Trees (2012) 26:16051616 DOI 10.

1007/s00468-012-0735-2

ORIGINAL PAPER

Do the phenology and functional stem attributes of woody species allow for the identication of functional groups in the semiarid region of Brazil?
Luiz Alves de Lima Everardo Valadares de Sa Barretto Sampaio Andre Cibele Cardoso de Castro Maria Jesus Nogueira Rodal nio Celso Dantas Antonino Andre Laure nio de Melo Anto

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 mainly determined by water availability, which may vary as a function of wood density. The relationship among phenology, 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 ush and fall, owering 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
Communicated by H. Pfanz. A. L. A. de Lima (&) A. L. de Melo Universidade Federal Rural de Pernambuco (UFRPE), Unidade mica de Serra Talhada (UAST), Fazenda Saco s/n, Caixa Acade Postal 063, 56900-000 Serra Talhada, Pernambuco, Brazil e-mail: andrelimabotanica@yahoo.com.br Barretto Sampaio A. C. D. Antonino E. V. de Sa Centro de Tecnologia, Departamento de Energia Nuclear, s Universidade Federal de Pernambuco (UFPE), Av. Prof. Lu ria, 50740-540 Recife, Freire 1000, Cidade Universita Pernambuco, Brazil C. C. de Castro Universidade Federal Rural de Pernambuco, Unidade mica de Garanhuns, Avenida Bom Pastor, s/n-Boa Vista, Acade 55296-901 Garanhuns, Pernambuco, Brazil M. J. N. Rodal rea de Bota nica, Universidade Departamento de Biologia/A Federal Rural de Pernambuco (UFRPE), Rua Dom Manoel de os, 52171-900 Recife, Pernambuco, Medeiros s/n, Dois Irma Brazil

dry weight) and high water potential during the year, as opposed to 15 deciduous species that showed high wood density (DHWD, C0.5 g cm-3). Leaf ush, owering 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 ush during the dry season and owering at the end of dry season. These results suggest 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, owers 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 seasons-Magallally dry forests of the tropics (Bullock and Sol 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 tissues (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

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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. Conversely, 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; Markesteijn 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 dry environments (Holbrook et al. 1995), especially in the caatinga, a dry forest that occupies approximately thousand 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 veried the existence of three groups of species: (1) deciduous species with high wood density, whose phenological events were directly related to precipitation; (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 differences 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 species. 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 conditions 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 owers 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 precipitation; and (3) similar to species with low wood density, the water 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 (78590 0000 S, 388190 1600 W), belonging to the Company of Pernambuco Agricultural Research, municipality of Serra Talhada, Pernambuco state. The Station is 500 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 provided by Lammi (2008). During the rst 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 % was concentrated between 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 perimeters [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 ranged 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

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Trees (2012) 26:16051616 Fig. 1 Accumulated monthly precipitation and mean monthly photoperiod of Serra Talhada municipality, Pernambuco state, Brazil

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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 o) A.C.Sm. Amburana cearensis (Allema Anadenanthera colubrina (Vell.) Brenam Aspidosperma pyrifolium Mart. Bauhinia cheilantha (Bong.) Steud. Combretum pisonioides Taub. Commiphora leptophloeos (Mart.) Gillet. Croton blanchetianus Baill. Croton rhamnifolioides Pax and K. Hoffm. Cynophalla exuosa (L.) J. Presl Jatropha mollissima (Pohl) Baill. Licania rigida Benth. Manihot epruinosa Pax & K. Hoffm. Mimosa ophtalmocentra Mart. ex Benth. o Myracrodruon urundeuva Allema Piptadenia stipulacea (Benth.) Ducke Poincianella pyramidalis (Tul.) L. P. Queiroz Pseudobombax marginatum (A. St.-Hil., Juss., & Cambess.) A. Robyns Rollinia leptopetala R. E. Fr. Sapium glandulosum (L.) Morong Schinopsis brasiliensis Engl. ll. Arg. Sebastiania macrocarpa Mu Spondias tuberosa Arruda Varronia leucocephala (Moric.) J. S. Mill. Ziziphus joazeiro Mart. Number of individuals 15 11 11 12 2 13 12 12 12 9 2 13 15 13 9 21 15 12 11 8 7 11 10 8 Family Fabaceae Fabaceae Apocynaceae Fabaceae Combretaceae Burseraceae Euphorbiaceae Euphorbiaceae Capparaceae Euphorbiaceae Chrysobalanaceae Euphorbiaceae Fabaceae Anacardiaceae Fabaceae Fabaceae Malvaceae Annonaceae Euphorbiaceae Anacardiaceae Euphorbiaceae Anacardiaceae Boraginaceae Rhamnaceae Dispersal modes Anemo Auto Anemo Auto Anemo Zoo Auto Auto Zoo Auto Zoo Auto Auto Anemo Auto Auto Anemo Zoo Auto Anemo Auto Zoo Zoo Zoo

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

QAsat = 100 (Msat-MS)/MS. The classication 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

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storage in the stem was tested using the Spearman correlation 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 represented only by plants with high canopies making it unpractical to collect samples. Three individuals, other than those used for wood density evaluations, were used for each 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 value of 4.5 MPa which was the pressure limit that the Scholander chamber could stand. This limit implies an underestimation 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 ush, leaf fall, owering (the presence of buds and/or owers) 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 multivariate analysis (MANOVA) was performed to determine groups of species with similar features with respect to the following variables: water potential, wood density, capacity of water storage in the stem, leaf ush, leaf fall, the amount of leaves, owering 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 information (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 ush and fall, owering 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 leptophloeos 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 leaess during the dry season and started ushing at the end of this season. Therefore, they are deciduous with low wood density (DLWD). The ush of 15 species with high wood density that were also leaess during the dry season began with the occurrence of rain (Fig. 3a, b), except for Mimosa ophtalmocentra and Ziziphus joazeiro, who ushed 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 ush synchronously; owers 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 exuosa and Licania rigida, remained with leaves through the dry season and are considered evergreen species (Fig. 4). The leaf ush 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 ush 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.

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Trees (2012) 26:16051616 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 gure) = deciduous species with low wood density; Black arrow: evergreen species. DHWD (other species, except the evergreen ones) = deciduous species with high wood density

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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

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 leaess 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).

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Fig. 4 Leaf ush and fall a and owering and fruiting b of two evergreen species in Serra Talhada municipality, Pernambuco state, Brazil

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 ush and fall occurred at different periods of the year (Fig. 4a), although leaf ush was more common in the dry season. Flowering of C. exuosa 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 rm conclusion. Flowering of DLWD species occurred in the transition between the dry and rainy seasons or during the dry season, whereas the owering 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 owering 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 signicant (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 owered at the beginning of the dry season and produced fruits soon afterward (Pseudobombax marginatum and Amburana cearensis) were anemochorous. The fruit production of DHWD species also presented a correlation 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 maintained 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 zoochorous, 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 precipitation (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

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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

one to ten species (average of 8) between September and January (dry time). Similar to DHWD species, evergreen species demonstrated 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, wood densities, 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 community belonging to each group seem to differ among

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1612 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 (September 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 Months September October November December January August September October November December January F 16.937*** 8.809 3.081
**

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Rain period Months February March April May June July February March April May June July F 4.999* 5.037* 5.037* 1.170 1.408 1.408 1.752 3.332 2.847 4.839* 2.574 6.264**

15.527*** 22.905*** 13.537*** 19.502

***

12.059*** 12.337*** 10.248** 19.451***

*** 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, ve plants) in Serra Talhada municipality, Pernambuco state, Brazil. (Average standard devation: DHDW = -1.3 MPa; EHWD = -0.49 MPa; DLWD = -0.1 MPa)

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 community (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 physiological behaviors were very similar to those of the DLWD species. 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 phenological 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 forests. The high capacity of DLWD species to store water in their stems and their tendency to produce leaves at the end of 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 rst 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; Holbrook et al. 1995); (b) from dew through leaf absorption -Bosch 2010), which is (Breshears et al. 2008; Munne 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) conrmed that DLWD species may use stored water to produce new leaves and that leaf ush 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 ush 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).

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Trees (2012) 26:16051616 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 ush and fall, quantity of leaves, owering and fruiting. The top group includes species with high wood density (except Spondias tuberosa), while the lower group includes species with low wood density

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The answer to the second question is related to a strategy 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 ush and/or owering 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 ush 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 ecological factors. It would be more advantageous to ush 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, owers 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 efcient, would already be produced at the beginning of the rainy season, and photosynthetic 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

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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 always occur 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 ush occurred at the beginning of the rainy season, except in Ziziphus joazeiro and Mimosa ophtalmocentra. These species were classied as DHWD (having limited capacity to store water). A possible explanation for obtaining water could be the growth of the root 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 ush and owering began synchronously between individuals. This phenological behavior ts 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 ower 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 ush leaves and owers during the dry season. The continuous leaf ush 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 ush 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), inuencing leaf ush and fall (Borchert 1994a, b, c). Leaf ush 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 variations 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 correlated to water availability in the soil. Reproductive events The occurrence of owering 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 seasonally dry forests (Frankie et al. 1974a; Borchert 1994a; Holbrook et al. 1995). Plants that produce owers at the end of the dry season would enjoy a reduction in the competition for pollinators (Frankie et al. 1974b) because the number of owering 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 compose a large group of species in the area, they are ecologicaly important because they provide oral resources in the dry season. The owering 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 owers 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 owers and fruits during the dry season, such as Amburana cearensis 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 species need water to release disapores (Griz and Machado 2001). Plants that produce owers 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).

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1615 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 J (eds) growth in tropical trees. In: Viemont JD, Crabbe 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) Modication 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 owering 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 s-Magallanes JA (1990) Phenology of canopy trees Bullock SH, Sol xico. Biotropica 22:2235. of a tropical deciduous forest in Me 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 owering in the tropics. Trees-Struct Funct. doi: 10.1007/s00468-010-0456-3 dio em ncia de xilopo Cavalcanti NB, Resende GM (2006) Ocorre plantas nativas de imbuzeiro. Caatinga 19:287293 Chapotin SM, Razanameharizaka JH, Holbrook NM (2006) Baobab trees (Adansonia) in Madagascar use stored water to ush 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 tropical semi-deciduous forest in north-western Costa Rica. J Ecol 60:147170. doi:10.2307/2258048 Elliott S, Baker JP, Borchert R (2006) Leaf ushing 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) stica em trechos de vegetac o or o de caatinga e Composic a a , Pernambuco. o do Vale do Pajeu brejo de altitude na regia nica 21:715. doi:10.1590/S0100Revista Brasileira de Bota 84041998000100002 todo cuantitativo para la medicio n de Fournier LA (1974) Un me sticas fenolo gicas en a rboles. Turrialba 24:422423 caracter

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 different phenological and physiological strategies related to water availability in the soil or water stored in plant tissues. Such features inuence wood density and water potential. Species with low wood density are capable of ush independent 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 suggest 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 oral resources in the dry season.
Acknowledgments We thank the Empresa Pernambucana de Pes ria (IPA) for its support during the eld work and the quisa Agropecua Brazilian National Research Council (CNPq) and the State of Per` Cie n o de Amparo a nambuco Research Council (FACEPE-Fundac a cia e Tecnologia do Estado de Pernambuco) for their nancial support. This study is part of the rst authors PhD thesis.

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