Do seasonal changes in light availability influence the inverse
leafing phenology of the neotropical dry forest understory shrub
Bonellia nervosa (Theophrastaceae)?
Oscar M. Chaves1,2 & Gerardo Avalos1,3
1
2
3
Escuela de Biología, Universidad de Costa Rica, Ciudad Universitaria Rodrigo Facio, San Pedro, San José, Costa
Rica; ochaves@gmail.com
Instituto para la Conservación y el Desarrollo Sostenible San José, Costa Rica; Universidad Nacional Autónoma de
México, Antigua Carretera a Pátzcuaro No. 8701 , Col. Ex-Hacienda de San José de La Huerta, C.P. 58190 Morelia,
Michoacán, México; ochaba@oikos.unam.mx; incodeso@yahoo.com
The School for Field Studies, Center for Sustainable Development Studies, 10 Federal St., Salem, MA 01970 USA;
avalos@fieldstudies.org
Received 23-vII-2006.
Corrected 11-III-2007.
Accepted 14-v-2007.
Abstract: In tropical dry forests most plants are deciduous during the dry season and flush leaves with the onset
of the rains. In Costa Rica, the only species displaying the opposite pattern is Bonellia nervosa. To determine
if seasonal changes in light availability are associated with the leaf and reproductive phenology of this species,
we monitored leaf production, survival, and life span, as well as flower and fruit production from April 2000
to October 2001 in Santa Rosa National Park. Leaf flushing and flower bud production took place shortly after
the autumnal equinox when day length starts to decrease. Leaves began expansion at the end of the wet season,
and plants reached 70 % of their maximum leaf area at the beginning of the dry season, maintaining their foliage throughout the entire dry period. Leaf shedding occurred gradually during the first three months of the wet
season. Leaf flushing and shedding showed high synchrony, with leaf numbers being related to light availability.
Maximum leaf production coincided with peaks in radiation during the middle of the dry season. Decreasing day
length induces highly synchronous flower bud emergence in dry forest species, but this is the first study indicating induction of leaf flushing by declining day length. Rev. Biol. Trop. 56 (1): 257-268. Epub 2008 March 31.
Key words: photoperiodic induction, inverse phenology, Bonellia nervosa, Santa Rosa National Park, tropical
dry forest.
Tropical dry forests portray a diverse mosaic of phenological strategies, which facilitate
plant adjustment to changes in the availability
of water, light, and nutrients across significant
spatial and temporal environmental gradients
(Borchert 1994, 2000). The phenological patterns of tropical dry forest plants are complex
(Borchert 1994), and range from evergreen species restricted to moist microsites along riparian habitats, to dry-season deciduous species
occupying some of the driest habitats –including seasonal deserts– found in the Neotropics
(Borchert et al. 2004). Understanding the
integration of the environmental and endogenous controls of such diverse phenological
patterns stretches the limits of plant physiological ecology (Borchert 1983, 2000, Rivera
et al. 2002, Borchert et al. 2005), requiring a
detailed knowledge of physiological mechanisms within the ecological and evolutionary
context under which they are expressed.
In the tropical dry forests of Guanacaste,
Costa Rica, most woody plants become deciduous during the dry season (Janzen 1967,
Frankie et al. 1974, Opler et al. 1980, Reich
and Borchert 1984), but some species show
Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (1): 257-268, March 2008
257
an inverse leafing phenology, producing and
maintaining all leaves during the dry season,
to abscise them with the onset of the rains
when the canopy begins to close (Janzen
1970, Sobrado 1986, Reich 1995, Roupsard
et al. 1999). Bonellia nervosa C. Presl.
(Theophrastaceae) –formerly Jacquinia pungens– (Janzen 1970, 1983, Daubenmire 1972,
Bullock and Solís-Magallanes 1990, Ståhl and
Källersjö 2004) belongs to this category. An
inverse leafing phenology is prevalent in
phreatophytic species (Janzen 1970, Holbrook
et al. 1995) where the depth of the root system facilitates access to underground water
sources that reduce water stress during the dry
period (Dawson and Pate 1996, Roupsard et
al. 1999). This strategy expands the previous
classification of dry forest phenological strategies into functional groups (Borchert 1994),
being in contrast with that of leaf-exchanging
species (which drop leaves at the start of the
dry season, and expand new leaves almost
immediately as depending on the availability
of water), or with the phenological pattern
of spring-flushing species (which flush new
leaves around the spring equinox before the
first rains, Elliott et al. 2006). These latter
species are restricted to humid microsites
that have the water to afford leaf expansion,
and remain well hydrated throughout the rest
of the dry season (Borchert 1994, Elliott et
al. 2006). Phreatophytic species belong into
a category of their own, being analogous to
cold-temperate understory plants of deciduous forests, which complete their reproductive
cycle early in the spring before trees leaf out
and the canopy closes.
B. nervosa is an understory shrub abundant in deciduous and semi-deciduous forests
throughout the pacific coast of Mesoamerica,
from southern Jalisco, Mexico, to northwestern
Costa Rica (Ståhl 1989, Ståhl and Källersjö
2004). This species is found in mature and secondary dry forests, forest edges, and pastures,
over a variety of soil conditions. The overall
structure of B. nervosa is clearly xerophytic.
Leaves are coriaceous, with the apex modified
as a spine, and are produced synchronously at
258
the start of the dry season. A crop of new leaves,
flushed in synchrony, is likely to be more efficient controlling gas exchange during the dry
season peak in understory light availability than
a crown composed of overlapping leaf cohorts
of different ages. This is afforded by a considerably deep root system (down to 8 m, Janzen
1970, 1983, Oberbauer 1985), which facilitates
access to subsoil water when the majority of
the plant community is deciduous. B. nervosa
is the only species in its family showing this
intriguing pattern of inverse leafing phenology
(B. Ståhl, pers. com.). Under more severe water
seasonality (i.e., the Sonoran Desert, Mexico)
B. nervosa is evergreen, but shows inverse
phenology in the deciduous forests of veracruz,
México (A. Búrquez, pers. com.), which have a
rainfall seasonality similar to that of our study
site in Santa Rosa, Costa Rica.
In this study, we explored the extent to
which seasonal changes in light availability
are associated with the leafing and reproductive phenology of B. nervosa. In addition, we
measured the synchrony in leaf, flower, and
fruit production, and analyzed the effect of
plant size on leaf, flower, and fruit production.
Understanding how light is related to the phenological behavior of B. nervosa will increase
our knowledge on the strength of proximate
causes influencing the phenology of tropical
plants. This is becoming critically important
within the context of rapid changes in weather
conditions related to global warming, which
are influencing the phenological behavior and
carbon budget of tropical forests (Wright et al.
1999, Clark et al. 2003).
MATERIALS AND METHODS
Study Site: this study was carried-out over
18 months (April-July 2000, and November
2000 to October 2001), along the “Indio Pelado”
trail in Santa Rosa National Park, Guanacaste,
Costa Rica. Santa Rosa lies between the Gulf
of Papagayo and the Panamerican Highway
(10°44'13'' to 11°00'37'' N and 85°34'48'' to
85°58'51'' W) at 290 m in elevation. The upper
Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (1): 257-268, March 2008
plateau maintains tropical premontane forests,
whereas the coastal lowlands present a large
extension of tropical dry forest (Tosi 1969).
Average annual rainfall is 1 423 mm. The dry
season starts in late November and extends
into late April. During this period most of the
canopy trees are deciduous (Janzen 1967).
Average annual temperature is 25.7 °C, and
average relative humidity is 81 % (Santa Rosa
National Park Climate Records).
The “Indio Pelado” trail is dominated by
seedlings and saplings of canopy species and
understory shrubs (i.e., Cochlospermum vitifolium, Semialarium mexicanum, B. nervosa),
trees of 10-20 m in height (i.e., Spondias
mombin, Bursera simaruba), and a few 20-35
m tall trees still remaining from the original primary forests (i.e., Pachira quinata,
Manilkara chicle, Hymenaea courbaril and
Pseudobombax septenatum).
Study species: the genus Bonellia
(Theophrastaceae) consists of 22 species of
xerophytic shrubs and small trees distributed in
dry areas of Mesoamerica, the Greater Antilles,
Central America, and northern and western
South America (Ståhl and Källersjö 2004).
Only B. nervosa has an inverted leafing phenology. In Santa Rosa National Park, B. nervosa reaches a density of 0.1-60 adults per Ha
(Janzen 1970). Adults range 1.5-6 m in height,
but individuals above 5 m are rare. Leaves are
coriaceous, simple, alternate, with the apex
modified as a spine. Production of leaf buds
start in late September to mid-October (Opler
et al. 1980, pers. obs.), and leaves are dropped
in July-August (pers. obs.) Small orange flowers are produced in terminal cimes, and are
very likely pollinated by bees, as deduced
from flower morphology and scent chemistry
(Knudsen and Ståhl 1994). Fruit production
takes place during the dry season (FebruaryMarch), one month after anthesis. Fruit expansion extends to the onset of the rains in May.
Ripe fruits are orange, and contain up to 10
seeds covered by a sweet, fleshy aril. Fruits are
maintained on the plant for nearly two years
(Opler et al. 1980). Although dispersal agents
are not known with certainty, rodents could
easily crack the fruit and eat the aril, helping to
disperse the seeds (Janzen 1970).
Measurement of leaf phenology and leaf
structure: leaf production and life span were
monitored every two weeks from October 2000
to August 2001. We randomly selected 80 individuals with stem diameters >2 cm. Of these
individuals, we randomly chose 36 plants of a
variety of heights, on which all measurements
were concentrated. We randomly selected 20
external branches per plant and marked them
with plastic tags (200 leaves per plant, 5-15
leaves per branch). We obtained a sample
of 5 leaves taken from each of 30 different
adult plants, measured leaf length and width,
and then estimated the actual leaf area with a
Li-Cor Li-3100 leaf area meter (LI-COR Inc,
Lincoln, Nebraska). We used a linear regression to calculate the leaf area in the field using
leaf length and width as predictor variables
(r2=0.97, N=125, p=0.001). Estimates of leaf
area were obtained every week at the beginning
of the dry season (between December 2000 and
February 2001) using 20 marked leaves from
each plant. To monitor the temporal progression of changes in leaf structure, we determined
leaf mass per area (LMA) taking ten leaves per
plant every two weeks from December 2000 to
June 2001.
Leaf, flower and fruit synchrony: synchrony in leaf production was calculated following Augspurger (1983) using the formula:
Xi=∑ej=i/(n-1)fi, where Xi is average synchrony in module production at the population
level; ej is the number of days in which plants
i and j produced a particular module; fi is the
life span of the module in plant i; and n is the
sample size. The index varies between 1 (100
% of synchrony) and 0 (total asynchrony).
Assessment of variation in the light
environment: hemispherical canopy photographs were taken 0.5 m above the crown
under overcast sky conditions using a FC-E8
Nikon Coolpix 950 digital camera adapted to
Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (1): 257-268, March 2008
259
a fish-eye lens of 7.5 mm. Digital images were
analyzed using Hemiview (Delta-T Devices
Ltd.) We analyzed the specific site distribution
of direct and diffuse radiation (site factors)
using the expected radiation values per site.
We obtained the direct site factor to evaluate
the fraction of direct radiation reaching each
plant relative to the total amount of light available at the top of the canopy. We calculated the
indirect site factor (diffuse factor, or radiation
filtered by the canopy) observed at the plant
crown relative to the radiation reaching an
open site. Using these indices, combined with
photon flux density data (PFD) obtained from
the Santa Rosa National Park weather station,
we calculated values of direct and indirect
radiation reaching each plant, according to the
canopy conditions and light intensities prevalent at each sampling date.
Statistical analyses: to determine the
influence of radiation on leaf, flower and fruit
production over time, we applied general mixed
linear models (GMLMs) for repeated measures
(SAS 1994) considering that deviations from
normality and heterogeneity of variances of
the response variables did not allow the use
of MANOvA or repeated measures ANOvA.
GMLMs do not assume normal distributions
or homogeneous variances, but rather inspect
different probabilistic distributions to calculate
the residual error (Breslow and Clayton 1993).
The models calculate a response variable Y
from a linear function of a group of values y1,
y2, ..., yp obtained from the original response
variables Y1, Y2, ..., Yp. This response variable
is known as the linking function (g(µ)):
g(µ)=β0+Σβixi
According to Breslow and Clayton (1993),
the regression coefficients, βi, compare the
effects of each factor ai on the dependent variable Y with a base factor chosen at random,
whose effect by definition is zero. When βi>0
the base factor increases the value of Y, if βi<0
the base factor decreases the value of Y, and
when βi=0 there is no effect on Y. In this case,
260
the effects of indirect and direct radiation and
plant size on leaf, flower and fruit production
were analyzed through GMLMs using a logarithmic linking function, since the data and the
error showed a negative binomial distribution
(X2=74.5, df=224, p=0.34). We obtained the
following model:
g(µ) = log(p) = µ + β1x1 + β2x2 + β3x3 + e,
where p is leaf, flower or fruit production
assuming a repeated measures model, x1 is
the effect of direct radiation, x2 is the effect of
indirect radiation, and x3 is plant size. Finally,
e is the residual error according to the negative
binomial distribution. The degree of significance of each component is calculated using a
X2 test. To control for Type I errors we applied
a sequential Bonferroni correction following
Rice (1989).
RESULTS
Influence of light and plant size on leaf
phenology: direct light was related to leaf and
flower bud production, and number of flowers.
Diffuse light (indirect light) and plant size were
not associated with leaf and reproductive phenology (Table 1). Leaf flushing and bud production took place right after the autumnal equinox
following a decrease in day length. Leaves
started expanding at the end of the wet season
(mid to late October), so that plants reached
about 70 % of their maximum crown area at
the beginning of the dry season (November).
Leaf numbers were coupled with the temporal
variation in direct light (Table 1, Fig. 1A).
The number of new leaves per plant changed
with the variation in direct light throughout
the study period (r2=0.37, N=27, p=0.0006).
Leaf numbers and direct light reached a peak
high in February during the middle of the dry
season, and then decreased with the onset of
the rains in May as the canopy began to close,
although decreasing leaf numbers lagged two
weeks behind the reduction in direct light after
the start of the rains in May (Fig. 1A). Peaks
Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (1): 257-268, March 2008
TABLE 1
Regression coefficients (±1 SE) between light availability and leaf, flower and fruit production in 36 reproductive plants
of B. nervosa in Santa Rosa National Park, Costa Rica
β
SE
X2
df
Leaf production
Direct light
Direct light*date
Indirect light
Plant size
0.0013
0.028
-0.0001
0.0007
0.0001
0.007
0.0027
0.0009
19.23 **
24.8 *
0.002 NS
0.65 NS
1
8
1
1
Flower bud production
Direct light
Indirect light
Plant size
0.011
- 0.0262
0.0035
0.0004
0.0125
0.0038
14.50 *
1.65 NS
0.75 NS
1
1
1
Flower production
Direct light
Indirect light
Plant size
0.0086
-0.0594
-0.0028
0.0015
0.0132
0.0026
10.03 *
3.15 NS
0.62 NS
1
1
1
Fruit production
Direct light
Indirect light
Plant size
-0.0015
0.0183
0.0081
0.0004
0.0075
0.0030
3.52 NS
4.62 NS
2.07 NS
1
1
1
Phenological character
Factor
* p < 0.01, ** p < 0.001, NS = non-significant.
in flower and fruit production in February
2001 coincided with a peak in direct light that
lasted two months (Fig. 1B). The increase in
direct light coincided with the onset of leaf
flushing and the production of flower buds.
This temporal relationship was reflected in a
significant association between direct light on
leaf, flower bud, and flower production, and a
significant interaction between direct light and
time vs. leaf production (Table 1). All plants
were deciduous by August (mid rainy season).
Average life span was 11.15 months (SD=1.33,
N=120), which included the time from leaf
bud production to leaf shedding. This value
could be overestimated, since most senescent
leaves reached a light yellow coloration by mid
July, but remained on the plant a substantial
time, before falling off. The synchrony in leaf
production was considerably high (mean=0.88,
SD=0.06, N=36 plants).
Leaf production coincided with flower bud production in the majority of plants
(Fig. 1A). Anthesis started by mid January
and reached a peak during the first week of
February (Fig. 1B). The synchrony of flower
(mean=0.38, SD=0.26, N=36) and fruit production (mean=0.18, SD=0.18, N=36) was
relatively low. Only direct light was significantly related to the number of flowers during
the study period. The number of fruits was not
associated with direct light, indirect light or
plant size (Table 1).
In addition to the significant increase in
PFD in the understory observed in October
2001 (Fig. 1A), we recorded a slight increase in
mean air temperature of 0.76 oC (from 23.68 oC
±0.47 in September to 24.44 oC ±0.7 in October,
Fig. 2). The low magnitude of the differences
and the timing of peaks in air temperature
makes this factor unlikely to have affected leaf
Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (1): 257-268, March 2008
261
August
July
June
Flower buds
May
March
February
January
November
October
September
April
Leaves
PFD
A
Wet season
Dry season
140
900
800
700
100
600
80
500
400
60
300
1%' NPMtN-2s-1)
Number of leaves / Flower buds
120
40
200
20
100
0
0
71
87
102 118 131 152 171 184
Flowers
March
February
January
November
October
September
Ripe fruits
Dry season
202 218 234 252 271
Fruits
August
B
52
July
36
June
26
May
13
April
0
Wet season
0.9
0.8
Proportion of maximum value
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
-0.1
0
13
26
36
52
71
87
102 118 131 152 171 184 202 218 234 252 271
Time (days)
Fig. 1. (A) Seasonal variation in direct light (PFD) and its relationship with leaf and flower bud production; (B) proportion
of maximum values of flower, fruit and ripe fruit production in Bonellia nervosa. values are means (±1 SE) of modules of
36 reproductive plants.
262
Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (1): 257-268, March 2008
30
Mean air temperature (ºC)
29
Wet season
Dry season
Wet season
28
27
26
25
24
23
22
21
20
Sept
2000
Oct
Nov
Dec
Jan
2001
Feb
Mar
Apr
Jun
Jul
Fig. 2. Mean air temperature (±1 SE) in Santa Rosa National Park, Costa Rica.
120
80
60
40
20
0
0
21
35
50
80
148
163
178
193
Time (days)
7
Wet season
Dry season
B
6
Leaf area (gm-2)
Rate of leaf expansion: leaf expansion
was completed in 20.5 d (SD=5.7, N=150, Fig.
3B) reaching 5.28 cm2 (SD=3.32, N=155) at
the end of the wet season. Leaf area in fully
expanded leaves was not related to the initial
light environment in which expansion took
place (r2=0.031, N=18, p=0.57).
Wet season
Dry season
A
100
LMA (gm-2)
production, since the highest temperature values
were observed in April at the end of the dry season (Fig. 2), whereas the peak in leaf production
was observed in February (Fig. 1A).
Leaf mass per area (LMA): this parameter
showed a steady increase throughout the study
period (Fig. 3A). It increased with the advancing dry season, reaching 103 gm-2 (SD=33.77,
N=215) at the end of May, and then it decreased
during the following months. The decrease in
LMA was associated with loss of photosynthetic pigments, and an increase in the yellow
hue of the leaf before abscission.
5
4
3
2
1
0
DISCUSSION
0
10
30
46
55
Time (days)
In weakly seasonal tropical forests the vegetative and reproductive phenology of canopy
trees is concentrated during periods of high
irradiation (Janzen 1967, Wright 1992, Wright
Fig. 3. (A) Seasonal variation in mean LMA; and (B)
temporal changes in the rate of leaf expansion in 25 adult
plants of B. nervosa. values are means (±1 SE) of 5 leaves
per plant.
Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (1): 257-268, March 2008
263
and van Schaik 1994, Grace et al. 1995, AnguloSandoval and Aide 2000, Hamann 2004). This
tendency has been observed for diameter
increases in the evergreen forests of Suriname
(Schultz 1960), in the flowering of canopy trees
of peninsular Malaysia (Wright and van Schaik
1994), in diameter growth and flower and fruit
production of canopy trees at La Selva, Costa
Rica (Raich et al. 1991, Clark and Clark 1994),
in leaf (Barone 1998) and flower production on
Barro Colorado Island, Panama (Croat 1969,
1975), and in seed production of canopy trees in
Borneo (Wycherley 1973). The increased light
conditions caused by El Niño on Barro Colorado
Island favored fruit production by reducing
light limitation and synchronizing reproduction
(Wright et al. 1999).
In contrast, in tropical dry forests, water
limitation –and thus, susceptibility to seasonal
drought– is considered the most important
factor driving leafing and reproductive phenology (Borchert 1983, 1994, Lieberman and
Lieberman 1984). The seasonality of water
availability entrains vegetative growth, synchronizing it to match periods in which water
is not limiting (Borchert 1983). In this manner,
plant physiological status is affected by water
seasonality, which controls vegetative growth
and consequently determines flower periodicity. However, these controls are not simple,
and depend on the vascular architecture, overall tree architecture and morphology, and the
pattern of biomass allocation (i.e., amount of
biomass allocated to roots). Recently, several
authors have pointed out that leaf flushing and
flower production in tropical forests during the
dry season can be induced by increasing day
length (spring equinox in the northern hemisphere, Borchert et al. 2005), being facilitated
by sufficient access to subsoil water to afford
leaf production and maintenance during the
remaining part of the dry season (Rivera et al.
2002, Borchert et al. 2005, Elliot et al. 2006).
This scenario could work in the opposite manner for B. nervosa, since leaf flushing and
flower bud production took place shortly after
the autumnal equinox when day-length started
to decrease. Leaves started expansion at the
264
end of the wet season (mid-to-late October),
so that plants reached 70 % of their maximum
leaf standing crop at the beginning of the dry
season, maintaining their foliage throughout
the entire dry period. Decreasing day length
induces the highly synchronous emergence of
flower buds in deciduous tropical dry forest tree
species (Rivera and Borchert 2001, Borchert et
al. 2004), but induction of leaf flushing by
declining day length has not been reported
until now. Even in the driest microhabitats of
tropical dry forests there is clear selection for
increased leaf area when the opportunity for
carbon gain is high, as long as water stress is
prevented. Borchert (1994) found that trees
colonizing dry upland forests concentrated
flushing at the start of the rainy season, but
those near a river peaked before the start of the
dry season. In the monsoon forests of Thailand
and India most trees flush new leaves in March
and May, the driest and hottest time of the year,
just 1-2 months before the first monsoon rains,
relying on subsoil water to afford leaf production. In these forests, leaf flushing is induced
by an increase in photoperiod after the spring
equinox (Elliot et al. 2006). Congruent with
these patterns, in B. nervosa –whose roots can
reach subsoil water– leaf and flower production were closely related to increased levels of
direct light, following the autumnal equinox.
Janzen (1970) observed leaf production from
late November to early December coinciding
with canopy aperture and increased light intensity, whereas Opler et al. (1980) reported leaf
flushing in September. Methodological differences in the monitoring of leaf flushing, as well
as microhabitat differences, are most likely
responsible for these discrepancies. However,
we observed the initiation of leaf production
and shortly after, flower bud production in midto-late October with a relatively high degree of
synchrony in leaf production.
In contrast to leaf production, flower and
fruit production had low values of synchrony. It
is likely that plants, independently of their size,
invest in reproduction according to their access
to resources. Leaf and flower bud production
were very likely the result of storage, since
Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (1): 257-268, March 2008
the initiation of both processes coincided with
increased canopy aperture and both peaked
relatively quickly. Flower initiation was not
determined by achieving a peak in leaf area,
although it is possible that concentrating leaf
area during the dry season favors the rapid
nutrient accumulation to balance the expenses
of growth and reproduction the following year.
Although increased light was associated with
flower bud production and number of flowers,
it was not related to fruit production. To fully
explain these differences it is necessary to
study the reproductive ecology of B. nervosa,
which still is poorly understood. The number
of flowers that are fertilized is dependent on the
behavior of pollinators, but this aspect, along
with the dispersal ecology of the species, is not
well known.
Patterns of plant phenology in the tropics are highly complex, and are affected by
multivariate factors. Irrigation experiments in
dry forests (e.g., Reich and Borchert 1984) and
seasonal moist forests (e.g., Barro Colorado
Island, Wright and Cornejo 1990) show high
variation in the timing of leaf flushing and leaf
fall, which for many species are not associated with water stress. Changes in photoperiod,
relative humidity, wind speed, and incident
radiation are superimposed on the life history
strategies of biomass and reproductive allocation, as affected by competitors and seed
predators (e.g., Liberman and Lieberman 1984,
Aide 1992), as well as by endogenous rhythms
(correlative controls following Borchert 2000).
Since physical and biological factors work
simultaneously, it is not surprising that most
phenological studies are based on correlations
between changes in phenological characters
and the temporal variation in physical factors, whose causality is established by proposing a tentative physiological mechanism.
Most of the studies that have increased our
understanding of the phenological patterns of
tropical plants by presenting testable hypotheses are based on correlative observations
and indirect evidence (i.e., consistent patterns
across species and ecosystems, Borchert 2000,
Borchert et al. 2004, 2005, Elliot et al. 2006).
Controlling and isolating environmental factors at the community level is not feasible.
Simpler experiments, using seedlings in growth
chambers, are more reasonable to implement,
but whether their conclusions can be extended
to complex tropical dry forest communities
is still under dispute. Within this context, our
methods of analyses were exploratory, and the
clear timing between direct light and leaf and
flower production suggests a link between light
availability and leaf phenology in B. nervosa.
This pattern is congruent with the production of
maximum leaf area during periods of high light
availability (with leaf flushing cued by decreasing photoperiod), and rapid leaf loss shortly
after canopy closure. Our results showed a high
degree of synchrony in leaf production, which
changed in accordance with canopy aperture.
Although in several tropical dry forest species
early leaf flushing coincides with peaks in air
temperature (i.e., Tabebuia rosea, Gómez and
Fournier 1996, and Enterolobium cyclocarpum,
Rojas 2001); we do not consider this to be the
case in B. nervosa, due to the low magnitude
of the temperature differences and the timing
of peaks in air temperature.
It is well established that in adults of B.
nervosa the root system can reach 8 m in depth
(Janzen 1970), allowing access to subsoil water
throughout the entire dry season. In Faidherbia
albida, another species with inverse phenology, roots can reach 30 m in depth (Dupuy and
Dreyfus 1992). Roupsard et al. (1999) showed
that the phreatophytic character of this species
enables it to withstand the dry season without
being exposed to severe water stress. Similar
biomass allocation patterns have been observed
in seedlings of B. nervosa (pers. obs.).
B. nervosa is specialized to exploit the
higher light levels prevalent in the understory
during the dry season. This was reflected in the
tight coupling between the leafing phenology
and increased light levels, the presence of a
deep root system, and the magnitude and temporal progression of leaf structural characters.
In addition, leaf and flower bud production were
triggered by decreasing day length, since both
processes began with high synchrony shortly
Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (1): 257-268, March 2008
265
after the autumnal equinox. Due to the potentially high respiratory demands and the reduced
light levels, B. nervosa looses all its foliage during the wet season. In most sun-adapted species,
high metabolic rates represent high respiratory
costs relative to shade-adapted species (Bazzaz
and Carlson 1982, Pearcy et al. 1987, Mulkey et
al. 1993, Chazdon et al. 1996, Zotz and Winter
1996), and are incompatible with prolonged
shade (Givnish 1988, Chazdon et al. 1996).
Future studies should examine the environmental controls of light quantity and quality on the plasticity of expression of the
inverse leafing phenology, as well as the factors that influence the transition of B. nervosa
seedlings from evergreen to deciduous. It is
likely that with higher light availability during the wet season B. nervosa could maintain
an evergreen habit, but it is not clear how the
leafing phenology changes with light, water
access, and photoperiod in other latitudes. Our
study has only outlined the basic phenological
pattern, and calls for more in situ, mechanistic
studies on the plasticity and evolution of the
inverse leafing phenology of this dry forest
understory shrub.
ACKNOWLEDGMENTS
En los bosques tropicales secos la mayoría de las
plantas pierden sus hojas durante la estación seca y las
producen con el inicio de las lluvias. En Costa Rica la
única especie que muestra el patrón fenológico inverso es
Bonellia nervosa. Para determinar si los cambios estacionales en la disponibilidad de luz estaban asociados con la
fenología foliar y reproductiva en esta especie, monitoreamos la producción y sobrevivencia de hojas, así como la
producción de flores y frutos de abril del 2000 a octubre del
2001 en el Parque Nacional Santa Rosa. La producción de
hojas y botones florales ocurrió poco después del equinoccio de otoño, cuando el fotoperíodo comenzó a disminuir.
Las hojas comenzaron a expandirse a finales de la estación
lluviosa, y las plantas alcanzaron 70 % de su área foliar
máxima al inicio de la estación seca, manteniendo las
hojas durante todo el período seco. La caída de hojas tuvo
lugar gradualmente durante los primeros tres meses de la
estación lluviosa. La producción y caída de hojas mostró
alta sincronía, estando el número de hojas relacionado
con la disponibilidad de luz. La producción máxima de
hojas coincidió con picos en la radiación a mediados de la
estación seca. La disminución del fotoperíodo induce alta
sincronía en producción de botones florales en especies del
bosque seco, pero este es el primer estudio que reporta la
inducción de producción de hojas debido a la disminución
en el fotoperíodo.
Palabras clave: inducción fotoperiódica, fenología inversa, Bonellia nervosa, Parque Nacional Santa Rosa, Bosque
Tropical Seco.
REFERENCES
This article is dedicated to the memory
of one of the pioneers of the study of the phenology of tropical trees, Luis Fournier. The
authors thank Oscar J. Rocha and Luis Fournier
for their logistical support during fieldwork.
Jorge Lobo helped with statistical analyses.
María Marta Chavarría and Felipe Chavarría
provided invaluable help during fieldwork in
Santa Rosa. Rolf Borchert provided helpful
criticism on an early version of this manuscript. Blair Brown proofread the final draft.
This research was supported by the Graduate
School of the University of Costa Rica (SEP),
the Organization for Tropical Studies (OTS)
through an Andrew W. Mellon Foundation fellowship, and by the organization IDEAWILD.
266
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