functional groups of woody species in semi-arid regions at low latitudes

Functional groups of woody species in semi-arid regions atlow latitudes

CLEMIR CANDEIA DE OLIVEIRA,1* ROBERTA BOSCAINI ZANDAVALLI,1

ANDRÉ LUIZ ALVES DE LIMA2 AND MARIA JESUS NOGUEIRA RODAL3

1Graduate Course of Ecology and Natural Resources, Department of Biology, Federal University ofCeará – UFC, Building 906, Fortaleza, CE 60455-760, Brazil (Email: [email protected]), and2Academic Unit of Serra Talhada (UAST), Federal Rural University of Pernambuco -UFRPE, SerraTalhada, and 3Department of Biology, Botany, Federal Rural University of Pernambuco – UFRPE,Recife, PE, Brazil

Abstract In seasonally dry environments, woody species have different survival strategies. However, little isknown about how environmental variables affect the phenology and water dynamics of these species. We aim tounderstand which variables initiate the vegetative phenophases of species in a tropical semiarid climate at 3°Slatitude, where variation in photoperiod is minimal and rainfall is seasonal. We hypothesize that groups of specieswith similar vegetative phenologies, under similar conditions, are functionally similar in terms of water storage anduse.We analyse the relationship between functional characteristics related to the acquisition and utilization of water,such as wood density, water storage capacity, water potential and vegetative phenology.The attributes were orderedby multidimensional scaling, and a multiple response permutation procedure was used to test consistency of thegroups. Canonical correspondence analysis and Mantel tests were used to evaluate the phenophase response toenvironmental variables.We found four functional groups: (i) deciduous low wood density, which lose 75% of theirleaves one month before the end of the rains; (ii) evergreen high wood density; (iii) early deciduous high wooddensity, which lose 75% of their leaves one month after the end of the rains; and (iv) late deciduous high wooddensity, which lose 75% of their leaves two months after the end of the rains. As expected, the vegetativephenodynamics of the deciduous high wood density group were mainly influenced by water availability. Theevergreens did not show a correlation with rainfall. Only leaf shedding of the late deciduous, and the vegetativephenophases of the evergreens, responded to an increase in temperature and photoperiod. Bud-break responded toincreased photoperiod and soil humidity in the deciduous low wood density group.The foliar periodicity groups canbe explained by the presence of species that differ mainly in their mechanisms of water acquisition and use.

Key words: functional ecology, functional traits, phenological strategy, tropical dry woodland, water potential,wood density.

INTRODUCTION

Plants under a seasonal dry tropical climate presentdifferent strategies of resistance to drought; those thattolerate (evergreen) and those that avoid (deciduous)it (Markesteijn & Poorter 2009). Nevertheless, the roleof these strategies in regions of low latitude underseasonal climates is not well defined. Identification offunctional groups through the analysis of the similari-ties and differences in a set of functional characterspresent in the species of a plant community enablestheir role to be understood (Borchert & Rivera 2001;Lima et al. 2012). The identification of groups isone way of analysing, at the community level, howthe vegetation responds to environmental changes(Cornelissen et al. 2003).

Since the early 1990s it has been known that inseasonal dry tropical climates a relationship existsbetween the phenophases of plants with wood densityand with the water storage capacity of the stem(Borchert 1994). It has been explained that bud-breakand flowering phenophases can be triggered by factorsindependent of rainfall in species with low wooddensity, due to the utilization of water stored in thewood during the dry season (Borchert et al. 2002;Rivera et al. 2002; Seghieri et al. 2012). However, indeciduous species with high wood density, thephenophases are generally associated with rainfall, asthey lack water storage capacity in their stems(Borchert 1994; Borchert & Rivera 2001; Borchertet al. 2002; Kushwaha et al. 2011; Lima et al. 2012).

Evergreens manage to trigger their phenophases inany period of the year, independent of wood density(Reich & Borchert 1984; Borchert 1994). This occursbecause they have mechanisms which allow water

*Corresponding author.Accepted for publication June 2014.

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absorption, such as deep roots or water storage capac-ity in the roots (Reich & Borchert 1984; Borchert1994; Markesteijn & Poorter 2009), which maintainthe flow of water even in the driest periods of the year(Williams et al. 2008).

Although photoperiod and temperature do act astriggers which stimulate the phenophases in specieswith mechanisms of water storage and/or deep roots(Borchert et al. 2002; Rivera et al. 2002; Elliott et al.2006; Lima et al. 2012), it is not yet clear whetherspecies in environments where these factors are fairlyconsistent have the same triggers, since previousstudies of this type have been conducted in regions athigher latitude (Borchert & Rivera 2001; Rivera et al.2002).

Based on this information, we question whether thephotoperiod and temperature, which vary little in sea-sonally dry regions close to the equator, such as in thesemiarid environment of north-east Brazil, are stillcapable of stimulating the vegetative phenophases ofevergreens, or species with low wood density. So weexamined whether species with a similar periodicity ofthe vegetative phenophases, triggered by the sameenvironmental factors, are functional equivalents.

Therefore, our objective was to evaluate the influ-ence of environmental variables (temperature, photo-period, rainfall) and functional characters (wooddensity, water storage capacity of the stem and waterpotential) on the initiation of vegetative phenophasesin dry and rainy periods throughout the year. In thisway, we can understand how environmental variablesinfluence the phenology of woody species in accord-ance with the water dynamics of these species.

Our hypothesis is that species that live in environ-ments that have a strong environmental filter, such aswater resources, and show similar phenology, will befunctionally equivalent in the use and storage of waterand, where they are equivalent, the similarity will be sostrong to the point that functional groups are formed.From this work, we can infer which functional charac-teristic of a given species enables initiation of the veg-etative phenophases in the dry season, as well aspredict which possible environmental variable will bethe trigger of these phenophases, even where low vari-ation of photoperiod and temperature exist, such as inthe semiarid region, close to the equatorial zone.

METHODS

Study area

The study was conducted at the Fazenda Experimental Valedo Curú (Curú Valley experimental station) in Pentecoste,Ceará (3°48′26.60″S and 39°21′8.40″W), in the semiaridregion of north-east Brazil. The historical average annualrainfall is approximately 772.2 mm according to data from

the meteorological station at the farm. During the study, in2012, the annual rainfall was 416.9 mm (Fig. 1), with thegravimetric water content of the soil varying in proportionfrom 2.55% to 6.62% (Fig. 1) over the year. The averagetemperature was 28.7°C, with a relative humidity of 58.9%(Fig. 1). Variation in photoperiod was 27 min (Fig. 1), withthe shortest day occurring in June 2012 (11 h 54 min) andthe longest in December 2011 (12 h 21 min).

Data collection and analysis

Phenology

For phenological monitoring of the species we defined anarea of 100 × 50 m, subdivided into 50 plots of 10 × 10 m, inwhich we marked the adult individuals conforming to thecriteria proposed by Rodal et al. (1992). For each of the 22species sampled (Table 1), we marked from five to twentyindividuals (Fournier & Charpantier 1975). We made fort-nightly observations of the phenophases of bud break

Fig. 1. (A) Monthly rainfall and photoperiod. (B) Monthlyrainfall and gravimetric soil water content. (C) Monthly tem-perature and air humidity. Fazenda Experimental Vale doCurú, Pentecoste-CE, Brazil.

2 C. C. OLIVEIRA ET AL.

© 2014 The Authorsdoi:10.1111/aec.12165Austral Ecology © 2014 Ecological Society of Australia

(growing), leaves in the canopy (unfolded/adult leaves) andleaf shedding (yellow or brown leaves, when leaves werepartly or completely lost by the individual). The intensity ofphenological events was measured as described by Fournier(1974). Leaf longevity was measured in five individuals ofeach species. Because of the difficulty in measuring longevityin large trees, we use the average time in months between budbreak to the leaf shedding. We defined deciduous species asthose that remained without leaves for at least one month,and evergreens as those that had leaves all year (Williamset al. 1997).

The average data for rainfall, temperature and air humiditywere obtained from a meteorological substation located inthe study area. The photoperiod data were obtained fromLammi (2009).

Water potential

We conducted monthly measurements in three individualsfrom each of the 22 species. From each plant we selected andpruned a terminal branch of approximately 10 cm, at thesame height from the soil to avoid variation in water potentialin individuals of each species (for standardization).The deci-sion to collect branches was due to the fact that in dryperiods, some species lose their leaves and it is not possible tomeasure from the petiole. Sampling occurred before sunrise,from 1.00 hours to 4.00 hours, when the transpiration rate

was minimal, favouring water recovery and equilibrium ofthe water potential of the stem and the soil (Bucci et al.2004). We cut the end of the pruned branch, wrapped it inplastic cling-film and stored it in a polystyrene container,chilled, to prevent as much as possible the loss of sap fromthe branch. We measured the water potential no more thantwo hours after the material was collected (Borchert 1994),using a Scholander type pressure chamber (Scholander et al.1965), with a maximum pressure of 100 bars, exerted bycompressed nitrogen.

Wood density

The collection followed the method proposed by Trugilhoet al. (1990) (dry weight/volume), in which we selected fiveindividuals of each species (different individuals to thoseobserved for phenology), and extracted five sample disks,with a diameter ≥ 3 cm, from different branches and then thebark was removed.

We calculated the wood basic density and amount of waterstored from the average of the 25 discs of each collectedspecies.We considered low wood density species those with adensity lower than 0.5 g cm−3, and high wood density whendensity was greater than or equal to this value (Borchert1994).We calculated the wood basic density (D, g cm−3) andthe amount of saturated water (QWsat, %) according toBorchert (1994).

Table 1. Woody species with wood density values (WD) in ascending order and quantity of saturated water (QWsat) indescending order

Species WD (g cm−3)QWsat

(%)Dry season(Ψ – MPa)

Rainy season(Ψ – MPa)

LeafPhenology

(months> 25%)

Cochlospermum vitifolium (Willd.) (L.) Spreng. 0.20 (±0.05) 416 −1.2 −0.2 Deciduous 3Commiphora leptophloeos (Mart.) J.B. Gillett 0.30 (±0.02) 236 −1.5 −0.3 Deciduous 4Manihot carthaginensis (Müll. Arg.) Allemão 0.34 (±0.04) 195 −1.1 −0.2 Deciduous 3Amburana cearensis (Allemão) A.C. Sm. 0.46 (±0.03) 118 −1.2 −0.6 Deciduous 5Ziziphus joazeiro Mart. 0.55 (±0.04) 85 −2.7 −0.6 Evergreen 12Cordia oncocalyx Allemão 0.55 (±0.02) 83 −7,5 −0.7 Deciduous 5Combretum leprosum Mart. 0.55 (±0.02) 83 −4.5 −0.4 Deciduous 7Cordia trichotoma (Vell.) Arráb. exSteud. 0.55 (±0.04) 82 −8.0 −0.7 Deciduous 4Cynophalla flexuosa (L.) J. Presl 0.56 (±0.03) 79 −2.4 −0.7 Evergreen 12Helicteres heptandra L.B. Sm. 0.57 (±0.02) 75 −8.3 −0.4 Deciduous 4Piptadenia stipulacea (Benth.) Ducke 0.57 (±0.03) 76 −5.5 −0.6 Deciduous 7Ximenia americana L. 0.58 (±0.05) 74 −7.0 −0.9 Deciduous 10Piptadenia viridiflora (Kunth) Benth. 0.59 (±0.03) 69 −3.2 −0.9 Evergreen 12Anadenanthera colubrina (Griseb.) Altschul 0.61 (±0.02) 64 −7.3 −0.7 Deciduous 9Lafoensia pacari St. Hil. 0.62 (±0.01) 62 −7.1 −0.4 Deciduous 5Sebastiana macrocarpa Müll. Arg. 0.62 (±0.01) 61 −6.8 −0.6 Deciduous 4Croton blanchetianus Baill. 0.62 (±0.02) 61 −8.3 −0.5 Deciduous 4Libidibia ferrea (Mar. ex Tul.) L.P. Queiroz 0.65 (±0.02) 55 −3.3 −0.9 Deciduous 10Aspidosperma pyrifolium Mart. 0.65 (±0.02) 55 −6.5 −0.7 Deciduous 7Poincianella bracteosa (Tul.) L.P. Queiroz 0.65 (±0.02) 54 −5.4 −0.7 Deciduous 6Mimosa caesalpiniifolia Benth. 0.65 (±0.03) 54 −8.2 −0.5 Deciduous 4Bauhinia cheilantha (Bong.) D. Dietr. 0.67 (±0.02) 50 −8.0 −0.5 Deciduous 5

Minimum water potential (dry season) and maximum water potential (rainy season) before dawn. Pattern of leaf phenologyand the duration of the adult leaves phenophase when it was at an intensity higher than 25% (Fournier 1974) in FazendaExperimentalVale do Curú, Pentecoste – CE, Brazil.

FUNCTIONAL GROUPS PHENOLOGICAL OF WOODY SPECIES 3




Soil water content

We conducted monthly measurements, on the same date asthe water potential data collection.We obtained soil samplesat depths of 0–20 and 21–40 cm to obtain the average soilmoisture within the 40 cm. We collected samples from eachalternate plot of 10 × 10 m, totalling 25 points.

To prevent moisture loss, we stored the soil samples insealed pots until they were weighed in the laboratory toobtain the wet weight, and the weight after drying in a ovenat 105°C (EMBRAPA 1997). We used the data to calculategravimetric soil water content: % (G): (wet weight − dryweight)/(dry weight) × 100.

Statistical analysis

We analysed the phenophases using Fournier intensity valuesas input data to run the circular statistics software ORIANA4 (Kovach 2013) which deals with cyclical events, and weverified the patterns of vegetative phenophases (bud break,adult leaves and leaf shedding), in the period from December2011 to November 2012. Zero degrees corresponds to 1December 2011. We converted fifteen days into angles, withintervals of 15°, and we calculated the average angle oraverage date (μ), converted into days by dividing the value of(μ) by 0.986 which corresponds to one day in angles. Theaverage angle (μ) is the period of greatest intensity of thephenophase during the year, i.e, when the species is 100% inits phenophase.We used the value of (μ) converted into daysas an attribute of vegetative phenophases of each species.

We inserted the attributes collected from the functionaltraits of the species (bud break, adult leaves, leaf shedding,water potential, leaf longevity, wood density and quantity ofsaturated water) in a matrix, with species in the rows andtraits in the columns. To standardize the measured traits, wesubtracted from the observed values the average value of eachtrait and divided by its respective standard deviation (Kröberet al. 2012).We applied the Euclidean distance coefficient inthe matrix using the software Past ver. 2.17b (Hammer et al.2001). We then imported the matrix to the programPC-ORD 6 (McCune & Mefford 2011), in which we per-formed cluster analysis, using the unweighted method ofpaired groups using the arithmetic mean.We performed mul-tidimensional scaling (NMDS) to rank the attributes of thespecies according to their functional similarity. This methodproduces a graphical representation of the similarity betweensamples in a small number of dimensions (Henderson &Seaby 2008).We performed a principal components analysis(PCA) to determine which of the functional traits analysedwere grouping the species.

We checked homogeneity within the groups sorted byNMDS by multiple response permutation procedure(MRPP), which compares the functional similarity withingroups, using the Euclidean distance. The MRPP providesthe value A, ranging from 0 to 1, which acts as a descriptor ofhomogeneity within the group compared with that expectedby chance; A = 1 indicates that species are identical withinthe groups, and A = 0 indicates that heterogeneity within thegroup is equal to that expected by chance and the species aredifferent, and A < 0 indicates that there is less similarity ofthe species than expected by chance (McCune & Mefford

2011). According to McCune and Grace (2002), in commu-nity ecology, the value of ‘A’ is generally below 0.1, and if ‘A’is bigger than 0.3, it is considered a high value.Therefore, thegroups were considered valid if A > 0.3.

We performed a canonical correspondence analysis (CCA)using two matrices, one with variable responses (vegetativephenophases of the group), and the other with environmentalvariables (photoperiod, rainfall, temperature and air andgravimetric soil water content).We extracted the values of themost informative axis with the environmental variables gen-erated by the CCA and used a Mantel test to see if theenvironmental variables significantly influenced the responsevariables in the program PC-ORD 6.

RESULTS

We found different interspecific phenological patterns:(i) deciduous species, which have a short duration ofthe ‘adult leaves’ phenophase, with a periodicity of 3–6months; (ii) deciduous late species, which maintaintheir leaves for a longer time period, and can spend upto 10 months in-leaf; and (iii) evergreen species, whichhave leaves throughout the year (Table 1).

Wood basic density and water storage capacity of thespecies were highly variable (Table 1) and inverselyproportional (r2 = −0.994, P < 0.001). Density variedfrom 0.20 to 0.67 g cm−3 and water storage capacitybetween 50% and 416% of dry weight (Table 1). Wealso verified that species with high water storage capac-ity and low wood basic density (DLWD) had littlevariation in water potential throughout the year, alwaysmaintaining high water potential, contrary to theobservations for deciduous species with high woodbasic density (Table 1).

Visual interpretation of the cluster analysis, with theattributes collected from the phenological characteris-tics, wood density, water storage capacity and waterpotential, showed four functional groups (Fig. 2).We note that the first group contained four deci-duous species with DLWD, and a relatively constantaverage water potential throughout the year (−0.8 ±−0.3 MPa); the second group contained four species oflate deciduous high wood density (LDHWD), withgreater variation in water potential (−2.5 ± −1.1 MPa),being those that lose their leaves slowly after the rainyseason; the third group was composed of three ever-green species (EG), also with little variation in waterpotential (−1.8 ± −0.5 Mpa) and the fourth groupconsisted of eleven species of early deciduous highwood density (EDHWD), with high variation in waterpotential (−4.6 ± −1.8 MPa), being those which losetheir leaves rapidly after the rainy season.

The NMDS ordination analysis showed that thespecies were ordered in accordance with the clusteranalysis (Fig. 3), resulting in a final stress of 0.06,meaning that the spatial configuration generated by



the test is close to the actual data configuration and theMRPP indicated consistency in the groups (A = 0.45,P < 0.001).

With the spatial configuration of the species gener-ated by the NMDS and the PCA (Fig. 3), we identi-fied the most similar characteristics between thespecies that strengthened the formation of the groups.We found that clustering of the DLWD was drivenprincipally by increased water storage capacity andminimal water potential in the rainy season andmaximum in the dry season. Formation of the EGgroup was principally driven by leaf longevity andsynchrony in the phenological event bud-break. TheEDHWD group was strengthened principally by highwood density, as well as by synchrony of the adultleaves and leaf shedding phenophases. The LDHWDgroup was strongly influenced by similarity in theperiod of bud-break of the species and in leaf longevity(Fig. 3).

As the groups differed in their functional character-istics, they also differed in their phenological patterns,and in their relationship to environmental factorsactive in triggering their vegetative phenophases. Weobserved that the bud-break phenophase of theDLWD began at the end of the dry season, but hadgreater intensity in the first months of the rainy season,with January being the average date of occurrence ofthis phenophase (Fig. 4). This group also had a shortperiod of adult leaves, of approximately two and a halfmonths, only in the rainy season, and a long periodwithout leaves, of eight and a half months for morethan 50% of the species, with leaf shedding startingthe one month before the end of the rains (Fig. 4).The

average date of adult leaves occurred at the beginningof April and that of leaf shedding in September(Fig. 4).

The bud-break phenophase of the EG groupoccurred at the height of the drought, and the averagedate of occurrence of this phenophase was in October(Fig. 4). This group had adult leaves for the wholeyear, having a small reduction only during the dryseason, the period in which a gradual exchange ofleaves occurred.The average date of occurrence of theadult leaves phenophase was in March (rainy season),and leaf shedding in September (dry period) (Fig. 4).

The group formed by the EDHWD showed agreater intensity of bud-break in the rainy season, witha peak in March, however the average date of occur-rence of this phenophase occurred in early February(Fig. 4).The peak of adult leaves occurred throughoutthe last four rainy months. From the first monthwithout rain (July) more than 50% of the leaves hadbeen lost, with a prolonged leaf shedding lasting for aperiod of up to eight months (Fig. 4).The average dateof occurrence of the adult leaves phenophase occurredin April (rainy), and leaf shedding occurred in October(dry) (Fig. 4).

Bud-break of the LDHWD group began at the endof the dry season, but was more intense in January,after the beginning of the rainy season, with an averagedate of occurrence in January (Fig. 4). The highestintensity of adult leaves for this group lasted through-out the rainy season, and lasted for more than tenmonths after the end of the rains, with an average datein April (Fig. 4). Leaf shedding lasted approximatelyfive months, with an average date in October (Fig. 4).

Fig. 2. Cluster analysis of the functional attributes of woody species in an area of caatinga, Pentecoste, Ceará, Brazil. Theabbreviated species correspond to the species in Table 1.



Bud-break of the DLWD and LDHWD was influ-enced by an increase in photoperiod and soil humidity,and in the EDHWD group it was most influenced byan increase in air humidity, whilst in the EGs thisphenophase was related to an increase in temperature,as can be seen in the CCA (Fig. 5), which was verifiedusing a Mantel test (r = −0.22, P = 0.03).

The increase in rainfall and soil humidity enabledthe maintenance of the adult leaves phenophase in thegroups EDHWD, LDHWD and DLWD (Fig. 5).Thelatter was strongly influenced by air humidity.The EGswere more strongly influenced by increasing tempera-ture and photoperiod (Fig. 5), as shown by the Manteltest (r = 0.86, P = 0.001).

Fig. 3. Multidimensional scaling (NMDS) analysis of the sampled species. (A) Deciduous low wood density (DLWD) ((1)Amburana cearensis, (5) Cochlospermum vitifolium, (7) Commiphora leptophloeos and (15) Manihot carthaginensis). (B) Earlydeciduous high wood density (EDHWD) ((2) Anadenanthera colubrina, (4) Bauhinia cheilantha, (8) Cordia oncocalyx, (9) Cordiatrichotoma, (10) Croton blanchetianus, (12) Helicteres heptandra, (13) Lafoensia pacari, (16) Mimosa caesalpiniifolia, (19) Poincianellabracteosa, (20) Sebastiania macrocarpa and (21) Ximenia americana. (C) Late deciduous high wood density (LDHWD) ((3)Aspidosperma pyrifolium, (6) Combretum leprosum, (14) Libidibia ferrea, (17) Piptadenia stipulacea). (D) EG Evergreen ((11)Cynophalla flexuosa, (18) Piptadenia viridiflora and (22) Ziziphus joazeiro). Principal components analysis (PCA) of the attributesof the sampled species. (QWsat = quantity of saturated water, Ψ rainy season = maximum water potential in the rainy season, Ψdry season = minimum water potential in the dry season).



Fig. 4. Circular analysis with Fournier’s average percentage of the species groups: deciduous low wood density (DLWD),evergreen (EG), early deciduous high wood density (EDHWD) and late deciduous high wood density (LDHWD), fromDecember 2011 to November 2012. Note: Vegetative phenophases in the columns and groups in the rows.



We found that leaf shedding in the EDHWD wasinfluenced by a decrease in rainfall, and soil and airhumidity (Fig. 5). Leaf shedding in the DLWD wastriggered mainly by a decrease in air humidity, whilethe LDHWD and EG were influenced by an increasein temperature and photoperiod (Fig. 5), as confirmedby the Mantel test (r = 0.40, P = 0.01).

DISCUSSION

As expected, similar behaviour of the groups of woodyspecies studied proved our hypothesis. We can predictthat species with similar phenology, also have similarfunctional attributes, which consequently respond tothe same environmental factors. Similar mechanismsin seasonally dry environments have been discussed byother authors (Borchert 1994; Reich et al. 2003; Limaet al. 2012).

Thus, the fact that DLWD initiate their bud-breakphenophase even in the dry season, possibly occursdue to the high water storage capacity of the stemthroughout the year, independent of the season beingdry or rainy (Borchert 1994; Borchert & Rivera 2001;Lima & Rodal 2010; Lima et al. 2012; Seghieri et al.2012). However, whilst bud-break was initiated beforethe start of the rainy season, we observed greater inten-sity of this phenophase during the rainy season. Bud-break occurring before the start of the rainy season issuggested by some authors to be an adaptation toavoid predation by herbivores (Chapotin et al. 2006).It can also be seen as a way of extending the period ofcarbon assimilation, since in these environments therainy season is short (Elliott et al. 2006).

The short period with adult leaves in the DLWDand the rapid leaf shedding before the end of the rainyseason could be considered to be a water saving strat-egy (Reich & Borchert 1982; Borchert & Rivera 2001;Borchert et al. 2002). Generally, the increase in pho-toperiod is the key factor for triggering the bud-breakphenophase of these species due to the high waterstorage capacity of the stem (Borchert et al. 2002;Rivera et al. 2002; Kushwaha et al. 2010; Lima et al.2012). However, we found that along with the photo-period, an increase in soil humidity also influenced thisphenophase.

The occurrence of bud-break in the EG throughoutthe dry season and of adult leaves for the whole year isprobably related to the capacity of their deep roots toacquire underground water (Borchert 1994), or towater storage capacity of the roots (Jackson et al.1997). Thus, the EGs can trigger their bud-breakphenophase at any time of year (Reich & Borchert1984; Borchert 1994). In this study, we found that thisoccurred only in the dry season. In accordance with Fuet al. (2012), the presence of leaves throughout theyear is favoured by a secure hydraulic system that

Fig. 5. Canonical correspondence analysis with environ-mental factors photoperiod (Photo), rainfall (Rain), tempera-ture (Temp), air humidity (AH) and gravimetric soilwater content (SWC), indicating their influence on thephenophases bud break, adult leaves and leaf shedding in thefour groups: evergreens (EG), deciduous low wood density(DLWD), early deciduous high wood density (EDHWD)and late deciduous high wood density (LDHWD).



maintains the flow of water in the stem of the EGs.Markesteijn and Poorter (2009) observed that thistransport of water to the leaves in the driest period ofthe year also avoids cavitation and confers stronghydric control.

Therefore, it can be argued that EGs have one of thebest strategies of drought resistance (Reich & Borchert1984; Borchert 1994; Markesteijn & Poorter 2009;Poorter et al. 2010). Another advantage of this group,suggested by Pringle et al. (2011), is that EG specieshave less palatable leaves, decreasing the rate ofpredation. So, why do EGs not predominate in sea-sonal dry forest communities? It is possible that thefactor limiting the richness and abundance of thisgroup is the high intra- and inter-annual variation inrainfall, which can decrease and even dry-out thequantity of water in the aquifers. Borchert (1998)demonstrated a change from EG to deciduous speciesin dry forests, due to a scarcity of water in the soil. Ingeneral, a greater predominance of deciduous speciesis associated with environments with low soil waterretention (Pringle et al. 2011).

The low water storage capacity of deciduous speciesmeans their vegetative phenophases are principallytriggered by factors related to rainfall (Borchert 1994).Also, there is large variation in water potential betweenthe dry and rainy seasons, varying in accordance withthe water availability of the soil (Lima et al. 2012).Therefore, it is common to find a correlation betweenthe bud-break and adult leaves phenophases of decidu-ous species with factors related to water availability(Russo et al. 2010).The timing of each phenophase indeciduous species can vary in accordance with theintensity of rainfall or the soil water retention time(Bach 2002).

Thus, the variation in leaf longevity between earlyand late deciduous species could be related to severalfactors, from the duration of the dry period to thecapacity to control water loss (Reich & Borchert 1984;Borchert 1994). In general, species that spend moretime ‘in-leaf’ are more sensitive to a water deficit,closing their stomatas at any sign of increase in waterdeficit and evaporation rate, rapidly decreasing the rateof photosynthesis (Reich et al. 2009).

Another possible influence on the earlier bud-breakof the LDHWD species is the previous year’s rainfall,which was well above the annual average (911.7 mmfrom January to August 2011). This probably resultedin a longer period with soil water, which is necessaryfor the species of this group to change their leaves,even before the onset of the rainy season. This behav-iour is not generally found in the literature, consider-ing that deciduous high wood density species dependprincipally on soil water to trigger their vegetativephenophases (Borchert 1994; Lima et al. 2012).

Herewith, we can conclude that the functionalgroups have distinct patterns in their vegetative

phenophases, which respond to different abioticfactors due to a large variation in the specific attributesof the species in each group. We can also infer thephenological patterns of woody species in a seasonallydry climate, from attributes such as wood density, andwater storage capacity of the stem.

Even in seasonally dry regions close to the equator,where photoperiod and temperature remain relativelyconstant, we are able to determine the onset ofphenophases of some species, especially those in theevergreen and deciduous low wood density functionalgroups, as these show other mechanisms of use andstorage of water in the stem.

Species with similar strategies of tolerance to waterdeficit in dry tropical forests tend to have a largerfunctional convergence, which allows functionalgroups to be formed, which may explain the differentstrategies of acquisition, storage and use of water inthese groups of species in seasonally dry environments.Therefore, one may expect trade-offs to exist between awide variety of functional characters in the species ofthese groups, allowing them to coexist in seasonallydry environments.

ACKNOWLEDGEMENTS

Thanks go to the Conselho Nacional de Pesquisa eDesenvolvimento for financial support through thebolsa de produtividade grant of Maria Jesus NogueiraRodal (process CNPq No. 303157/2009-7). The pro-fessors Dr Fernando Roberto Martins and DrEverardo Valadares de Sá Barretto Sampaio are alsothanked for contributions made to this work.

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functional groups of woody species in semi-arid regions at low latitudes

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