do the phenology and functional stem attributes of woody species

7/28/2019 Do the Phenology and Functional Stem Attributes of Woody Species

1/12

O RI G I N A L P A P E R

Do the phenology and functional stem attributes of woody speciesallow for the identification of functional groups in the semiarid

region of Brazil?

Andre Luiz Alves de Lima Everardo Valadares de Sa Barretto Sampaio

Cibele Cardoso de Castro Maria Jesus Nogueira Rodal

Antonio Celso Dantas Antonino Andre Laurenio de Melo

Received: 4 June 2011/ Revised: 17 February 2012/ Accepted: 5 May 2012 / Published online: 24 May 2012

Springer-Verlag 2012

Abstract The phenology of tree species in environments

that are subject to strong climatic seasonality is mainlydetermined by water availability, which may vary as a

function of wood density. The relationship among phe-

nology, water potential, wood density and the capacity of

water storage in the stem were determined for woody

species of caatinga vegetation (dry forest) in the semiarid

region of NE Brazil. Leaf flush and fall, flowering and

fruiting events were recorded over a 31-month period, and

the water potential was measured over a two-year period.

These data were related to precipitation, water availability

in the soil and photoperiod. Seven deciduous species

exhibited low wood density (DLWD,\0.5 g cm-3), high

capacity of water storage in the stem (until 250 % of the

dry weight) and high water potential during the year, as

opposed to 15 deciduous species that showed high wooddensity (DHWD, C0.5 g cm-3). Leaf flush, flowering and

the fruiting of DHWD species were related to precipitation,

whereas these phenological events occurred at the end of

the dry season and/or the beginning of the rainy season for

DLWD species and were related to the photoperiod. The

two evergreen species showed variations of water potential

that were intermediate between those of DHWD and

DLWD deciduous species, leaf flush during the dry season

and flowering at the end of dry season. These results sug-

gest the existence of three functional groups: evergreen

species, DHWD deciduous species and DLWD deciduous

species.

Keywords Caatinga Dry forest Flushing

Photoperiod Water potential Wood density

Introduction

Phenology is of great importance for the assessment of

ecosystems because the production of leaves, flowers and

fruits is closely related to several biotic and abiotic factors

(Rathcke and Lacey 1985). These phenological events

occur during the rainy season for most species in season-

ally dry forests of the tropics (Bullock and Sols-Magall-

anes 1990; Bach 2002; McLaren and McDonald 2005)

because the development of vegetative and reproductive

structures depends on water availability. However,

regardless of the rainy season, plants can obtain water from

the soil or use water previously accumulated in plant tis-

sues (Borchert 1994a; Holbrook et al. 1995; Frederic et al.

2005; Elliott et al. 2006). In these forests, some species

develop deep root systems (Mooney et al. 1995; Holbrook

Communicated by H. Pfanz.

A. L. A. de Lima (&) A. L. de Melo

Universidade Federal Rural de Pernambuco (UFRPE), Unidade

Academica de Serra Talhada (UAST), Fazenda Saco s/n, Caixa

Postal 063, 56900-000 Serra Talhada, Pernambuco, Brazil

e-mail: [email protected]

E. V. de Sa Barretto Sampaio A. C. D. Antonino

Centro de Tecnologia, Departamento de Energia Nuclear,

Universidade Federal de Pernambuco (UFPE), Av. Prof. Lus

Freire 1000, Cidade Universitaria, 50740-540 Recife,Pernambuco, Brazil

C. C. de Castro

Universidade Federal Rural de Pernambuco, Unidade

Academica de Garanhuns, Avenida Bom Pastor, s/n-Boa Vista,

55296-901 Garanhuns, Pernambuco, Brazil

M. J. N. Rodal

Departamento de Biologia/Area de Botanica, Universidade

Federal Rural de Pernambuco (UFRPE), Rua Dom Manoel de

Medeiros s/n, Dois Irmaos, 52171-900 Recife, Pernambuco,

Brazil

123

Trees (2012) 26:16051616

DOI 10.1007/s00468-012-0735-2


2/12

et al. 1995) or store water in their stems and root tissues

(Barbosa 1991; Borchert 1994a; Rivera et al. 2002).

Plants are subject to strong water stress in seasonally dry

environments, making their hydraulic systems subject to

cavitation (Hacke et al. 2001). Consequently, plants have

developed several adaptive mechanisms to adjust to this

condition, such as variations in wood density. High wood

density and thick cell walls protect plants from cavitation,but they cause low water storage in stem tissues. Con-

versely, low wood density and thin cell walls increase the

chances of cavitation (Sobrado 1993; Stratton et al. 2000;

Hacke et al. 2001; Reich et al. 2003; Bunker et al. 2005;

Swenson and Enquist 2007; Chave et al. 2009). However,

water storage may be higher, and the maintenance of a high

water potential may be longer (Hacke et al. 2001; Mark-

esteijn and Poorter 2009). These differences related to

water availability may result in different phenological

patterns (Holbrook et al. 1995).

The interaction between phenological and physiological

aspects is not well understood for many seasonally dryenvironments (Holbrook et al. 1995), especially in the

caatinga, a dry forest that occupies approximately thou-

sand km2 in NE Brazil, near the equator. The caatinga is

characterized by low and erratic precipitation and high

potential evapotranspiration and is located at the driest

portion of the distribution of deciduous forests (Sampaio

1995). Only a few studies related to plant phenology in the

caatinga currently exist (e.g., Barbosa et al. 1989; Pereira

et al. 1989; Machado et al. 1997; Griz and Machado 2001;

Amorim et al. 2009). All of them consider precipitation to

be the trigger factor of phenological events, despite the

presence of some species that exhibit the beginning of

phenological events during the dry season.

A recent study (Lima and Rodal 2010) investigated the

relationship between phenology and wood density of

caatinga species and verified the existence of three groups

of species: (1) deciduous species with high wood density,

whose phenological events were directly related to pre-

cipitation; (2) deciduous species with low wood density,

whose phenological events started before the rainy season,

and (3) evergreen species exhibiting high wood density,

whose phenology did not have any direct relationship with

precipitation. It is possible that the phenological differ-

ences between these species are related to distinct patterns

of variation in water potential throughout the year, but

there have been no studies on this topic for caatinga spe-

cies. These types of studies also remain scarce for other dry

forests (Reich and Borchert 1984; Borchert 1994a, b;

Holbrook et al. 1995), and no research has studied condi-

tions as dry as those of the caatinga.

The aim of this study is to verify the relationship among

precipitation, wood density, water potential and phenology

in woody species of caatinga vegetation. The hypotheses

are: (1) water potential of species with low wood densities

is high throughout the year (aside from the long duration of

the dry season and the extreme conditions of water loss),

and the production of leaves and flowers is not directly

dependent on precipitation; (2) the water potential of the

species with high wood density falls sharply during the dry

season, and the phenophases are controlled by precipita-

tion; and (3) similar to species with low wood density, thewater potential of evergreen species is high throughout the

year, but these plants store low levels of water in their

stems, and the occurrence of their phenophases is similar to

those of species with low wood density.

Materials and methods

The study was conducted at the Experimental Station

Lauro Bezerra (785900000S, 3881901600 W), belonging to the

Company of Pernambuco Agricultural Research, munici-

pality of Serra Talhada, Pernambuco state. The Station is500 to 700 m tall. Predominantly, luvisols (stony phase)

and lithic eutrophic neosolis (Jacomine et al. 1973) are

present. The annual mean precipitation is approximately

650 mm, with broad variations over time, and the mean

temperature is approximately 26 C, with slight variations

over time (Melo 1988). Precipitation data from April 2007

to October 2009 (Fig. 1) were obtained from the National

Institute of Space Researchs Web site (http://www6.cptec.

inpe.br/proclima/). Photoperiod data were calculated based

on the geographical coordinates, using the formulas pro-

vided by Lammi (2008).

During the first year of the study, the dry season was very

long, continuing from April 2007 to January 2008, and the

precipitation was only 156 mm (Fig. 1). In 2008 and 2009,

the annual precipitation was more than 800 mm (Fig. 1). In

2008, 75 % of the precipitation occurred in February and

March,and in 2009, 90 % wasconcentratedbetween January

and May. The annual variation of the photoperiod was

approximately 55 min (Fig. 1); the days with the shortest

(1132 hours) and the longest (1227 hours) photoperiods

occurred in June and December, respectively (Lammi 2008).

The density of trees and shrubs with stem perime-

ters[9 cm at soil level was recorded as being 3,690 plants/

ha, the mean basal area was 20.5 m2 ha-1, the canopy was

between 4 and 5 m high, and the emergent individuals ran-

ged between 9 and 10 m high (Farias, unpublished data).

Wood density was determined for three individuals from

24 species that presented higher values of importance in the

community (phytosociological data in Ferraz et al. 1998,

Table 1). From each individual, stems or branches with at

least 3 cm diameter were collected (Barbosa and Ferreira

2004). The disks, including bark and wood, were obtained

on the same day during the rainy season. They were

1606 Trees (2012) 26:16051616

123
http://www6.cptec.inpe.br/proclima/http://www6.cptec.inpe.br/proclima/http://www6.cptec.inpe.br/proclima/http://www6.cptec.inpe.br/proclima/


3/12

saturated in water for 3 days, weighed (Msat) and placed in

water again to determine their volume (Trugilho et al.

1990). They were then dried at 103 C until they reached a

constant weight (MS). The basic wood density (D g cm-3)

and the amount of saturated water (QAsat %) were calcu-

lated following Borchert (1994a): D = MS/volume and

QAsat = 100 (Msat-MS)/MS. The classification of species

with respect to wood density followed Borchert (1994a):

low-density species were those whose wood density was

less than 0.5 g cm-3, while high-density species were

those with values up to and including 0.5 g cm-3. The

relation between wood density and capacity of water

Fig. 1 Accumulated monthly

precipitation and mean monthly

photoperiod of Serra Talhada

municipality, Pernambuco state,

Brazil

Table 1 Species studied in relation to phenology, water potential and wood density, with respective family name and dispersal mode (anemo

anemochorous, auto autochorous and zoo zoochorous) in Serra Talhada, Pernambuco state, Brazil

Species Number of individuals Family Dispersal modes

Amburana cearensis (Allemao) A.C.Sm. 15 Fabaceae Anemo

Anadenanthera colubrina (Vell.) Brenam 11 Fabaceae Auto

Aspidosperma pyrifolium Mart. 11 Apocynaceae Anemo

Bauhinia cheilantha (Bong.) Steud. 12 Fabaceae Auto

Combretum pisonioides Taub. 2 Combretaceae Anemo

Commiphora leptophloeos (Mart.) Gillet. 13 Burseraceae Zoo

Croton blanchetianus Baill. 12 Euphorbiaceae Auto

Croton rhamnifolioides Pax and K. Hoffm. 12 Euphorbiaceae Auto

Cynophalla flexuosa (L.) J. Presl 12 Capparaceae Zoo

Jatropha mollissima (Pohl) Baill. 9 Euphorbiaceae Auto

Licania rigida Benth. 2 Chrysobalanaceae Zoo

Manihot epruinosa Pax & K. Hoffm. 13 Euphorbiaceae Auto

Mimosa ophtalmocentra Mart. ex Benth. 15 Fabaceae Auto

Myracrodruon urundeuva Allemao 13 Anacardiaceae Anemo

Piptadenia stipulacea (Benth.) Ducke 9 Fabaceae Auto

Poincianella pyramidalis (Tul.) L. P. Queiroz 21 Fabaceae Auto

Pseudobombax marginatum (A. St.-Hil., Juss., & Cambess.) A. Robyns 15 Malvaceae Anemo

Rollinia leptopetala R. E. Fr. 12 Annonaceae Zoo

Sapium glandulosum (L.) Morong 11 Euphorbiaceae Auto

Schinopsis brasiliensis Engl. 8 Anacardiaceae Anemo

Sebastiania macrocarpa Mull. Arg. 7 Euphorbiaceae Auto

Spondias tuberosa Arruda 11 Anacardiaceae ZooVarronia leucocephala (Moric.) J. S. Mill. 10 Boraginaceae Zoo

Ziziphus joazeiro Mart. 8 Rhamnaceae Zoo

Trees (2012) 26:16051616 1607

123


4/12

storage in the stem was tested using the Spearman corre-

lation test (Zar 1996).

Water potential was also measured in the 24 species

whose wood density was evaluated, except in Schinopsis

brasiliensis and Combretum pisonioides, which were rep-

resented only by plants with high canopies making it

unpractical to collect samples. Three individuals, other

than those used for wood density evaluations, were used foreach species, except for L. rigida, represented by the only

two individuals in the area. Samples of terminal branches

measuring 10 cm in length were collected monthly during

the pre-dawn period (between 0400 and 0530 hours) from

September 2007 to August 2009. Water potential was

measured with a Sholander pressure chamber (Borchert

1994a). Branches were chosen for this analysis because

many species had no leaves during the dry season. To avoid

water loss by the collected branches, the branches were

placed into plastic bags immediately after cutting, stored in

a cooler and processed within 2 h after sampling (Borchert

1994a). Measurements were taken to the maximum valueof 4.5 MPa which was the pressure limit that the Scho-

lander chamber could stand. This limit implies an under-

estimation of the lower values of water potential and it was

taken into account for the data interpretation.

Phenological data were collected in intervals of 15 days

for 264 individuals belonging to the 24 species, among

those present in an area of 1 ha, selected to have the

highest species diversity in the caatinga vegetation of the

station (Table 1). The number of plants of each species was

set at 11 or more, following the sample sizes suggested by

Frankie et al. (1974a) and Fournier and Charpantier (1975),

except when fewer that 11 were present in the area, in

which cases all present were measured. Leaf flush, leaf fall,

flowering (the presence of buds and/or flowers) and fruiting

(the presence of immature or mature fruits) were recorded

according to a semi-quantitative scale varying from zero to

100, with intervals of 25, and was used to describe the

percentual intensity of the phonological events (Fournier

1974). Dispersal syndromes were determined according to

the morphological criteria proposed by Van der Pijl (1982).

The data were analyzed in two ways. First, a multivar-

iate analysis (MANOVA) was performed to determine

groups of species with similar features with respect to the

following variables: water potential, wood density, capac-

ity of water storage in the stem, leaf flush, leaf fall, the

amount of leaves, flowering and fruiting. For this analysis,

the intensity of the phenophase was investigated (Fournier

1974). Due to the large amount of data for each species, a

factorial analysis was performed to reduce the number of

initial variables with the smallest possible loss of infor-

mation (Vicini and Souza 2005). Then, the MANOVA was

conducted using the SPSS (Statistical Package for the

Social Sciences) software. In the second analysis, a

Spearman correlation (Zar 1996) was used to evaluate the

relationship between biotic (water potential, leaf flush and

fall, flowering and fruiting) and abiotic (precipitation and

photoperiod) variables. Two analyses were carried out to

assess phenological events: one of the analyses used the

number of species that exhibited the phenophase, and

another used the intensity of the phenological event

(Fournier 1974) for each group of species.Finally, a variance analysis coupled with a Tukey test

(Zar 1996) was performed to compare water potential

among the species with low wood density, species with

high wood density and the evergreen species.

Results

Wood density and capacity of water storage in the stem

Wood density and the amount of water stored in saturated

wood were inversely correlated (rs = -0.80, p\ 0.0001,Fig. 2). Seven species exhibited low wood density and a

capacity for water storage higher than 100 % of their dry

weight. For some species, such as Commiphora lepto-

phloeos and Pseudobambax marginatum, this value was

more than 230 %. A total of 17 species showed high wood

density and a capacity for water storage that varied from 55

to 84 % of their dry weight.

Phenology

The seven species with low wood density were leafless

during the dry season and started flushing at the end of this

season. Therefore, they are deciduous with low wood

density (DLWD). The flush of 15 species with high wood

density that were also leafless during the dry season began

with the occurrence of rain (Fig. 3a, b), except for Mimosa

ophtalmocentra and Ziziphus joazeiro, who flushed at the

end of the dry season. Therefore, these 15 species are

deciduous with high wood density (DHWD). Z. joazeiro

lost its leaves gradually in the middle of the dry season and

showed leaf flush synchronously; flowers of this species

were produced at the end of the dry season, after the loss of

all the leaves. Two high wood density species, Cynophalla

flexuosa and Licania rigida, remained with leaves through

the dry season and are considered evergreen species

(Fig. 4).

The leaf flush of both DLWD and DHWD species had a

positive correlation with precipitation. For DHWD species,

this correlation was stronger (rs = 0.50; p\ 0.001) than

for DLWD species (rs = 0.31; p = 0.02). The leaf flush of

the DLWD species had a strong correlation with the

enhanced photoperiod (rs = 0.51; p\ 0.001), whereas

DHWD species did not exhibit this correlation.

1608 Trees (2012) 26:16051616

123


5/12

DLWD species not only produced leaves earlier than

DHWD species did (Fig. 3c) but also began to lose their

leaves before DHWD species did. DLWD species began

losing their leaves in the middle of the rainy season and

were leafless at the beginning of the dry season (Fig. 3c, d,

e). DHWD species maintained their leaves for a longer

period, and their leaves fell gradually during the dry season

(Fig. 3c).

Fig. 2 Mean wood density

(with standard deviations) and

quantity of water storage in

saturated wood (with standard

deviations), for each species, in

an area of the caatinga, Serra

Talhada municipality,

Pernambuco state, Brazil.

DLWD (seven species in the left

side of the figure) = deciduous

species with low wood density;

Black arrow: evergreen species.

DHWD (other species, except

the evergreen

ones) = deciduous species with

high wood density

Fig. 3 Vegetative phenological events of seven deciduous species

with low wood density (DLWD) and 15 deciduous species with high

wood density (DHWD) in Serra Talhada municipality, Pernambuco

state, Brazil. a and d intensity of phenophases; b and e proportion of

species in each phenophase; c proportion of leaves. Bar rainfall;

dotted line DLWD; continuous line DHWD

Trees (2012) 26:16051616 1609

123


6/12

Phenophase anticipation of DLWD species is reinforced

by the fact that leaf fall was also anticipated and occurred

during the same period through the years (Fig. 3d, e). It is

important to note that the falling of leaves in these species

had a positive correlation with precipitation (rs = 0.26;

p = 0.04), as opposed to the DHWD species, which

showed a negative correlation with precipitation (rs =

-0.29; p = 0.02).

Vegetative events in the two evergreen species did not

show an obvious pattern because leaf flush and fall

occurred at different periods of the year (Fig. 4a), although

leaf flush was more common in the dry season. Flowering

of C. flexuosa occurred during the dry season, and fruiting

occurred in the transition between the dry and rainy season

(Fig. 4b). Flowering of L. rigida also occurred in the dry

season but the number of observed plants (two) was too

small to allow any firm conclusion.

Flowering of DLWD species occurred in the transition

between the dry and rainy seasons or during the dry season,

whereas the flowering of DHWD species occurred only

during the rainy season (Fig. 5a, b), except for the species

Myracrodruon urundeuva, Ziziphus joazeiro, Mimosa

ophtalmocentra and Anadenanthera colubrina, which

showed some flowering individuals at the end of the dry

season. Flowering induction by precipitation in DHWD

species is indicated by the strong positive correlation

between these variables (rs = 0.56; p\ 0.001), as opposed

to the DLWD species, whose correlation was not signifi-

cant (rs = 0.02; p = 0.89).

The fruit production of DHWD and DLWD species

occurred continuously during the year (Fig. 5c, d) and

seemed to vary as a function of the dispersal syndrome(Fig. 5e, f). Five of the seven DLWD species, including

Spondias tuberosa and Commiphora leptophloeos, were

autochorous and zoochorous (Table 1) and produced fruits

at the end of the dry season or at the beginning of the rainy

season. However, the diaspores were dispersed only during

the rainy season. This phenological behavior of DLWD

species resulted in a high correlation between fruiting and

precipitation (rs = 0.60; p\ 0.001). Both DLWD species

that flowered at the beginning of the dry season and pro-

duced fruits soon afterward (Pseudobombax marginatum

and Amburana cearensis) were anemochorous.

The fruit production of DHWD species also presented acorrelation with precipitation (rs = 0.28; p = 0.02). Eight

out of 15 DHWD species were autochorous, and fruit

production tended to occur during the rainy season,

although some species, such as Poincianella pyramidalis

and Sebastiania macrocarpa, had fruits that were main-

tained in the plant during part of the dry season. Ziziphus

joazeiro, a zoochorous species, began to produce fruits at

the end of the dry season, but dispersion occurred during

the rainy season. Rollinia leptopetala, which is also zooc-

horous, produced and dispersed its fruits during the rainy

season. Among the anemochorous species, Myracrodruon

urundeuva and Aspidosperma pyrifolium produced fruits

during the dry season.

Water potential

The water potentials of the DHWD, DLWD and evergreen

species were different during the dry season and similar

during the rainy season (Table 2). The potential of the

DHWD species (Fig. 6) was positively correlated with

precipitation (rs = 0.60; p = 0.001). The water potential

of DLWD species was less variable during the year, always

higher than -0.5 MPa (Fig. 6), and independent of pre-

cipitation (rs = 0.13; p = 0.54).

Water stress during the dry season was so high for

DHWD species that the water potential of most of them

surpassed the measuring capacity of the pressure camera

(-4.5 Mpa). Even considering their water potential in these

occasions as the limit of the chamber (which certainly

overestimated the true values) the potentials in the dry

season were clearly lower than than those of DLWD and

evergreen species (Fig. 6). The number of DHWD species

with water potentials of less than -4.5 MPa varied from

Fig. 4 Leaf flush and fall a and flowering and fruiting b of two

evergreen species in Serra Talhada municipality, Pernambuco state,

Brazil

1610 Trees (2012) 26:16051616

123


7/12

one to ten species (average of 8) between September and

January (dry time).

Similar to DHWD species, evergreen species demon-

strated a positive correlation between water potential and

precipitation (rs = 0.58; p\ 0.01; Fig. 6). However, the

variation in water potential of these species during the year

was lower than that recorded for DHWD species.

Groups of species

The species were separated into two main groups: one

group was composed of high wood density species, and the

other was composed of low wood density species, except

for Spondias tuberosa, which was considered a sister group

of the high wood density species (Fig. 7). Although this

species had low wood density, it showed phenological and

physiological features similar to those of low wood density

species, so it was treated within this group. We discuss this

species in more detail below. The group of high wood

density species included both deciduous and evergreen

species, in spite of their differences in phenological events.

Discussion

Vegetative events

It was possible to identify three groups of species that

exhibited strong relationships with water potentials, wooddensities, water storage capacity in the stem tissues and

phenology. Species with high wood density were divided

into two groups, deciduous (DHWD species) and evergreen

species. The third group was that of deciduous low wood

density (DLWD) species These same basic groups have

been registered in studies developed in other dry tropical

forests (Borchert 1994a; Rivera et al. 2002). However, the

proportions of species and plants in the vegetation com-

munity belonging to each group seem to differ among

Fig. 5 Reproductive events of 7 deciduous species with low wood

density (DLWD) and 15 deciduous species with high wood density(DHWD) in Serra Talhada municipality, Pernambuco state, Brazil.

a and c intensity of the phenophases; b and d proportion of species in

each phenophase; e and f number of species for each dispersal mode

Trees (2012) 26:16051616 1611

123


8/12

forests (Borchert 1994a; Borchert et al. 2002). In our area,

most of the species (62 %) belong to the DHWD species

group and they comprise 82 % of the trees in the com-

munity (while evergreens were represented by only two

species, comprising 2 % of the trees in the community.

Caatinga is the driest of dry tropical forests, with its low

and erratic rainfall coupled to a very high potential

evapotranspiration, Therefore, water limitation seems to

restrict the presence of evergreens to a higher degree than

the other groups and it seems to favor the selection of

species with high wood density that resist to high negative

pressures in their xylems (Hacke et al. 2001).

The inclusion of Spondias tuberosa as a sister group of

the DHWD species in the grouping analysis may have

occurred because of its relatively high wood density

(0.49 g.cm-3). However, its phenological and physiologi-

cal behaviors were very similar to those of the DLWDspecies. The high capacity of this species to store water

within its root tissues (Cavalcanti and Resende 2006) may

explain these results.

The DLWD species had morphological and phenologi-

cal characteristics similar to those of the Dlight species

mentioned by Borchert (1994a), with similar water storage

capacity in the stem tissue (average of 193 % of the stem

dry weight) and high water potentials ([-0.5 MPa). To

Borchert (1994a) water storage capacity is one of the main

determinants of plant functional types in tropical dry for-

ests. The high capacity of DLWD species to store water in

their stems and their tendency to produce leaves at the endof the dry season and at the beginning of the rainy season

and to lose leaves during the rainy season led to certain

questions: (1) Why do DLWD species begin to produce

leaves during the dry season?; (2) Why do DLWD species

begin to lose leaves during the rainy season?; (3) If DLWD

species have large amounts of stored water, why do they

not produce new leaves after their leaves fall?; and (4) Why

do DLWD species begin to produce leaves only at the end

of the dry season?

There are two answers to the first question (that are not

mutually exclusive) related to the attainment of water and

evolutionary strategy. Plants need water (Holbrook et al.

1995), which can be obtained in three ways: (a) root growth

and exploitation of underground water (Mooney et al.

1995; Borchert 1994a; Holbrook et al. 1995; Pratt et al.

2007; Jackson et al. 2007), which is not commonly

observed in DLWD species (Chapotin et al. 2006; Hol-

brook et al. 1995); (b) from dew through leaf absorption

(Breshears et al. 2008; Munne-Bosch 2010), which is

impossible because the plants did not have leaves during

this period; and (3) from plant tissues (Daubernmire 1972;

Reich and Borchert 1982; 1984; Borchert 1994a; Borchert

and Rivera 2001), which is the most plausible possibility.

Chapotin et al. (2006) confirmed that DLWD species may

use stored water to produce new leaves and that leaf flush

at the end of the dry season would be advantageous

because plants could enjoy the sporadic rains that occur

during this period.The second explanation is related to

evolutionary strategy, i.e., plant species would be selected

to begin their flush at the end of the dry season to avoid or

to minimize injuries made by herbivores (van Schaik et al.

1993; Coley and Barone 1996; Chapotin et al. 2006; Sloan

et al. 2006).

Table 2 Results of the analysis of variance of water potential

between deciduous species with low wood density, deciduous species

with high wood density and evergreen species during the dry (Sep-

tember 2007 to January 2008 and August 2008 to January 2009) and

rainy (February to July 2008 and 2009) seasons in Serra Talhada

municipality, Pernambuco state, Brazil

Dry period Rain period

Months F Months F

September 16.937*** February 4.999*

October 8.809** March 5.037*

November 3.081 April 5.037*

December 15.527*** May 1.170

January 22.905*** June 1.408

August 13.537*** July 1.408

September 19.502*** February 1.752

October 12.059*** March 3.332

November 12.337*** April 2.847

December 10.248** May 4.839*

January 19.451

***

June 2.574July 6.264**

*** P\0.001, ** P\0.01, * P\ 0.05

Fig. 6 Mean water potential (with standard deviations) of deciduous

species with low wood density (seven species, 21 plants) and high

wood density (13 species, 39 plants) and evergreen species (two

species, five plants) in Serra Talhada municipality, Pernambuco state,

Brazil. (Average standard devation: DHDW = -1.3 MPa;

EHWD = -0.49 MPa; DLWD = -0.1 MPa)

1612 Trees (2012) 26:16051616

123


9/12

The answer to the second question is related to a strat-

egy used to avoid water loss during the dry season and

water storage when water is abundant. Another explanation

is that plants store large amounts of water during the rainy

season, allowing leaf flush and/or flowering to occur at the

end of the dry season. If this is true, it would be more

advantageous to lose leaves at the end of the rainy season

and at the beginning of the dry season, avoiding excessive

water loss (Borchert and Rivera 2001; Borchert et al.2002). This is the most plausible explanation, and it shows

the importance of the maintenance of a large quantity of

water within stem tissues, similar to what was observed in

this study.

The third question follows the same logic as the second

one. If DLWD plants flush during the rainy season, they

expose their leaves to the long dry season and, thus, lose

large quantities of water that they would not be able to

replace during the same season. This occurrence could

result in a collapse of vascular bundles due to embolism

(Sobrado 1993; Chave et al. 2009).

The fourth question seems to be related to several eco-

logical factors. It would be more advantageous to flush

leaves at the end of the dry season because the rainy season

would be closer, and water used for the production and

maintenance of new leaves, flowers and fruits could be

replaced in a relatively short period of time (Rivera et al.

2002; Elliott et al. 2006). Additionally, the mature leaves,in which photosynthesis is more efficient, would already be

produced at the beginning of the rainy season, and photo-

synthetic gain would be maximized during this short period

(Rivera et al. 2002; Elliott et al. 2006).

How do plants recognize the end of the dry season?

Several studies discuss this question (Borchert and Rivera

2001; Rivera and Borchert 2001; Rivera et al. 2002;

Borchert et al. 2004; Chapotin et al. 2006; Sloan et al.

2006; Calle et al. 2010). Plant species would be selected to

Fig. 7 Dendrogram showing

the relationships among species

in Serra Talhada municipality,

Pernambuco state, Brazil, based

on values of wood density,

capacity of water storage in the

stem, water potential, leaf flush

and fall, quantity of leaves,

flowering and fruiting. The top

group includes species with

high wood density (except

Spondias tuberosa), while the

lower group includes species

with low wood density

Trees (2012) 26:16051616 1613

123


10/12

initiate their vegetative and reproductive activities when

induced by a photoperiod enhance that occur at the end of

the dry season. This seems to be the only environmental

aspect that does not vary over the years, occurring on a

regular basis (Rivera et al. 2002). This explanation is

supported by the strong coincidence between photoperiod

enhancement and the occurrence of phenological events

and also by the regularity of these events, which alwaysoccur during the same period of the year. However, there

are no studies that test this hypothesis for caatinga species.

Only experimental studies would allow more consistent

support for this hypothesis.

As opposed to what was observed for DLWD species,

DHWD species presented phenological behavior and

morpho-functional features that were directly related to

precipitation. Leaf flush occurred at the beginning of the

rainy season, except in Ziziphus joazeiro and Mimosa

ophtalmocentra. These species were classified as DHWD

(having limited capacity to store water). A possible

explanation for obtaining water could be the growth of theroot system (Frederic et al. 2005) or water storage within

the root system (Jackson et al. 2007). At the end of the dry

season, Ziziphus joazeiro lost its leaves completely.

Afterward, leaf flush and flowering began synchronously

between individuals. This phenological behavior fits the

pattern described by Borchert (2000) for brevideciduous

species, which lose their leaves for some weeks at the end

of the dry season and then sprout and flower afterwards.

Some researchers (Daubernmire 1972; Reich and Borchert

1982; Borchert 1994a) explain that old leaves have reduced

stomatic control, and consequently, the quantity of water

lost through evapotranspiration is larger than that absorbed

by the roots. When the plant loses its leaves completely, it

reduces water loss, and root absorption becomes positive.

The plant thereby rehydrates itself and can flush leaves and

flowers during the dry season.

The continuous leaf flush observed in DHWD species

during the rainy season suggests that these plants are active

when there is water in the soil, as opposed to what was

observed in DLWD species, which showed reduced leaf

flush and the falling of their leaves even under high water

potential (i.e., with water availability in the plant tissues)

during the rainy season.

The water potential of DHWD species showed wide

variation during the year (Ackerly 2004; Bucci et al. 2004),

influencing leaf flush and fall (Borchert 1994a, b, c). Leaf

flush in these plants occurred continuously during the rainy

season and diminished when the precipitation became

scarce; then, the leaves began to fall, probably as a strategy to

minimize water loss. According to Borchert (1994a), falling

leaves in DHWD species may occur as a function of varia-

tions of water status, and water status may vary with water

availability in the soil, which varies across microhabitats.

The water potential of DHWD species diminished

gradually during the dry season to acquire the water in the

soil; when water became scarce, the plant lost its leaves

(Borchert 1994a). Therefore, the minimum water potential

of DHWD species is an important predictor of water

availability in the soil, contrary to what was observed for

DLWD species, in which the water potential was not cor-

related to water availability in the soil.

Reproductive events

The occurrence of flowering at the end of the dry season

and beginning of the rainy season, as observed in DLWD

species, has been commonly recorded in areas of season-

ally dry forests (Frankie et al. 1974a; Borchert 1994a;

Holbrook et al. 1995). Plants that produce flowers at the

end of the dry season would enjoy a reduction in the

competition for pollinators (Frankie et al. 1974b) because

the number of flowering species is lower during this time

than it is during the rainy season. Additionally, Janzen(1967) and van Schaik et al. (1993) suggested that many

plants do not grow leaves during the dry season, which

attracts pollinators. Although DLWD species do not com-

pose a large group of species in the area, they are eco-

logicaly important because they provide floral resources in

the dry season.

The flowering period is of great importance for the

reproductive success of plants (Rathcke and Lacey 1985).

It may therefore be directly related to dispersal syndromes,

as was observed in the anemochoric species in the study

area. This species tend to produce flowers at the end of the

rainy season and produce fruits during the dry season,

which is favorable for diaspore dispersal (Lampe et al.

1992) because when most species do not grow leaves,

obstacles to dispersion are diminished (Lampe et al. 1992),

and the stronger wind can carry diaspores larger distances

(Morellato 1995). However, species that produce flowers

and fruits during the dry season, such as Amburana cear-

ensis and Pseudobombax marginatum, store water within

their tissues or must have a deep root system capable of

reaching sub-soil water. Contrary to anemochoroic species,

autochorous species tend to produce fruits during the rainy

season. Some authors suggest that many autochorous spe-

cies need water to release disapores (Griz and Machado

2001). Plants that produce flowers at the end of the dry

season, such as the zoochorous Spondias tuberosa and

Commiphora leptophloeos, produce fruits at the end of the

dry season; their seeds can be dispersed when the rainy

season begins. This strategy allows seeds to be dispersed

when water is available, favoring seedling establishment

(Rathcke and Lacey 1985). Generally, zoochoric species

tend to disperse their seeds during the rainy season, when

the availability of dispersers is high (Morellato 1995).

1614 Trees (2012) 26:16051616

123


11/12

Generally, it is observed that, independent of wood

density, the time production of fruits varies according to

the dispersal mode. However, species that begin fruit

production during the dry season must have water available

to support the physiological changes and, in the case of

DLWD species, the water may come from the reserves

stored in the stem.

Conclusions

Strong rain seasonality seems to constitute a selective

pressure that determines the evolution of species with dif-

ferent phenological and physiological strategies related to

water availability in the soil or water stored in plant tissues.

Such features influence wood density and water potential.

Species with low wood density are capable of flush inde-

pendent of rain and exhibit high water potential throughout

the year, as opposed to species with high wood density,

which directly depend on precipitation. These results sug-gest that the phenology of species with low wood density is

induced by the photoperiod and that not only rainfall but

also water potential, wood density and water storage

capacity are important factors in determining phenological

events in low rainfall areas. DLWD species, although not

abundant in the area, are ecologically important because

they provide floral resources in the dry season.

Acknowledgments We thank the Empresa Pernambucana de Pes-

quisa Agropecuaria (IPA) for its support during the field work and the

Brazilian National Research Council (CNPq) and the State of Per-

nambuco Research Council (FACEPE-Fundacao de Amparo a Cien-

cia e Tecnologia do Estado de Pernambuco) for their financialsupport. This study is part of the first authors PhD thesis.

References

Ackerly DD (2004) Functional strategies of chaparral shrubs in

relation to seasonal water deficit and disturbance. Ecol Monogr

74:2544. doi:10.1890/03-4022

Amorim IL, Sampaio EVSB, Araujo EL (2009) Fenologia de especies

lenhosas da caatinga do Serido, RN. Revista Arvore 33:491499.

doi:10.1590/S0100-67622009000300011

Bach CS (2002) Phenological patterns in monsoon rainforests in the

northern territory, Australia. Austral Ecol 27:477489. doi:

10.1046/j.1442-9993.2002.01209.xBarbosa DCA (1991) Crescimento de Anadenanthera macrocarpa

(Benth.) Brenan (LeguminosaeMimosoideae). Phyton 52:5162

Barbosa RI, Ferreira CAC (2004) Densidade basica da madeira de um

ecossistema de campina em Roraima, Amazonia brasileira.

Acta Amazonica 34:587591. doi:10.1590/S0044-5967200

4000400010

Barbosa DCA, Alves JLH, Prazeres SM, Paiva AMA (1989) Dados

fenologicos de 10 especies arboreas de uma area de Caatinga

(AlagoinhaPE). Acta Botanica Brasilica 3:109117

Borchert R (1994a) Soil and stem water storage determine phenology

and distribution of tropical dry forest trees. Ecology

75:14371449. doi:10.2307/1937467

Borchert R (1994b) Water status and development of tropical trees

during seasonal drought. Trees 8:115125. doi:10.1007/BF00

196635

Borchert R (1994c) Induction of rehydration and bud break by

irrigation or rain in deciduous trees of a tropical dry forest in

Costa Rica. Trees 8:198204. doi:10.1007/BF00196847

Borchert R (2000) Organismic and environmental controls of bud

growth in tropical trees. In: Viemont JD, Crabbe J (eds)

Dormancy in plants: from whole plant behavior to cellular

control. CAB International, Wallingford, pp 87107

Borchert R, Rivera G (2001) Photoperiodic control of seasonal

development and dormancy in tropical stem suculent trees. Tree

Physiol 21:213221. doi:10.1093/treephys/21.4.213

Borchert R, Rivera G, Hagnauer W (2002) Modification of vegetative

phenology in a tropical semi-deciduous forest by abnormal

drought and rain. Biotropica 34:2739. doi:10.1111/j.1744-7429.

2002.tb00239.x

Borchert R, Meyer SA, Felger RS, Porter-Bolland L (2004)

Environmental control of flowering periodicity in Costa Rican

and Mexican tropical dry forests. Glob Ecol Biogeogr

13:409425. doi:10.1111/j.1466-822X.2004.00111.x

Breshears DD, McDowell NG, Goddard KL, Dayem KE, Martens SN,

Meyer CW, Brown KM (2008) Foliar absorption of intercepted

rainfall improves woody plant water status most during drought.

Ecology 89:4147. doi:10.1890/07-0437.1

Bucci SJ, Goldstein G, Meinzer FC, Scholz FG, France AC,

Bustamante M (2004) Functional convergence in hydraulic

architecture and water relations of tropical savanna trees: from

leaf to whole plant. Tree Physiol 24:891899. doi:10.1093/

treephys/24.8.891

Bullock SH, Sols-Magallanes JA (1990) Phenology of canopy trees

of a tropical deciduous forest in Mexico. Biotropica 22:2235.

doi:10.2307/2388716

Bunker DE, DeClerck F, Bradford JC, Colwell RK, Perfecto I,

Phillips OL, Sankaran M, Naeem S (2005) Species loss and

aboveground carbon storage in a tropical forest. Science

310:10291031. doi:10.1126/science.1117682

Calle Z, Schlumpberger BO, Piedrahita L, Leftin A, Hammer SA, Tye

A, Borchert R (2010) Seasonal variation in daily insolation

induces synchronous bud break and flowering in the tropics.

Trees-Struct Funct. doi: 10.1007/s00468-010-0456-3

Cavalcanti NB, Resende GM (2006) Ocorrencia de xilopodio em

plantas nativas de imbuzeiro. Caatinga 19:287293

Chapotin SM, Razanameharizaka JH, Holbrook NM (2006) Baobab

trees (Adansonia) in Madagascar use stored water to flush new

leaves but not to support stomatal opening before the rain season.

New Phytol 169:549559. doi:10.1111/j.1469-8137.2005.01618.x

Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE

(2009) Towards a worldwide wood economics spectrum. Ecol

Lett 12:351366. doi:10.1111/j.1461-0248.2009.01285.x

Coley JD, Barone JA (1996) Herbivory and plant defenses in the

tropical forests. Annu Rev Ecol Syst 27:305335. doi:10.1146/

annurev.ecolsys.27.1.305

Daubernmire R (1972) Phenology and other characteristics of tropicalsemi-deciduous forest in north-western Costa Rica. J Ecol

60:147170. doi:10.2307/2258048

Elliott S, Baker JP, Borchert R (2006) Leaf flushing during the dry

season: the paradox of Asian monsoon forests. Glob Ecol

Biogeogr 15:248257. doi:10.1111/j.1466-8238.2006.00213.x

Ferraz EMN, Rodal MJN, Sampaio EVSB, Pereira RCA (1998)

Composicao florstica em trechos de vegetacao de caatinga e

brejo de altitude na regiao do Vale do Pajeu, Pernambuco.

Revista Brasileira de Botanica 21:715. doi:10.1590/S0100-

84041998000100002

Fournier LA (1974) Un metodo cuantitativo para la medicion de

caractersticas fenologicas en arboles. Turrialba 24:422423

Trees (2012) 26:16051616 1615

123
http://dx.doi.org/10.1890/03-4022http://dx.doi.org/10.1590/S0100-67622009000300011http://dx.doi.org/10.1046/j.1442-9993.2002.01209.xhttp://dx.doi.org/10.1590/S0044-59672004000400010http://dx.doi.org/10.1590/S0044-59672004000400010http://dx.doi.org/10.2307/1937467http://dx.doi.org/10.1007/BF00196635http://dx.doi.org/10.1007/BF00196635http://dx.doi.org/10.1007/BF00196847http://dx.doi.org/10.1093/treephys/21.4.213http://dx.doi.org/10.1111/j.1744-7429.2002.tb00239.xhttp://dx.doi.org/10.1111/j.1744-7429.2002.tb00239.xhttp://dx.doi.org/10.1111/j.1466-822X.2004.00111.xhttp://dx.doi.org/10.1890/07-0437.1http://dx.doi.org/10.1093/treephys/24.8.891http://dx.doi.org/10.1093/treephys/24.8.891http://dx.doi.org/10.2307/2388716http://dx.doi.org/10.1126/science.1117682http://dx.doi.org/10.1007/s00468-010-0456-3http://dx.doi.org/10.1111/j.1469-8137.2005.01618.xhttp://dx.doi.org/10.1111/j.1461-0248.2009.01285.xhttp://dx.doi.org/10.1146/annurev.ecolsys.27.1.305http://dx.doi.org/10.1146/annurev.ecolsys.27.1.305http://dx.doi.org/10.2307/2258048http://dx.doi.org/10.1111/j.1466-8238.2006.00213.xhttp://dx.doi.org/10.1590/S0100-84041998000100002http://dx.doi.org/10.1590/S0100-84041998000100002http://dx.doi.org/10.1590/S0100-84041998000100002http://dx.doi.org/10.1590/S0100-84041998000100002http://dx.doi.org/10.1111/j.1466-8238.2006.00213.xhttp://dx.doi.org/10.2307/2258048http://dx.doi.org/10.1146/annurev.ecolsys.27.1.305http://dx.doi.org/10.1146/annurev.ecolsys.27.1.305http://dx.doi.org/10.1111/j.1461-0248.2009.01285.xhttp://dx.doi.org/10.1111/j.1469-8137.2005.01618.xhttp://dx.doi.org/10.1007/s00468-010-0456-3http://dx.doi.org/10.1126/science.1117682http://dx.doi.org/10.2307/2388716http://dx.doi.org/10.1093/treephys/24.8.891http://dx.doi.org/10.1093/treephys/24.8.891http://dx.doi.org/10.1890/07-0437.1http://dx.doi.org/10.1111/j.1466-822X.2004.00111.xhttp://dx.doi.org/10.1111/j.1744-7429.2002.tb00239.xhttp://dx.doi.org/10.1111/j.1744-7429.2002.tb00239.xhttp://dx.doi.org/10.1093/treephys/21.4.213http://dx.doi.org/10.1007/BF00196847http://dx.doi.org/10.1007/BF00196635http://dx.doi.org/10.1007/BF00196635http://dx.doi.org/10.2307/1937467http://dx.doi.org/10.1590/S0044-59672004000400010http://dx.doi.org/10.1590/S0044-59672004000400010http://dx.doi.org/10.1046/j.1442-9993.2002.01209.xhttp://dx.doi.org/10.1590/S0100-67622009000300011http://dx.doi.org/10.1890/03-4022


12/12

Fournier LA, Charpantier C (1975) El tamano de la muestra y la

frequencia de las observaciones en el estudio de las caracterist-

icas fenologicas de los arbores tropicales. Turrialba 25:4548

Frankie GW, Baker HG, Opler PA (1974a) Comparative phenological

studies of trees in tropical lowland wet and dry forest in the

lowlands of Costa Rica. J Ecol 62:881913

Frankie GW, Baker HG, Opler PA (1974b) Tropical plant phenology:

applications for studies in community ecology. In: Lieth H (ed)

Phenology and seazonality modeling. Springer-Verlag, Berlim,

pp 287296

Frederic CD, Goudiaby VA, Gimenez O, Diagne AL, Diouf M,

Rocheteau A, Akpo LE (2005) Environmental influence on

canopy phenology in the dry tropics. For Ecol Manage

215:319328. doi:10.1016/j.foreco.2005.05.022

Griz LMS, Machado ICS (2001) Fruiting phenology and seed

dispersal syndromes in caatinga, a tropical dry forest in the

northeast of Brazil. J Trop Ecol 17:303321. doi:10.1017/

S0266467401001201

Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001)

Trends in wood density and structure are linked to prevention of

xylem implosion by negative pressure. Oecologia 126:457461.

doi:10.1007/s004420100628

Holbrook NM, Whitbeck JL, Mooney HA (1995) Drought responses

of Neotropical dry forest trees. In: Bullock SH, Mooney HA,

Medina E (eds) Seasonally dry tropical forests. Cambridge

University Press, Cambridge, pp 243276

Jackson RB, Pockman WT, Hoffmann WA, Bleby TM, Armas C

(2007) Structure and function of root systems. In: Pugnaire FI,

Valladares F (eds) Functional Plant Ecology, 2nd edn. CRC

Press (Taylor & Francis Group), USA, pp 151173

Jacomine PKT, Cavalcanti AC, Burgos N, Pesso SCP, Silveira CO

(1973) Levantamento exploratorioreconhecimento de solos do

Estado de Pernambuco. Recife: EMBRAPADivisao de Pes-

quisa Pedologica, (Boletim Tecnico, 26Pedologia, 14), 28V

Janzen DH (1967) Synchronization of sexual reproduction of trees

within the dry season in Central America. Evolution 21:620637.

doi:10.2307/2406621

Lammi J (2008) Online photoperiod calculator. http://www.

nic.fi/*benefon/sun.php3. Accessed on 03 May 2010

Lampe MG, Bergeron Y, Mcneil R, Leduc A (1992) Seasonal

flowering and fruiting patterns in tropical semi-arid vegetation of

northeastern Venezuela. Biotropica 24:6476

Lima ALA, Rodal MJN (2010) Phenology and wood density of plants

growing in the semi-arid region of northeastern Brazil. J Arid

Environ 74:13631373. doi:10.1016/j.jaridenv.2010.05.009

Machado ICS, Barros LM, Sampaio EVSB (1997) Phenology of

caatinga at Serra Talhada, PE, northeastern Brazil. Biotropica

29:5768. doi:10.1111/j.1744-7429.1997.tb00006.x

Markesteijn L, Poorter L (2009) Seedling root morphology and

biomass allocation of 62 tropical tree species in relation to

drought- and shade-tolerance. J Ecol 97:311325. doi:10.1111/

j.1365-2745.2008.01466.x

McLaren KP, McDonald MA (2005) Seasonal patterns of flowering

and fruiting in a dry tropical forest in Jamaica. Biotropica37:584590. doi:10.1111/j.1744-7429.2005.00075.x

Melo N (1988) Areas de excecao da Paraba e dos Sertoes de

Pernambuco. SUDENE, PSU/SER, Recife: SUDENE (Serie de

estudos regionais, 19)

Mooney HA, Bullock SH, Medina E (1995) Introduction. In: Bullock

SH, Mooney HA, Medina E (eds) Seasonally dry tropical forests.

Cambridge University Press, Cambridge, pp 18

Morellato LPC (1995) Os frutos e a dispersao de sementes. In:

Morellato LPC, Leitao-Filho HF (eds) Ecologia e preservacao de

uma floresta tropical urbana: Reserva de Santa Genebra. Editora

da UNICAMP, Campinas, pp 6465

Munne-Bosch S (2010) Direct foliar absorption of rainfall water and

its biological significance in dryland ecosystems. J Arid Environ

74:417418. doi:10.1016/j.jaridenv.2009.09.001

Pereira RMA, Araujo-Filho JA, Lima RV, Paulho FDG, Lima AON,

Araujo ZB (1989) Estudo fenologico de algumas especies

lenhosas e herbaceas da caatinga. Ciencia Agronomica 20:1120

Pratt RB, Jacobsen AL, Ewers FW, Davis SD (2007) Relationships

among xylem transport, biomechanics and storage in stems and

roots of nine Rhamnaceae species of theCalifornia chaparral. New

Phytol 174:787798. doi:10.1111/j.1469-8137.2007.02061.x

Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial

plants. Annu Rev Ecol Syst 16:179214. doi:10.1146/annurev.

es.16.110185.001143

Reich PB, Borchert R (1982) Phenology and ecophysiology of the

tropical tree, Tabebuia neochrysantha (Bignoniaceae). Ecology

63:294299

Reich PB, Borchert R (1984) Water stress and tree phenology in a

tropical dry forest in the Lowlands of Costa Rica. J Ecol

72:6174. doi:10.2307/2260006

Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J,

Westoby M, Walters MB (2003) The evolution of plant

functional variation: traits, spectra, and strategies. Int J Plant

Sci 164:143164. doi:10.1086/374368

Rivera G, Borchert R (2001) Induction of flowering in tropical trees

by a 30-min reduction in photoperiod: evidence from field

observations and herbarium collections. Tree Physiologist

21:201212. doi:10.1093/treephys/21.4.201

Rivera G, Elliott S, Caldas LS, Nicolssi G, Coradin VTR, Borchert R

(2002) Increasing day-length induces spring flushing of tropical

dry forest trees in the absence of rain. Trees 16:445456. doi:

10.1007/s00468-002-0185-3

Sampaio EVSB (1995)Overviewof theBrazilian Caatinga.In: Bullock

SH, Mooney HA, Medina E (eds) Seasonally dry tropical forests.

Cambridge University Press, Cambridge, pp 3563

Sloan SA, Zimmerman JK, Sabat AM (2006) Phenology ofPlumeria

alba and its herbivores in a tropical dry forest. Biotropica

39:195201. doi:10.1111/j.1744-7429.2006.00249.x

Sobrado MA (1993) Trade-off between water transport efficiency and

leaf life-span in a tropical dry forest. Oecologia 96:1923. doi:

10.1007/BF00318025

Stratton L, Goldstein G, Meinzer FC (2000) Stem water storage

capacity and efficiency of water transport: their functional

significance in a Hawaiian dry forest. Plant Cell Environ

23:99106. doi:10.1046/j.1365-3040.2000.00533.x

Swenson NG, Enquist BJ (2007) Ecological and evolutionary

determinants of a key plant functional trait: wood density and

its community-wide variation across latitude and elevation. Am J

Bot 94:451459. doi:10.3732/ajb.94.3.451

Trugilho PF, Silva DA, Frazao FJL, Matos JLM (1990) Comparacao

de metodos de d eterminacao da densidade basica em madeira.

Acta Amazonica 20:307319

Van der Pijl L (1982) Principles of dispersal in higher plants.Springer, New York

Van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of

tropical forests: adaptive significance and consequences for

primary consumers. Annu Rev Ecol Syst 24:353377. doi:

10.1146/annurev.es.24.110193.002033

Vicini L, Souza AM (2005) Analise Multivariada da Teoria a Pratica.

UFSM, CCNE, Santa Maria

Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall, New

York

1616 Trees (2012) 26:16051616

123
http://dx.doi.org/10.1016/j.foreco.2005.05.022http://dx.doi.org/10.1017/S0266467401001201http://dx.doi.org/10.1017/S0266467401001201http://dx.doi.org/10.1007/s004420100628http://dx.doi.org/10.2307/2406621http://www.nic.fi/~benefon/sun.php3http://www.nic.fi/~benefon/sun.php3http://www.nic.fi/~benefon/sun.php3http://www.nic.fi/~benefon/sun.php3http://dx.doi.org/10.1016/j.jaridenv.2010.05.009http://dx.doi.org/10.1111/j.1744-7429.1997.tb00006.xhttp://dx.doi.org/10.1111/j.1365-2745.2008.01466.xhttp://dx.doi.org/10.1111/j.1365-2745.2008.01466.xhttp://dx.doi.org/10.1111/j.1744-7429.2005.00075.xhttp://dx.doi.org/10.1016/j.jaridenv.2009.09.001http://dx.doi.org/10.1111/j.1469-8137.2007.02061.xhttp://dx.doi.org/10.1146/annurev.es.16.110185.001143http://dx.doi.org/10.1146/annurev.es.16.110185.001143http://dx.doi.org/10.2307/2260006http://dx.doi.org/10.1086/374368http://dx.doi.org/10.1093/treephys/21.4.201http://dx.doi.org/10.1007/s00468-002-0185-3http://dx.doi.org/10.1111/j.1744-7429.2006.00249.xhttp://dx.doi.org/10.1007/BF00318025http://dx.doi.org/10.1046/j.1365-3040.2000.00533.xhttp://dx.doi.org/10.3732/ajb.94.3.451http://dx.doi.org/10.1146/annurev.es.24.110193.002033http://dx.doi.org/10.1146/annurev.es.24.110193.002033http://dx.doi.org/10.3732/ajb.94.3.451http://dx.doi.org/10.1046/j.1365-3040.2000.00533.xhttp://dx.doi.org/10.1007/BF00318025http://dx.doi.org/10.1111/j.1744-7429.2006.00249.xhttp://dx.doi.org/10.1007/s00468-002-0185-3http://dx.doi.org/10.1093/treephys/21.4.201http://dx.doi.org/10.1086/374368http://dx.doi.org/10.2307/2260006http://dx.doi.org/10.1146/annurev.es.16.110185.001143http://dx.doi.org/10.1146/annurev.es.16.110185.001143http://dx.doi.org/10.1111/j.1469-8137.2007.02061.xhttp://dx.doi.org/10.1016/j.jaridenv.2009.09.001http://dx.doi.org/10.1111/j.1744-7429.2005.00075.xhttp://dx.doi.org/10.1111/j.1365-2745.2008.01466.xhttp://dx.doi.org/10.1111/j.1365-2745.2008.01466.xhttp://dx.doi.org/10.1111/j.1744-7429.1997.tb00006.xhttp://dx.doi.org/10.1016/j.jaridenv.2010.05.009http://www.nic.fi/~benefon/sun.php3http://www.nic.fi/~benefon/sun.php3http://dx.doi.org/10.2307/2406621http://dx.doi.org/10.1007/s004420100628http://dx.doi.org/10.1017/S0266467401001201http://dx.doi.org/10.1017/S0266467401001201http://dx.doi.org/10.1016/j.foreco.2005.05.022

do the phenology and functional stem attributes of woody species

Documents