
climate reference works (18, 58, 105, 131). In everwet areas, 53% of the
flushing peaks (n = 17) fell within one month of the month of maximum
duration of sunshine, about twice the number expected by chance (Gadj. =
5.88, P< 0.05). This effect is weaker in seasonally dry forests (33%, n =
18; n.s.), in which flushing tends to peak about two months later. As to
flowering" 39% of the community-wide peaks are associated with the month
of highest sunshine in everwet forests (n.s.), vs 50% (twice the expected
value) in seasonally dry forests (n = 20; Gadj. = 5.61, P < 0.05). Thus,
community-level patterns also support the hypothesis, given that duration of
sunshine roughly approximates total radiation.
Cloud cover reduces direct beam radiation more than diffuse radiation (36).
Seasonal variation in cloud cover can thus result in differential effects among
forest strata. The understory of deciduous forests experiences wide extremes
of seasonal variation in irradiation (36, 80). In contrast, the understory of
TROPICAL FOREST PHENOLOGY 367
Conclusion
The phenology of tropical woody plants has been shaped by both biotic and
abiotic selective factors. This review demonstrates a major role for abiotic
factors, in particular irradiance and water stress. Biotic factors are frequently
less pervasive and may affect only species or guilds of species. Where they
affect the community, the selection is often for synchrony rather than any
particular timing.
Beyond these emerging generalizations, we must keep in mind that plants
must cope with numerous external biotic and abiotic factors that impinge on
their fitness, each of which may select for particular phenological responses.
In some cases, the pressures exerted by independent selective factors tend to
coincide. For example, by flushing and flowering during periods of high
illumination, plants may improve herbivore avoidance, pollination success,
and net photosynthesis. However, the pressures of external factors can also
select for incompatible outcomes. The challenge now is to design phenological
studies to examine how plants integrate the action of numerous, sometimes
conflicting, abiotic and biotic factors.
as mainstays of the primary consumer community (58, 61, 62, 147, 148).
The abundance of these resources may set the carrying capacity of the
consumer community, while the physical and nutritional properties of
keystone resources appear to determine some morphological features of
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Adaptations to Scarcity
food scarcity only rarely becomes severe enough for long enough to result in
mass starvation of vertebrate consumers. The best documented cases are from
Barro Colorado Island. Foster (45) records 4 episodes of extreme famine, and
10 episodes of mild famine in a 51-year period, all associated with anoma
lously heavy rains in the later part of the dry season. Unseasonal rains resulted
in the subsequent failure of many species to fruit in the ensuing wet season.
More generally, howler monkeys and coati mundis died on Barro Colorado
Island in greater than usual numbers during the normal period of fruit scarcity
in the latter part of the rainy season (79, 102). Apart from Barro Colorado
Island, which no longer holds jaguars, pumas, and harpy eagles, and which
is noted for high mammal densities (56, 67), evidence of animal starvation
in more humid tropical forests is lacking. In 18 years of observations at Cocha
Cashu, Peru, and in 16 years of observations at the Ketambe, Sumatra, we
have not found evidence of mass mortality of primates or other mammals.
Possibly, in these forests, many primary consumers may be kept at sufficiently
low population densities by predators that death by starvation is rare.
pith, fleshy petioles, twigs-16, 146; nectar-68, 114, 129, 144, 149), (ii)
are protected by hard coverings, which increase handling time (e. g. palm
nuts-66, 69, 140, 146), (iii) contain chemical deterrents, which limit the
quantities that can be ingested (mature foliage-52, 95, 101; immature
fruits-43, 146), or (iv) are diffusely distributed in the environment, so that
more time must be invested in searching (e.g. nectar, insects, 146).
Of all the behaviors that serve to mitigate the impact of scarcity, dietary
switching appears to be the most important. Within the guild of frugivorous
primates at Cocha Cashu, Peru, for example, species alter their diets as
Annu. Rev. Ecol. Syst. 1993.24:353-377. Downloaded from www.annualreviews.org
follows: tamarins and night monkeys tum to feeding on nectar (144 and 164);
spider, howler, and titi monkeys eat more leaves (101, 142, 164); squirrel
monkeys engage in day-long insect foraging bouts (146); and capuchins bite
open hard palm nuts (146).
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The opportunities for dietary switching of this kind are closely tied to
phenological patterns, depending, for example, on whether two categories of
resources vary in concert or in opposition over the seasonal cycle. Accord
ingly, the biomass of primate communities tends to be low where peak
abundances of fruit and foliage occur simultaneously, as in the neotropics,
because seasonal switching is precluded, and high where the periods of peak
abundance are seasonally offset, as in central Africa (145).
keystone plant resources at the Neotropical and Asian sites (see also 86).
However, figs do not play such a role at M'Passa (5 1), nor at certain
Amazonian terra firme sites (114). Further studies are obviously needed before
broader patterns emerge.
CONCLUSION
Despite early speculation to the contrary, all tropical forests studied to date
show pronounced phenological variation between seasons and/or between
Annu. Rev. Ecol. Syst. 1993.24:353-377. Downloaded from www.annualreviews.org
years, creating a boom and bust environment for consumers. The frequency,
severity, and duration of scarcity vary greatly from forest to forest, and the
corresponding impacts on consumer communities are likely to vary accord
ingly. Adaptations to scarcity include dietary switching, seasonal breeding,
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