BIOTROPICA 42(1): 104–111 2010 10.1111/j.1744-7429.2009.00539.

Phenology, Lignotubers, and Water Relations of Cochlospermum vitifolium, a Pioneer

Tropical Dry Forest Tree in Costa Rica

Lottie Fallas-Cedeño1, N. Michele Holbrook2, Oscar J. Rocha3, Nelly Vásquez4, and Marco V. Gutiérrez-Soto1,5
1
Estación Experimental Fabio Baudrit, Universidad de Costa Rica, Apartado 183-4050, Alajuela, Costa Rica
2
Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, U.S.A.
3
Department of Biological Sciences, Kent State University, Kent, OH 44242, U.S.A.
4
Laboratorio de Histologı́a, Centro Agronómico Tropical de Investigación y Enseñanza, Apartado 7170 CATIE, Turrialba, Cartago 30501, Costa Rica

ABSTRACT
We examined structural and physiological traits relevant to the phenology of the tropical dry forest (TDF) pioneer tree Cochlospermum vitifolium. Despite marked
seasonality in rainfall, meristem activity occurred throughout the year. Leaves were produced almost continuously during the rainy season, while leaf shedding started
early during drought, before changes in soil water content were observed. Phenological activity under drought included flowering and fruiting of leafless trees;
bud break and shoot extension took place before the end of the dry season. Low wood density of C. vitifolium stems (0.17 g/cm3) and lignotubers (0.14 g/cm3)
provided water and starch storage needed to support phenological events such as branch extension, leaf flushing, and reproduction during the dry season, and probably
also contributed to survival following mechanical damage and fire, typical of early TDF successional stages. Lignotuber water and starch contents showed substantial
seasonal variation, declining from the beginning of the dry season to their lowest levels at the time of reproduction and dry-season flushing. Stems progressively
replaced lignotubers as main storage organs as tree size increased. Evidence for a role of water stores in buffering daily water deficits was weak. Leaf water potentials
remained above  1.2 MPa and stomatal conductance below 350 mmol/m2/s, suggesting that gas exchange during the rainy season was limited to prevent xylem
cavitation. Leaf shedding occurred when early-morning and mid-day CL converged at the rainy–dry season transition, without changes in lignotuber or soil water
content, suggesting that leaves of C. vitifolium are closely tuned to atmospheric drought.

Abstract in Spanish is available at http://www.blackwell-synergy.com/loi/btp

Key words: dry-season flushing; fire; pioneer species; reserve storage; stem-succulent; stomatal conductance; succession.

TROPICAL DRY FORESTS (TDFs) are among the most threatened
biomes in the world ( Janzen 1988b). Compared with their tropical
rain forest counterparts, TDFs contain a wealth of unique species
that exhibit higher structural and functional complexity, higher flo-
ristic endemism, slower growth and reproductive activity, higher
phenological diversity, and higher resilience to frequent distur-
bances (Murphy & Lugo 1986, Holbrook et al. 1995). Efforts to
restore these ecosystems will succeed if the underlying physiological
traits that influence successional patterns are understood. However,
in contrast to tropical rain forests (Bazzaz & Pickett 1980, Mulkey
et al. 1996), TDF succession remains little studied from an eco-
physiological perspective (see Leiva et al. in press-a, b).
As a consequence of human intervention, recurrent fire events,
windstorms, and other disturbances (Rawitscher 1948, Vareschi 1962,
Molina & Lugo 2006, Otterstrom et al. 2006), most TDF remnants
are mosaics of forest patches at different stages of succession (Kramer
1997, Otterstrom et al. 2006). Many TDF tree species are deciduous,
drought-tolerant, and include some of the most valuable timber, fruit,
and ornamental shrubs and trees in the world (Record & Hess 1949).
In this seasonally harsh environment, asynchrony of resource supply
and demand is the rule (Chapin et al. 1990), and thus resource storage
may play an important role among deciduous tree species.
Received 1 August 2008; revision accepted 12 March 2009.
5
Corresponding author; e-mail: surdo26@racsa.co.cr
104
Journal compilation r 2009 by The Association for Tropical Biology and Conservation
In the TDF of northwestern Costa Rica, recently burned, early
successional sites are dominated by a small number of light-
demanding, wind-dispersed species whose regeneration may be en-
hanced by fire (Ewel 1977, Otterstrom et al. 2006). Of the 215 tree
species reported at Santa Rosa National Park, 25 percent have
wind-dispersed seeds and are considered pioneer species ( Janzen
1988a). In an area of Santa Rosa last affected by fire in 1979, 12
species of trees constituted at least 90 percent of the vegetative cover
in 1986. Most of the wind-dispersed initial colonizers were large
trees, attaining heights of 15–25 m, and life spans of 50 to several
hundred years ( Janzen 1988a).
Cochlospermum vitifolium (Wildenow) Sprengel (Cochlosper-
maceae), a stem-succulent, dry-season deciduous tree, is distributed
from Mexico through northern South America. It is one of the most
abundant early successional species in TDFs, where it typically
grows as a small tree, but may reach up to 20 m in height in mature
forests. Cochlospermum vitifolium is wind-dispersed, reproduces
throughout the dry season when leafless, with the onset of repro-
ductive maturity occurring as early as the first year following ger-
mination (Bawa & Frankie 1983). Cochlospermum vitifolium is
often described as a dry-season flushing species because it initiates
leaf flushing before the onset of the rainy season (Borchert & Rivera
2001, Rojas-Jiménez et al. 2007). Nonannual reproduction is com-
mon in this species, the fruits develop rapidly throughout the dry
season, and variations in reproductive frequency among individuals
is high (Bullock 1995).
r 2009 The Author(s)

Cochlospermum vitifolium develops low-density stems (Dauben-
mire 1972, Borchert 1994) and prominent lignotubers that become
evident from the earliest stages of seedling development. A variety of
life forms exhibit lignotubers in the Brazilian cerrados (Rawitscher
1948), California chaparrales (Keeley & Zedler 1978), Chilean ma-
torrales (Montenegro et al. 1983), Mediterranean ecosystems (Cana-
dell & López-Soria 1998), and semidry forests of Panamá (Tyree &
Ewers 1996), where they can account for as much as 80 percent of
belowground and 40 percent of total-plant biomass. These lignotu-
bers are often important storage organs for carbohydrates, minerals,
water, and defensive compounds (Chapin et al. 1990) and may play
important roles in resprouting and recovering after disturbance
events such as mechanical damage, herbivory, and fire, by serving as
a source of meristems (Von Fircks & Sennerby-Forsee 1988, Rod-
gers et al. 1995). However, the role of these underground organs in
the life history of TDF pioneers establishing in highly degraded hab-
itats, their significance at different phenological and successional
stages, and their relative contribution as a storage organ have not
been explored in these seasonally dry forests.
In this study, we describe the phenological behavior and the
water relations of C. vitifolium trees growing in the TDF of Santa
Rosa National Park, Guanacaste, Costa Rica, in relation to seasonal
changes in water availability. We present anatomical and physio-
logical evidence showing that the stems and lignotubers of this spe-
cies contain significant quantities of water and starch that sustain
respiration, the production of flowers, fruits and seeds during the
dry season, and the renewal of vegetative growth before the begin-
ning of the subsequent rainy season.
METHODS
STUDY SITE AND VEGETATION.—The study was conducted in the
TDF of Santa Rosa, Guanacaste, Costa Rica (10152 0 N, 85134 0 W;
285 m asl) from September 1999 to November 2000. Mean annual
rainfall is 1528 mm, with a pronounced dry season extending from
mid-December to mid-May. Mean annual air temperature is 281C
with relatively little annual variation. Precipitation, daily mean air
temperature, and wind speed during the study period were moni-
tored at the field site using automated sensors operated under the
control of a datalogger (model CR10X, Campbell Scientific,
Logan, UT, U.S.A.).
The study site is part of a patch of the park where the vegeta-
tion is typical of early successional stages of the TDF. According to
historical records at Santa Rosa National Park, the study site rep-
resents an early stage of TDF succession (ca 8 ha; 10150 0 N, 85136 0
W), located on a relatively flat and accessible terrain, under contin-
uous regeneration since the last fire episode in 1988. The soil is a
shallow Entisol with some vertisolic characteristics that results in
soil cracking during the dry season. Soil texture was medium to
fine, fertility and hydraulic conductivity were low, rocky outcrops
were abundant, and frequent waterlogging occurs during the rainy
season, indicating that the bedrock impeded water percolation. Soil
water content at the field site was measured with a time domain
reflectometer (model 1502B, Tektronics, Beaverton, OR, U.S.A.)
at two depths: 0–15 and 15–30 cm. Volumetric water content was
Ecophysiology of Cochlospermum vitifolium 105
computed according to the universal soil equation (Topp et al.
1980).
The woody vegetation present in 1 ha within the 8 ha study
site was surveyed at the beginning of the study. Cochlospermum vi-
tifolium made up 19 percent of the stems counted. Other abundant
tree and shrub species were Curatella americana (Dilleniaceae,
17%), Genipa americana (Rubiaceae, 13%), Gliricidia sepium
(Fabaceae, 10%), Byrsonima crassifolia (Malpigiaceae, 9.5%), Semi-
alarium mexicana (Celastraceae, 7%), Acacia spp. (Cesalpinaceae,
9%), Rhedera trinervis (Verbenaceae, 8.5%), and Roupala montana
(Proteaceae, 2%). Other perennial trees and shrubs species com-
prised 5 percent of the individuals surveyed. All of these species are
typical of early TDF successional stages ( Janzen 1988a).
ABOVEGROUND PHENOLOGY.—A group of 30 C. vitifolium trees were
randomly selected within the 8 ha study area to monitor their
aboveground phenology. Selected trees varied in height from 1.32
to 9.20 m. Aboveground tree phenology was evaluated every 2 wk
using a semiquantitative method (Fournier 1974, Rojas-Jiménez
et al. 2007), which assigns a value of 0–4 depending on the presence
and intensity of a particular phenological event. This scale assigns
0 in complete absence of the phenological stage, 1 if the stage
is present between 1 and 25 percent, 2 if present between 26 and 50
percent, 3 if present between 51 and 75 percent, and 4 if present
between 76 and 100 percent of the tree crown. We monitored
four phenological events: leaf flushing, leaf shedding, flowering,
and fruiting. The same method was applied to all phenological
events.
STEM AND LIGNOTUBER DIMENSIONS.—The relations between the
volume of the lignotubers, tree height, and stem volume of C. vi-
tifolium trees were evaluated in 45 individuals whose height ranged
from 0.35 to 6 m. These trees represent a parallel set of individuals
selected on the basis of their height, to cover most of the range in
size observed in the study area. Tree height and diameter at the base
and top of the stem were measured using a clinometer and a diam-
eter tape, respectively. Stem height and diameters measured at
10 cm aboveground and at the tree apical tip (ca 5.5 mm) were used
to calculate stem volume. To measure the weight and volume of the
lignotubers, 15 trees representing a range of sizes were excavated at
three different times during the year: early dry season (29 Decem-
ber 1999), mid-dry season (29 January 2000), and late dry season
(29 April 2000); the last sampling coincided with the onset of dry-
season flushing. The roots were wrapped in plastic in the field and
placed in a cooler to avoid dehydration, and transported to the lab-
oratory where their weight was measured using a balance (model
Sartorius 210S, Sartorius, Goettingen, Germany). The volume of
the lignotubers was measured using the Archimedes principle (Gi-
menez & Alvez 1994), according to which the weight of an object
immersed in water is proportional to the volume of that object, so
that the weight of the submerged lignotubers corresponded to their
volume.
ANATOMICAL OBSERVATIONS.—To determine the starch content in
lignotubers and stems, samples of parenchyma tissue were obtained
106 Fallas-Cedeño et al.

from excavated individuals. For lignotubers and stems, three alyzed using piece-wise regression and nonlinear regression proce-
different positions were sampled (basal, medial, and apical) at dures of JMP (SAS Institute 2001), respectively.
three depths. The samples were fixed in a solution of formalde-
hyde-acetic acid-alcohol, and later dehydrated in a series of ethanol
RESULTS
solutions of increasing concentration (301C to absolute). The sam-
ples were then infiltrated with resin (Technovit 7100, Heraeus,
MICROCLIMATIC CONDITIONS.—Conditions prevailing during the
Boadilla, Madrid, Spain) and cut in a sliding microtome (model
study, from September 1999 to November 2000, which encom-
Shandon-AS 325 Retraction, Miami, FL, U.S.A.) to produce sec-
passed one complete phenological cycle, were characterized by
tions 4–7 mm thick. The sections were stained with Schift–naph-
strong seasonality in rainfall and soil water content (Fig. S1). Mean
thol–blue/black to reveal the presence of starch. The sections were
air temperature was 251C and varied about 61C during the year,
examined and photographed using a light microscope (model
with the maximum (28–291C) occurring near the end of the dry
Nikon microphot FX, Nikon, Melville, NY, U.S.A.) at a magnifi-
season. Low-velocity winds characterized the rainy season, but dry
cation of  4.
season initiation coincided with a strong increase in the speed of
trade winds (Fig. S1). Soil water content was significantly lower
during the dry season at both depths sampled, especially in upper
LEAF WATER RELATIONS.—Early-morning (leaves collected before
soil layers (0–15 cm; F = 4.14, P o 0.05; Fig. S1). Water potential
0800 h) and mid-day leaf water potential (CL) was determined
of shallow soil layers was lower than  1.5 MPa during most of the
during the year of observation using a pressure chamber (model
dry season. In deeper soil layers, water potential declined only at the
PMS-100, PMS, Corvallis, OR, U.S.A.), following the procedures
end of the dry season (Fig. 1). Soil water content also decreased in
described by Ritchie and Hinckley (1975). Four young, fully ex-
late July as a consequence of a short period of low rainfall and
panded leaves per tree were obtained from ten trees. The leaves were
higher wind speed.
sampled from branches pointing to each cardinal point, enclosed in
plastic bags immediately before excision, transferred to a cooler,
and kept sealed in the dark for no more than 2 h before CL mea- ABOVEGROUND PHENOLOGY.—Most phase changes of the above-
surements were recorded. ground phenology of C. vitifolium occurred during the dry season,
Measurements of stomatal conductance ( gS) were obtained us- in a synchronized and rapid fashion (Fig. 1). Leaf shedding started
ing a steady-state porometer (model LI-1600, Li-Cor, Lincoln, NE,
U.S.A.) at approximately the same dates when CL measurements
were conducted. Measurements were conducted at 0600, 0900,
1100, 1300, and 1500 h on four fully expanded sun leaves per tree
from five trees. All gS measurements were obtained from fully ex-
posed sun leaves.

WATER CONTENT OF LIGNOTUBERS.—Water content of lignotubers

was measured gravimetrically on a parallel set of samples obtained
according to the procedure described above for root starch observa-
tions. At times when no root excavations were scheduled, at least
five samples were obtained using an increment borer from partially
exposed lignotubers. The fresh samples were weighed in an analyt-
ical balance (model Sartorius 210S), oven-dried at 701C for at least
72 h to obtain their dry weight.

STATISTICAL ANALYSES.—Multivariate analyses of variance using gen-

eral linear models of SAS (SAS Institute, Cary, NC, U.S.A.; Little
et al. 1992) were conducted to determine whether there were sig-
nificant differences between variables measured during different
phenological and climatic stages. For contrast analyses and analyses
of variance for repeated measurements through time (Potvin et al.
FIGURE 1. Phenology of 30 Cochlospermum vitifolium trees growing in the dry
1990), the date was taken as a fixed repeated measure and the rep-
forest of Santa Rosa, Costa Rica, evaluated every 2 wk using a semiquantitative
licates were nested within the treatments. Average values of CL, gS,
method (Fournier 1974), from September 1999 to November 2000. Each point
and lignotuber water content for individual trees were analyzed as
represents the median. The upward bar is the third quartile and the downward
nested sampling designs to avoid pseudo-replication. The relations
bar is the first quartile. Vertical shades indicate the length of the dry season.
between lignotuber volume and stem height and volume were an-

before the end of the rainy season in both 1999 and 2000, under
conditions of rainfall and high soil water content (Fig. 1). It inten-
sified after mid-November and all trees at the study site were leafless
by the end of February 2000. There were two low-intensity flushing
events recorded during the dry season, but these leaves were shed
before reaching full expansion and were not recorded as a shedding
event. Cochlospermum vitifolium behaved as a dry season-flushing
tree (Daubenmire 1972, Holbrook et al. 1995, Rojas-Jiménez et al.
2007), and resumption of meristematic activity occurred near the
end of the dry season, when shoot extension and leaf flushing be-
came evident (Fig. 1). Flushing started approximately 3 wk before
the onset of the rains, and continued throughout the rainy season
(Fig. 1). Leaf production ceased in November in both 1999 and
2000, and coincided with the differentiation of apical flower buds.
Flowering and fruiting during the 1999/2000 dry season were
scarce; both processes occurred in o 25 percent of the tree crown,
and only after leaf shedding had been completed (Fig. 1).
LEAF WATER RELATIONS.—Leaf water potential (CL) of C. vitifolium
trees differed significantly within a sampling day (early morning
and mid-day hours), and between sampling dates (F = 4.14,
P o 0.05), but remained higher than  1.2 MPa throughout the
year (Fig. 2). Overall, mid-day CL values were significantly lower
than early morning values (Fig. 2). The lowest CL values were mea-
sured in old leaves during the dry season 1999/2000, when early
morning and mid-day CL converged at values lower than –1 MPa
FIGURE 2. Mean leaf water potential (CL) and stomatal conductance ( gs) of
Cochlospermum vitifolium trees sampled at different times during the phenolog-
ical cycle. Each point is the mean  SE of four leaves sampled from ten trees.
Leaf gs values are averages of measurements conducted at 0600, 0900, 1100,
1300, and 1500 h on four fully expanded sun leaves per tree from five trees.
Discontinuity in the time axis during the dry season indicates absence of leaves
in deciduous trees. Vertical shades indicate the length of the dry season.
Ecophysiology of Cochlospermum vitifolium 107
just before leaf shedding. Similar values were observed in fully ex-
panded leaves during a low-rainfall period in the middle of the
rainy season (Fig. 2). In contrast, highest CL values (4 –0.7 MPa)
were recorded in young leaves at the beginning of the rainy season
of year 2000.
Stomatal conductance ( gS) did not show diurnal fluctuations,
but varied significantly between sampling dates (F = 15.6,
P o 0.0001; Fig. 2). Stomatal conductance declined throughout
the 1999/2000 dry season, which coincided with leaf senescence
(Fig. 2). Conversely, young leaves showed moderate gS values dur-
ing the rainy season of year 2000 (o 350 mmol/m2/s). Lower gS
values were measured on 20 July 2000, during a short period with
low rainfall (Fig. 2).
STORAGE OF WATER AND STARCH IN STEMS AND LIGNOTUBERS.—The
relation between lignotuber volume and tree height differed for the
range of tree sizes examined (0.12–6 m). Piece-wise regression re-
vealed that the relationship was different for young treelets (seed-
lings and samplings) and adult trees (P o 0.001). Lignotuber
volume varied from 0.8 to 6.0 mL in treelets o 0.25 m, to almost
1.4 L in 6-m-tall trees (Fig. 3). As lignotuber volume increased to
approximately 0.5 L, tree height also increased up to 2 m, but then
tree height increased more slowly (Fig. 3). In contrast, as lignotuber
volume increased, stem volume grew exponentially (F = 210,
P o 0.001; Fig. 3), so that in the tallest trees examined (3.6 m),
stem volume significantly surpassed lignotuber volume. Piece-wise
regression analysis provided a general equation to describe the re-
lationship between these two variables where:
Tree height = 0.831510.2019  ln(lignotuber volume)  seed-
ling10.00043  lignotuber volume  adult. If lignotuber vol-
ume o 500, then seedling = 1 and adult = 0; otherwise seedling = 0
and adult = 1, R2 = 0.94. Stem volume is also a function of ligno-
tuber volume where:
Stem volume ¼ 42:618e0:00673lignotuber volume ðR 2 ¼ 0:94Þ:
Lignotuber water content varied approximately 60 percent
during the year, declining from 0.75 to 0.8 g/cm3 during the rainy
months to o 0.5 g/cm3 near the end of the dry period (Fig. S2),
when dry-season flushing started. Microscopic examination of
lignotuber and stem tissues of C. vitifolium revealed abundant
starch reserves, which fluctuated substantially during the climatic
and phenological cycles (Fig. 4). Lignotubers and stems sampled in
late December 1999 at the end of the rainy season and near the time
of leaf shedding (Fig. 4) contained abundant starch reserves in pa-
renchyma cells. In contrast, samples collected on late April 2000
during dry-season flushing (Fig. 4) contained much lower amounts
of starch.
DISCUSSION
RESOURCE STORAGE AND PHENOLOGY IN C. VITIFOLIUM.—Seasonal
asynchrony of resource supply and demand (Chapin et al. 1990) is
the rule for plants in TDF ecosystems. We expected storage to play
an important role in this deciduous species. We also expected large
108 Fallas-Cedeño et al.

the rainy to the dry season, before changes in soil or lignotuber wa-
ter content became perceptible, indicating reduced CL recovery
during the night. Although leaf shedding has been explained as a
photoperiodic response to decreasing day-length (Borchert & Ri-
vera 2001), it is also possible that these trees show high vulnerability
to cavitation, so that the mechanism for tuning leaf phenology to
atmospheric drought may reside in the leaf itself (Brodribb et al.
2003, Gutiérrez-Soto et al. 2008). Furthermore, these mechanisms
may act synergistically with changes in leaf physiology triggered by
day length, influencing the ways in which leaves respond to increas-
ing atmospheric evaporative demand. Further experimental work in
this and other species is needed to understand the contribution of
internal and external factors in triggering leaf senescence.
Large-diameter vessels (Fig. 4) and low-density wood observed
in C. vitifolium stems would probably result in high vulnerability to
cavitation (Hacke et al. 2001). The maintenance of relatively high
CL (4 –1.2 MPa) and low gS (o 350 mmol/m2/s) during the day

FIGURE 3. Relations between the volume of lignotubers, tree height, and stem
volume in 45 Cochlospermum vitifolium trees. Log-transformed data are shown.
Models are: Tree height = 0.831510.2019  ln(lignotuber volume)  seed-
ling 1 0.00043  lignotuber volume  adult. If lignotuber volume o 500,
then seedling = 1 and adult = 0; otherwise seedling = 0 and adult = 1;
R2 = 0.94. Stem volume = 42.618e0.00673  lignotuber volume. R2 = 0.94.

variations in lignotuber water and starch reserves, and argued that

those variations are likely attributed to internal plant resource reg-
ulation rather than environmentally driven by variations in resource
supply because plants can control more tightly resource demand
than supply. Both expectations were met.
Our results indicate that the phenology displayed by C. vi-
tifolium in the TDF of Santa Rosa is possible because structural and
functional traits involved in resource storage are highly developed.
Resource-demanding phenological events of C. vitifolium can occur
during drought because succulent stems and lignotubers store the
resources required for dry season reproduction and flushing. Con-
sistent with other studies on stem-succulent trees (Braun 1984,
Chapotin et al. 2006c), lignotuber and stem starch storage de-
creased as active growth was resumed, so that minimum starch con-
tent was observed during dry-season leaf flushing. Other studies
show that root reserves are higher in deciduous trees that flush
leaves in the dry season, when massive drops in starch reserves are
observed (Würth et al. 2005), and that reproductive phenology
seems to have a lesser effect on reserve mobilization than dry-season
FIGURE 4. Seasonal variations in starch content in lignotubers and stems of
leaf production (Newell et al. 2002).
Cochlospermum vitifolium trees. Cross sections ( 4) of lignotuber and stem
Phenological responses to drought in stem-succulent trees like
tissues showing starch grains, sampled on 29 December 1999 at the end of the
C. vitifolium are conservative (Holbrook et al. 1995, Chapotin et al.
rainy season and on 23 April during the dry-season flushing of leaves at the end
2006a, b, c), so that CL remained high while leaves were present
of the dry season of 1999. Isolated, wide xylem vessels scattered among abundant
and stem water content was high during most of the year. Cochlos-
radial parenchyma cells rich in (dark) starch grains are observed.
permum vitifolium sheds leaves rapidly during the transition from

and at different times of the year (Fig. 2) suggests that water storage
in succulent stems and lignotubers did not significantly buffer di-
urnal changes in water availability (see Chapotin et al. 2006a, b, c).
Instead, C. vitifolium water reserves were used mostly to sustain
dry-season leaf production and reproduction. Even succulent trees
invest little in water storage, because this function implies a trade-
off with the benefits obtained from more favorable, alternative al-
location patterns (Chapin et al. 1990), so that the amount of water
stored in succulent stems and lignotubers is very limited relative to
daily total transpiration (Goldstein et al. 1998, Holbrook 1995,
Chapotin et al. 2006a, b, c). In C. vitifolium, low water loss rates of
dry-season flushed leaves (Fig. 2) (Brodribb et al. 2003, Chapotin
et al. 2006a, Rojas-Jiménez et al. 2007) and flowers (Chapotin et al.
2003) contributed to compensate this limitation.
There are large amounts of mucilage in various organs of
C. vitifolium, including the flowers, which may function as extra-
cellular sources of water (Morse 1990, Chapotin et al. 2003 and
references therein). This water could be accessed at times of short-
age or in the occurrence of major phenological events such as
dry-season flushing, as indicated by the decline in lignotuber
(Fig. S2) and stem water content observed as the dry season pro-
gressed and phenological development continued (Daubenmire
1972, Borchert 1994, Chapotin 2006a, c). Previous results
(Daubenmire 1972) show that C. vitifolium trees experience major
increments in stem diameter during the rainy season and later
shrink during dry-season flowering and leaf flushing, consistent
with the withdrawal of stored water to support dry-season pheno-
logical activities.
The observed relations between lignotuber volume and stem
height and stem volume (Fig. 3) suggest that the lignotubers are
more important as storage organs during early stages of tree growth
(up to 2 m height). Lower-density lignotuber tissue (0.14 g/cm3)
comparatively allocated a larger proportion of its volume to water
and starch storage than stems. However, in taller plants (4 2 m)
lignotubers apparently grow less and become progressively replaced
as storage organs by light-wood stems that grow rapidly in height
and diameter. The development of massive light-wood (0.17 g/cm3)
succulent stems (Fig. 3) rich in mucilage (Chapotin et al. 2003),
water (Fig. S2), starch (Fig. 4), and chemical defenses (Xenofonte de
Almeida et al. 2005), coupled to leaf shedding during early drought,
allows C. vitifolium trees to temporarily store resources for growth,
reproduction, and maintenance under drought.
Although the anatomical nature of lignotubers has been the
subject of some dispute (Canadell & López-Soria 1998), our ob-
servations indicate that the underground organs of C. vitifolium are
thickened roots (Fig. 4). However, their presence among the veg-
etation of the TDF and its functional significance in other succulent
species and successional stages remain unknown. Other studies that
show the importance of root storage in water-limited environments
(Schenk & Jackson 2002) confirm that starch is a main substrate
stored in stems and coarse roots (Newell et al. 2002, Barbaroux
et al. 2003, Würth et al. 2005) and that root storage is highly dy-
namic, reaching highest values when drought represses growth
and shedding causes resorbtion of leaf materials (Latt et al. 2001,
Newell et al. 2002).
Ecophysiology of Cochlospermum vitifolium 109
PHENOLOGY DURING EARLY TDF SUCCESSION.—Numerous dry-sea-
son-flushing trees thrive in Santa Rosa TDF (Daubenmire 1972,
Borchert & Rivera 2001, Rojas-Jiménez et al. 2007) and intense
phenological activity under drought is common in other dry eco-
systems as well (Rawitscher 1948; Murali & Sukumar 1993, 1994;
Chapotin et al. 2006a, b, c). Reproduction after leaf shedding may
facilitate the localization of flowers by pollinators and the realloca-
tion of resources to support fruit and seed development ( Janzen
1967, Frankie et al. 1974, Van Schaik et al. 1993).
Dry-season leaf flushing may serve as a mechanism to escape
from herbivory (Aide 1988, 1992; Murali & Sukumar 1993), re-
duce the leaching of minerals from young leaves exposed to strong
rainfall (Monasterio & Sarmiento 1976), or out-compete potential
shading neighboring trees. Dry-season flushing in C. vitifolium
would presumably allow young cohorts of leaves to establish chem-
ical and structural defenses to confront herbivores, whose popula-
tions typically increase at the beginning of the rainy season. Leaves
expanded during drought would also enter the rainy season with
fully developed cuticles capable of preventing nutrient losses from
the foliage (Monasterio & Sarmiento 1976).
Irrespective of the origin of the vegetation that currently dom-
inates the early stages of Santa Rosa TDF succession, and the con-
troversy over the prevalence of fire as a natural ecological factor in
this ecosystem (Vareschi 1962, Otterstrom et al. 2006), pioneer
TDF trees such as C. vitifolium display a unique set of structural
and physiological traits that distinguish them from their wet forest
counterparts. These include unusual reproductive precocity (seed-
lings younger than 1 yr may flower in nursery bags), wind-dispersed
seeds (to an extent shared with rainier counterparts), conservative
water use, drought-deciduous phenology, fire tolerance, dry-season
leaf flushing and reproduction, and low-density stems and lignotu-
bers capable of storing large amounts of mucilage, water, and or-
ganic reserves. Coping with seasonal drought and frequent fires may
rather constitute essential attributes for successful establishment
and reproduction in TDFs.
ACKNOWLEDGMENTS
This research was supported by the Andrew W. Mellon Foundation
program on Terrestrial Ecology. We thank the Research Depart-
ment of Area de Conservación Guanacaste for allowing us to con-
duct the fieldwork in Santa Rosa National Park. J. Arias helped
with the statistical analyses.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online
version of this article:
FIGURE S1. Environmental conditions prevailing at the field site
in Santa Rosa, Costa Rica, during the study period, from Septem-
ber 1999 to November 2000. Vertical shades indicate the length of
the dry season. Dotted lines show water content between field ca-
pacity (–0.33 MPa) and –1.5 MPa.
110 Fallas-Cedeño et al.
FIGURE S2. Gravimetric water content of lignotubers sampled at
several occasions during the phenological cycle. Each value is the
mean  SE of at least five samples of lignotuber tissue. Vertical
shades indicate the length of the dry season.
Please note: Wiley-Blackwell Publishing are not responsible for the
content or functionality of any supporting materials supplied by the
authors. Any queries (other than missing material) should be di-
rected to the corresponding author for the article.
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