REGULAR ARTICLE

Stem growth and phenology of two tropical treesin contrasting soil conditions

F. C. G. Cardoso & R. Marques & P. C. Botosso &

M. C. M. Marques

Received: 20 May 2011 /Accepted: 7 November 2011 /Published online: 9 December 2011# Springer Science+Business Media B.V. 2011

AbstractBackground and aims Phenological variations intropical forests are usually explained by climate.Nevertheless, considering that soil water availabilityand nutrient content also influence plant water statusand metabolism, soil conditions may also be importantin the regulation of plant reproductive and vegetativeactivities over time. We investigated whether phenolog-ical patterns and stem growth differ in trees growing intwo types of soil that display contrasting water andnutrient availability, namely, Gleysol (moist andnutrient-poor) and Cambisol (drier and nutrient-rich).Methods Phenological observations (flushing, leaffall, flowering and fruiting) and stem diameter growthwere recorded for 120 trees fitted with fixed

dendrometer bands, at 15 days intervals, for 1 year.Two species of contrasting deciduousness wereinvestigated: Senna multijuga (semi-deciduous) andCitharexylum myrianthum (deciduous).Results Both species were seasonal in all phenophases,regardless of soil type. However, frequency, meandate and intensity of phenophases varied accordingto soil type. Girth increment of C. myrianthum wasfour times greater in Cambisol than in Gleysol,whereas the type of soil had no significant effect onthat of S. multijuga.Conclusions These results show that soil characteristicsalso play an important role in determining phenologicalpatterns and growth and must be considered whenanalysing phenological patterns in tropical forests.

Keywords Citharexylum myrianthum . Diametergrowth . Seasonal rhythms . Senna multijuga . Soilnutrients . Tropical forest

Introduction

The reproductive and vegetative activities of tropicaltrees are mainly controlled by day length (Borchertet al. 2005; Marques et al. 2004; Wright and VanSchaik 1994), temperature (Morellato et al. 2000) andrainfall (Günter et al. 2008; Lieberman 1982; Reichand Borchert 1984). Day length and temperature arestrongly related to the break of leaf- and flower budsat solstice, whereas rainfall primary influences tree and

Plant Soil (2012) 354:269–281DOI 10.1007/s11104-011-1063-9

Responsible Editor: Alfonso Escudero.

F. C. G. Cardoso (*) :M. C. M. MarquesLaboratório de Ecologia Vegetal;Departamento de Botânica, SCB,Universidade Federal do Paraná,CP 19031, 81531-980 Curitiba, PR, Brazile-mail: fernanda.g.cardoso@gmail.com

R. MarquesDepartamento de Solos e Engenharia Agrícola,Universidade Federal do Paraná,Curitiba, Brazil

P. C. BotossoEmpresa Brasileira de Pesquisa Agropecuária,Embrapa Florestas,Colombo, Brazil

soil water status, affecting the growth and reproductionof plants subject to seasonal climates (Borchert 1994;Fenner 1998). Therefore, soil water availability,though rarely a trigger in plant phenology and growth(Marques et al. 2004), should be considered one ofthe most important environmental factors affectingtree growth and distribution (Hinckley et al. 1991).

Even when tropical trees grow under the sameprecipitation regime, they may show differentphenological patterns. These can be caused byvariation in the soil–plant–atmosphere continuum,and this, in turn, determines the plant water status(Hinckley et al. 1991). Plant annual rhythms occureven in environments with stable climate, such as wetforests. In these environments, plant responses toseasonal cues establish the annual diameter incre-ment in some species (Borchert et al. 2005;Newstrom et al. 1994). O’Brien et al. (2008)demonstrated a lower increment in diameter duringthe months following leaf fall for many deciduousspecies, whereas a relationship between growth andphenology was not found for evergreen species.Worbes (1999) found that evergreen species in atropical forest in Venezuela had only a short interrup-tion of wood growth during the dry season whereasdeciduous species stopped growth completely at theend of the rainy season.

Tree stems contract and expand as water is usedand stored by plants (Baker et al. 2002; Zweifel et al.2000). Diameter growth also varies from species tospecies and between individuals in response to factorssuch as age, season and microclimate conditions(Rozendaal and Zuidema 2011; Taiz and Zeiger1991). Tropical trees show considerable variation instem diameter, even during the course of a single day(Sheil 2003). In wet forests, these variations appear tobe annually cyclic and related to precipitation patternand soil water status (Botosso et al. 2000; Pélissierand Pascal 2000; Sheil 1995; Silva et al. 2002;Volland-Voigt et al. 2011). Trees occurring in soilsdisplaying cyclic inundation regimes usually growduring the unflooded period and stop growing duringflooding, for example in Amazonian floodplain forests(Worbes 1995; Schöngart et al. 2002). Furthermore,inundation induces leaf fall, and this is followed by a2-month period of cambial dormancy and theformation of an annual ring in trees growing inAmazonian floodplain forests (Schöngart et al. 2002).Variation in girth increment can also occur throughout

the year, and this is clearly related to alternating periodsof heavy precipitation followed by periods of longdrought (Pélissier and Pascal 2000; Lisi et al. 2008).

Phenology and growth are potentially modified byother environmental factors, including soil-relatedfactors (Brun et al. 2003; Wielgolaski 1974, 2001;Valdez-Hernández et al. 2010). For example, anincrease in soil nutrients resulted in increased flowerproduction in one tree species (Sperens 1997),whereas elevated copper concentrations in soildelayed the flowering and fruiting of ruderalspecies (Brun et al. 2003). Moreover, soil metalconcentration also affected flowering, leaf life-spanand fruit ripening in a ruderal species (Ryser andSauder 2006). Correlations have been found to occurbetween phenophases and the physical (clay, sand andsilt contents) and chemical (pH and levels of Ca, Mgand P) characteristics of soil (Wielgolaski 2001).Thus, soil may be an additional factor affectingtropical forest phenological patterns.

In this study, we compared the stem growth (stemgirth increment) and phenology of two tropical treespecies that differ in leaf deciduousness (Citharexylummyrianthum—deciduous and Senna multijuga—semi-deciduous) growing in two soil types that differ intheir water and nutrient status (Gleysol—moist andnutrient-poor and cambisol - drier and nutrient-rich).In particular, we addressed the following questions:(1) Do stem growth and phenology (phenophasesmean date, seasonality and intensity) differ accordingto soil type? (2) Is stem growth related to flushing,leaf fall, fruiting and flowering? (3) Is there arelationship between growth, phenology and soilcharacteristics (nutrient content and texture)?

Materials and methods

Study site

This study was carried out in Rio Cachoeira Reserve(25°19′15″ S and 45°42′24 W, elevation from 2 to900m a.s.l.), an 8,600 ha area in Antonina, Parana State,on the southern coast of Brazil. The reserve is part of theGuaraqueçaba Environmental Protection Area, or“APA”, a large region (more than 300,000 ha) thatincludes forests, estuaries, bays, islands, mangroves andlowlands, and is part of one of the most importantremaining areas of Atlantic Forest in Brazil (Ferretti and

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Britez 2006a). The climate in the region is humidsubtropical (Cfa), according to Köppen’s classifica-tion (Ferretti and Britez 2006a), with annual precip-itation of 3106 mm and mean temperature of 21°C(data from a meteorological ground station of SIME-PAR Institute of Technology, collected between 1999and 2008).

Four soil types occur in the reserve, namelyNeosol, Gleysol, Cambisol and Argisol (Ferretti andBritez 2006b). In this study, phenology and stemgrowth of trees growing in Gleysol and Cambisolwere compared. Gleysols are hydromorphic, mineral,sandy, with variable fertility and are permanently orperiodically saturated with water. Cambisols are non-hydromorphic, mineral, with variable fertility andhigh silt content (Embrapa 1999). Planted treesgrowing in areas of Gleysol and Cambisol wereselected to study phenology and stem growth. Alltrees investigated were part of a restoration projectconducted in different areas of the reserve, and wereplanted 8 years prior to the commencement of thestudy (Ferretti and Britez 2006b), so they were all ofthe same age and had similar diameter at breast height(6 cm≤DBH≤18 cm) at the beginning of the study.This procedure was adopted in order to reduce theeffect of age, size (crown, diameter, total biomass) andspacing on individual trees. The restoration systememployed on these sites involved the direct manualplanting of pioneer species seedlings, 2×3 m apart.Since the region has a mild climate, and rainfall is welldistributed throughout the year (>70 mm per month),restoration is efficient, survival is high (>70%) and plantgrowth is very fast. At the beginning of the study, alltrees were between 3 and 10 m tall and had alreadyexperienced at least one reproductive event. Detailedinformation on these restoration systems can be found inFerretti and Britez (2006a) and Bruel et al. (2010).

Species studied

Two pioneer tree species that are common insecondary Atlantic forests were selected for the study:Senna multijuga (Rich.) H.S. Irwin & Barneby(Fabaceae) and Citharexylum myrianthum Cham(Verbenaceae). The former is a semi-deciduous,dioecious tree, 2–10 m tall, and distributed throughoutLatin America. In Brazil, it is commonly found on thehillsides of the Atlantic Forest (Lorenzi 1992; Rodrigueset al. 2005). Flowers are small, yellow and occur in

raceme-like inflorescences (Rodrigues et al. 2005).The latter, is a deciduous and dioecious tree thatmainly occurs in moist sites. It varies from 8 to 20 min height and is distributed along the coastline thatstretches from the northeast to the south of Brazil(Lorenzi 1992; Rocca and Sazima 2006). Flowers aresmall, tubular, white-colored, and crepuscular, pollinatedby sphingids and occur in raceme-like inflorescences(Rocca and Sazima 2006).

Field measurement methods

A preliminary, phenological, 2-year (2004–2006)study of the selected species was performed alongsecondary forests trails of the reserve. The pres-ence of flushing, leaf fall, flowering and fruitingwas observed monthly for five individuals of eachspecies. The phenological variation (number of individ-uals in each phenophase per month) for the previous(2004–2005) and present study (2007–2008) was verysimilar for both species (0.46≤rs≤0.91, P<0.05).Therefore, it was assumed that the inter-annualvariations are weakly significant in this case, and thatthis phenological study (2007–2008) approximatelyrepresents the local pattern for these species.

Phenology and growth

Sixty individuals of each of the two species (120 treestotal) were randomly marked from amongst the treesplanted along the Gleysol and Cambisol restorationareas (30 trees of each species for each soil type). Stemgirth increment (at 1.3 m above ground level) wasrecorded using permanent, steel, dendrometer bands,having 0.2 mm precision (Botosso and Tomazello Filho2001). Data were recorded twice a month for12 months (24 measurements), starting in October2007. The first reading was adjusted to the 0 value forall trees in order to highlight the subsequent increaseor reduction of the stem diameter. All dendrometerbands were set up at least 1 month prior to taking thefirst reading, so that the bands could be fittedcorrectly around the stems (O’Brien et al. 2008).

Phenology (flushing, leaf fall, flowering andfruiting) of all selected trees was recorded at thesame time that the dendrometer bands were read.Flushing was considered to have begun when smaller,lighter coloured leaves were present and when leafbuds had started to develop. Leaf fall was recorded

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when gaps had appeared in the crown and fallenleaves had accumulated beneath the plant. Floweringwas recorded when the trees showed flower buds and/or open flowers, whereas fruiting was recorded whendeveloping fruit and/or mature fruit were observed(Marques et al. 2004; Morellato et al. 2000). Thephenophases were quantified and categorized asfollows: (0) absence of the phenophase, (1) a lownumber (1 to 50) of phenophase representativestructures (leaf buds, falling leaves, flowers or fruits);(2) a moderate number (50 to 100) of structures; (3) ahigh number (≥100) of these structures.

Soil characterization

In order to assess the groundwater available, piezometerswere set in both sites, depending on their size (12piezometers in Gleysol site and 17 in the Cambisol site).Piezometers were made of perforated PVC pipes, 10 cmin diameter, and were installed as much as 100 to 150 cmbelow ground level (Walthall and Ingram 1984). Theywere placed close to the marked individuals so as tomeasure, as accurately as possible, the groundwaterlevel along the area occupied by the trees. Variation ingroundwater level was similar in the two sites;however, groundwater level in Cambisol was lowerin most of the year in relation to Gleysol. Groundwaterwas deeper (less water available to plants) in June, Julyand September (months with lower precipitation), whenwater was more than 120 cm deep in Cambisol andapproximately 90 cm deep in Gleysol. The lower depth(water closer to surface) occurred in March (end of thewettest period) when it was only 7 cm below surface inCambisol and 13 cm in Gleysol.

Soil sampling was carried out beneath 15selected trees of each species for physical and nutritionalanalysis. Samples were collected at a depth of 0–10 cmfrom beneath each tree, at three equidistant pointsapproximately 100 cm from the trunk, for each speciesand soil type. Samples were then pooled in a polythenebag, each sample representing a single tree (total of 60samples). Soil samples were taken to the laboratory, air-dried and sifted. Standard chemical analyses wereperformed for pH, P, Al, Ca, Mg, K, Al and C (Embrapa1997), and physical analysis (soil texture) for thedetermination of clay, silt and sand content performedusing the densitometer method (Embrapa 1997). Thechemical analyses showed thatGleysol had significantlyhigher levels of Al and C than Cambisol, whereas the

latter had higher Ca, Mg and P contents. Potassiumlevels and pH did not differ between soils, but Gleysolhad higher levels of clay and sand whilst Cambisol hadhigher silt content (Table 1).

Data analysis

Spearman correlations (rs, Zar 1999) were performedfor each species, in order to test for possible relationshipsbetween phenophases in the two soil types (Gleysol andCambisol), using the number of individuals in each fieldobservation (n=24). For example, the amount ofindividuals flushing in each month in Gleysol wascompared to the one in Cambisol. The same wasperformed to leaf fall, flowering and fruiting

Circular statistical analyses (Zar 1999) wereperformed for each species in each soil type, in orderto determine the number of observations, the meanangle u (and standard deviation) and the length ofmean vector (r) of each of the four phenophases,using software ORIANA 2 (Kovach ComputingServices 2003). In this procedure, months wereconverted to angles with 15° intervals representing eachobservation (0° = first 15 days of January, 15° = last15 days of January, up to 345° = second half ofDecember), in a total of 24 intervals of 15° (Morellatoet al. 2010).

The number of observations refers to the frequencyof occurrence of each phenological variable in eachsoil type, reaching a maximum of 720 observations(30 individuals × 24 field observations) for eachspecies (note that each individual has entered in thesample every time it showed the phenophase). Themean angle was converted to a corresponding meandate that refers to the time of the year around whichthe dates of a given phenophase occurred for mostindividuals. The length of mean vector r is a measureof concentration around the mean angle that indicateswhether the phenophase is concentrated (values closerto 1) around a mean date.

The Rayleigh (z) test was performed in order todetermine the mean angle u which, when significant,indicates seasonality in the phenophase (Morellato etal. 2000). Prior to this analysis, we checked by visualinspection whether or not the phenograms wereunimodal, in order that we might assume the premisesof the test (Morellato et al. 2010; Zar 1999). When thedistribution seemed to be multimodal (two of 16cases), supported by the low r value, the test could

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not be used (Morellato et al. 2010) and we assumedno seasonality in phenophases. When the angle u wassignificant, we performed two-sample Watson-Williams tests (F) to compare the mean angle of eachphenological variable between sites and to determinewhether the different soils exhibited the same seasonalpatterns or mean angle (Morellato et al. 2000).

Differences between the frequencies of thephenophases intensity categories (from 0 to 3) accordingto soil type were determined using independence tests(G test) and these are mentioned in the text as“intensity of phenophases”.

Cumulative growth was compared between soil typesfor each species using repeated-measures ANOVA, assuggested by von Ende (2001) for growth and time-dependent measures. We first performed MauchlySphericity test to check for sphericity in the data. As itlacked sphericity, we adjusted epsilon using bothGreenhouse–Geisser (G-G) and Huynh–Feldt (H-F)adjustments. Possible relationships between phenophasesand stem growth were evaluated using Pearsoncorrelations (r, Zar 1999) based on the number ofindividuals in a given phenophase and the cumulativegirth increment (mm) for every 15 d interval. Toaccount for the effects of temporal autocorrelation inPearson correlation analyses between growth andphenology, we obtained corrected coefficients usingstationary bootstrap estimates with an average blocklength proportional to the maximum estimatedautocorrelation of the data (Mudelsee 2003;Montserrat-Marti et al. 2009).

A Principal Components Analysis (PCA) wasperformed to test for possible relationships betweengrowth, phenophases and soil nutrients. This ordinationanalysis was selected because all data showed an

approximate linear relationship amongst them (McCuneand Grace 1999). A main matrix was built for eachspecies. This contained phenology data (mean total ofoccurrences for each phenophase) and average growthdata for individual trees in both soil types. Thesecondary matrix held mean values for pH, Al, K, P,Mg, Ca, C, as well as data relating to the silt, sandand clay contents of the samples for each of the trees.Analyses were performed using PC-ORD (5.0)(McCune and Grace 1999).

Results

Phenological patterns in the two soil types

For Citharexylum myrianthum and Senna multijuga,flushing (respectively, rs=0.94 and rs=0.89, bothDF=22, P<0.001), leaf fall (rs=0.87 and rs=0.62,both DF=22, P<0.001), flowering (rs=0.83 and rs=0.99, both DF=22, P<0.001) and fruiting (rs=0.74and rs=0.93, both DF=22, P<0.001) were positivelycorrelated between soil types. However, there weredifferences in the frequency (number of observations),mean date (Table 2) and intensity (frequency ofintensity categories) of phenophases between soiltypes.

Citharexylum myrianthum showed a distinctlyseasonal pattern for all phenophases and soil types(Rayleigh test: all P<0.001) (Table 2). Flushingoccurred mainly from September to April and leaffall from March to November; flowering occurred inNovember and December, and fruiting from Decemberto February (Fig. 1). The length of mean vector r wasalways greater than 0.5 for both soil types (Table 2),

Table 1 Means (± SE) ofnutritional and physicalparameters in each soil typein southern Brazil. ns = notsignificative

aMeans between soils werecompared with a Z test

Cambisol Gleysol Z (P)a

pH CaCl2 4.07±0.04 4.01±0.02 0.16 (ns)

Al (cmolc/dm3) 1.67±0.14 2.15±0.10 2.30 (P<0.05)

Ca (cmolc/dm3) 2.40±0.39 0.19±0.03 6.59 (P<0.0001)

Mg (cmolc/dm3) 0.63±0.07 0.15±0.01 6.48 (P<0.0001)

K (cmolc/dm3) 0.10±0.01 0.09±0.004 1.00 (ns)

P (ppm) 8.54±0.39 6.90±0.40 2.40 (P<0.05)

C (g/dm3) 26.07±0.43 29.53±0.69 3.53 (P<0.0005)

Clay content 379.67±8.0 439.67±11.3 3.82 (P=0.0001)

Silt content 566.57±10.1 391.06±16.0 5.99 (P<0.0001)

Sand content 53.77±9.9 169.27±16.6 5.49 (P<0.0001)

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indicating high concentration (or seasonality) ofphenophases. All phenophases were more frequent(greater number of observations) in Gleysol forthis species. The mean leaf fall date was 25 daysearlier in Gleysol in relation to Cambisol (F=30.4,DF=1, P<0.001) and the other phenophases meandates did not differ between soils (F-test, P>0.05).Although mean angles were not significantly differentaccording to the F-test, all phenophases started atleast five days earlier in Gleysol when compared withCambisol. Intense (category 3) leaf fall and floweringwere more frequent in Gleysol than in Cambisol (G=14.24; DF=2; P=0.0008 and G=5.25; DF=1; P=0.02, respectively), whereas flushing and fruitingintensity frequencies did not differ between soil types(P>0.05).

Senna multijuga also revealed a seasonal patternfor all phenophases (Rayleigh test: all P<0.002).Flushing and leaf fall occurred continuously through-out the year, but flushing occurred mainly from

August to January; and leaf fall from April to Julyand November to December. Flowering continuedfrom January to March, and fruiting from March toOctober (Fig. 1). The concentration of phenophases(r) was comparatively low for flushing and leaf fall(approximately 0.3), suggesting low concentration ofphenophases. For reproductive phenophases (floweringand fruiting), the concentration (or seasonality) ofphenophases was higher (r>0.59; Table 2). For thisspecies, flushing and leaf fall were more frequent(more observations) in Gleysol, whereas floweringand fruiting were more frequent in Cambisol. The leaffall mean date was 19 days anticipated in Gleysol inrelation to Cambisol. The other phenophases meanangles did not differ between soils (F-test, P>0.05),although they also had a tendency of occurring earlierin Gleysol. Fruiting was more intense (higher frequencyof intensity category 3) in Cambisol (G=8.19; DF=2;P=0.01) whilst the intensity of other phenophases didnot differ between soil types (P>0.05).

Table 2 Results of circular analysis of phenology for two tree species (n=30), from two soil types in southern Brazil. All mean angles(u) are significant according to the Rayleigh test (P<0.05). * multimodal distribution (= not seasonal)

Citharexylum myrianthum Senna multijuga

Gleysol Cambisol Gleysol Cambisol

Flushing Observations (n) 377 371 495 475

Mean angle (u)±SD 345.8°±66.5° 354.6°±67.5° 315.6°±86.3° 316.9°±82.1°

Mean date (15 Dec) (24 Dec) (15 Nov) (17 Nov)

Length of mean vector (r) 0.51 0.50 0.32 0.36

Rayleigh test (P) <0.001 <0.001 <0.001 <0.001

Leaf fall Observations (n) 376 348 576 481

Mean angle (u)±SD 153.9°±58.4° 178.1°±56.3° * *

Mean Date (4 Jun) (29 Jun) * *

Length of mean vector (r) 0.60 0.62 0.09 0.1

Rayleigh test (P) <0.001 <0.001 * *

Flowering Observations (n) 43 13 68 90

Mean angle (u)±SD 315.4°±11.9° 321.9°±7.5° 36.6°±19.4° 38.0°±17.9°

Mean Date (15 Nov) (21 Nov) (6 Feb) (7 Feb)

Length of mean vector (r) 0.98 0.99 0.94 0.95

Rayleigh test (P) <0.001 <0.001 <0.001 <0.001

Fruiting Observations (n) 21 5 105 234

Mean angle (u)±SD 12.8°±21.0° 18.0°±11.2° 156.0°±55.3° 167.1°±59.0°

Mean Date (13 Jan) (18 Jan) (7 Jun) (18 Jun)

Length of mean vector (r) 0.96 0.98 0.62 0.59

Rayleigh test (P) <0.001 <0.001 <0.001 0.002

274 Plant Soil (2012) 354:269–281

Growth and phenology

All individuals of both species showed diameterincrements (0.6 to 108.5 mm in girth) after 12 months,except for two trees (both C. myrianthum) that did nothave any growth in during the study period Duringthe first 7 months following the commencement of theexperiment, rapid growth was observed for C.myrianthum growing in Cambisol, but noticeablyslower growth (about 75%) was observed for thesame species growing in Gleysol (Fig. 2). Conversely,growth of S. multijuga was similar between the twosites regardless of soil type (Fig. 2). The mean finalcumulative girth increment (± SE) for C. myrianthumwas 66.9±5.1 mm in Cambisol and 18.7±1.3 mm inGleysol. This represents, at the end of 12 months, atotal increase of 21.3±1.62 mm and 5.9 ±0.42 mm,respectively, in tree diameter at breast height (DBH),or 10.6±0.81 mm and 2.95±0.21 mm in radialincrement . Mean cumulative girth increment (± SE)for S. multijuga was 36.5±2.1 mm in Cambisol and

38.2±2.03 mm in Gleysol, corresponding to a total of11.6±0.67 mm and 12.2±0.65 mm in DBH of trees,or 5.8±0.33 and 6.1±0.32 mm in radial increment.The cumulative diameter growth of C. myrianthumwas greater in Cambisol than Gleysol (Table 3,Fig. 2), and the differences were due to interactionsbetween time and soil type. On the other hand, thegrowth of S. multijuga did not differ between soiltypes and time/soil type interactions, but differed inresponse to time (Table 3, Fig. 2).

Growth in DBH of C. myrianthum in Gleysol andCambisol was positively correlated to flushing andnegatively correlated to leaf fall (Table 4, Fig. 3a).Diameter increment in this species was also positivelycorrelated with fruit production, regardless of soiltype, but not to flowering in either soil (Table 4,Fig. 3a). Phenophases in S. multijuga were not soclosely related to DBH growth. Only flushing inCambisol was positively related to DBH growth. Allother correlations were not significant (Table 4,Fig. 3b).

Fig. 1 a Phenology (flushing, leaf fall, flowering and fruiting) of Citharexylum myrianthum in Cambisol, b Citharexylum myrianthumin Gleysol, c Senna multijuga in Cambisol and d Senna multijuga in Gleysol in southern Brazil

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Soil chemical composition, phenology and growth

For C. myrianthum, the principal components analysis(PCA) identified three main variation components(Fig. 4a), which, in total, explained 76.1% of the dataset variability. Component I contributed to 32.9% of thevariance (eigenvalue=1.97), component II contributed to22.8% (eigenvalue=1.37) and component III contributedto 20.4% (eigenvalue=1.22; not shown in the Fig 4a).

Greatest growth was observed in soils rich in Ca andMg, with higher silt content. Absence of leaves wasassociated with high Al content, whereas leaf fall,flowering and fruiting were associated, albeit weakly,with the clay and sand content of the soil (Fig. 4a).

For S. multijuga, PCA identified two mainvariation components, which, in total, contributed to62.9% of the data set variability. Component Icontributed to 39.1% of the variance (eigenvalue=1.95)

Table 3 Repeated-measuresanalysis between andwithin-subjects, containingeffects of time and soil typein the cumulative diametergrowth of two species insouthern Brazil

aG–G: Greenhouse–Geisser ε=0.048; H–F: Huynh–Feldt ε=0.049bG–G: ε=0.053; H–F: ε=0.055

Source of variation Num d.f. Den d.f. F Corrected P(G-G)

Corrected P(H-F)

Citharexylum myrianthum a

(a) Between-subjects

Soil 1 59 51.51

(b) Within-subjects

Time 22 38 11.05 0.001 0.001

Time × soil 22 38 7.65 0.001 0.001

Senna multijuga b

(a) Between-subjects

Soil 1 58 0.0006

(b) Within-subjects

Time 22 37 14.06 0.001 0.001

Time × soil 22 37 2.22 0.557 0.562

Fig. 2 Cumulative girth increment (mm) of Citharexylum myrianthum and Senna multijuga in two soil types in southern Brazil.Precipitation bars correspond to 15-days periods

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and component II contributed to 23.9% of the variance(eigenvalue=1.19) (Fig. 4b). For this species, stemgrowth, fruiting and flushing were associated withsoils rich in Ca, Mg and silt. Leaf fall in S. multijugawas also greatest in soils rich in Al and C (Fig. 4b).

Discussion

The phenological study of two tree species growing in thesame regional climate in Southern Brazil showed that,although general phenological patterns are approximatelythe same in distinct soil types, some phenophases differ infrequency, mean date and intensity. These findingssuggest that, besides the climatic factors previouslydescribed, edaphic conditions can also influence thephenology of tropical trees and must be considered whenanalysing tropical forest phenology.

Citharexylum myrianthum and Senna multijugawere highly seasonal for most phenophases andsoil types. Phenological seasonality is frequentlyrelated to day length and temperature in trees oftropical wet regions (Rivera and Borchert 2001;Wright and Van Schaik 1994). In the Atlantic RainForest, flushing and flowering occur in the warmerand rainy months and when days are longer; whereasleaf fall is more frequently observed in the dryer andcolder months and when days are shorter (Marquesand Oliveira 2004; Morellato et al. 2000), which wasalso the pattern observed for the two species studied.

Fruiting, a less predictable phenophase (Marques andOliveira 2008; Morellato et al. 2000), was seasonalfor both species, but occurred at different times of theyear (summer in C. myryanthum and winter for S.multijuga), probably due to differences in fruitmorphology and ripening (fleshy and dry fruits,respectively). Fleshy-fruited species are known tobear fruit mainly during the wet season, when themoisture levels are increased to allow fruit growthand maturation (Lieberman 1982) whereas wind andgravity-dispersed fruits mature mostly in the dryseason (Singh and Singh 1992).

Despite the marked seasonality of phenophases,some quantitative phenological aspects were due tocontrasting soil types (and species). Phenology differedaccording to soil types and, in general, the phenophasesof trees growing in Gleysol were more frequentlyobserved (almost all phenophases), more intense (leaffall) and occurred earlier (leaf fall) than in Cambisol.There are no obvious explanations for these differences,but they may have resulted in part from differentialaccess of trees to the soil nutrients and the water table. Itis possible that the Gleysol, which is moist and nutrientdeficient, promotes a higher leaf turnover, whereasreproductive capacity is not reduced. Phenophasesoccurrence (especially fruit production) of five treespecies of a tropical dry forest also tended to be higher ina site with ground water table closer to the surface(Valdez-Hernández et al. 2010).

Soil type determined quantitative differences inphenology of C. myrianthum and S. multijuga in thisstudy, but these differences were species-specific. Forexample, in C. myrianthum, leaf fall and floweringwere more intense in Gleysol (no differencesamong other phenophases) and for S. multijuga,fruiting was more intense in Cambisol. This may be aresult of several factors, including species growthrate, deciduousness and dispersion syndrome. Fastgrowing species can deplete soil resources faster thanslow growing species (Castro-Díez et al. 2003). Thismight affect phenology since the production of leaves,flowers and fruits may compete with stem growth fornutrients. In the richer and well drained Cambisol, C.myrianthum grew twice as much as S. multijuga (seediscussion below), and it is possible that this wasaffected by the resource partitioning within the tree(Lacointe 2000; Singh and Kushwaha 2006). Inaddition, storage of carbohydrates precedes leafabscission in deciduous tree species (such as C.

Table 4 Pearson’s correlation coefficients (r) after correctingfor temporal autocorrelation between diameter at breast height(DBH) growth and phenophases for each species in each soiltype in southern Brazil. Only significant correlations (P<0.05)are shown

Cambisol Gleysolr r

Citharexylum myrianthum

DBH growth and flushing 0.30 0.29

DBH growth and leaf fall −0.42 −0.36DBH growth and flowering – –

DBH growth and fruiting 0.56 0.84

Senna multijuga

DBH growth and flushing 0.40 –

DBH growth and leaf fall – –

DBH growth and flowering – –

DBH growth and fruiting – –

Plant Soil (2012) 354:269–281 277

myrianthum), and the energy required for leafproduction is expended only during a relatively shortperiod of the year (Callado et al. 2001; Tissue andWright 1995).

Girth increment of both species was positive;however, patterns varied depending on the soilcharacteristics. While C. myrianthum showed greaterdiameter increment when growing in the richer andwell drained soil (Cambisol), these factors appearedto have little effect on S. multijuga. C. myrianthum isprobably more sensitive than S. multijuga to soilwater excess and nutritional conditions, and suchspecies-specific differences were also detected inother tropical tree species (Worbes 1999; Yáñez-Espinosa et al. 2006; O’Brien et al. 2008; Couralet

et al. 2010). The girth increment for C. myrianthum(18.7 mm in Gleysol and 66.9 mm in Cambisol) andS. multijuga (38.2 mm in Gleysol and 36.5 mm inCambisol) was higher than that described by Lisiet al. (2008) for seasonal forest species in Brazil(4.9≥girth increment≤19.5 mm.year−1, 24 species)and by O’Brien et al. (2008) for moist forest speciesin Costa Rica (6.28≥girth increment≤34.5 mm.year−1, 10 species). These differences are probablydue to the fact that the species studied here arepioneer species that display concentrated stem growthduring the first years of their life cycle, what is alsoexplained by their low stem wood density (S.multijuga:0.48 g.cm−3, C. myrianthum: 0.6 g.cm−3)(Carvalho 2003).

Fig. 3 Precipitation (during the study period), girth increment and phenology of a Citharexylum myrianthum in Cambisol, bCitharexylum myrianthum in Gleysol, c Senna multijuga in Cambisol and d Senna multijuga in Gleysol in southern Brazil

278 Plant Soil (2012) 354:269–281

A relationship between girth increment and phenologywas detected in both species (and soil types) and has alsobeen reported for other tropical trees (Callado et al. 2001;Lisi et al. 2008; O’Brien et al. 2008). Correlationsbetween growth and flushing (in both species) suggestthat plants growing in non-seasonal climates are notrestricted to investing in stem growth at the same time(or in a short lag) that they invest in leaf production

(flushing), as has been described for species growingunder seasonal climates (Borchert 1999; Schöngart etal. 2002). Conversely, a negative relationship betweengrowth and leaf fall was only observed for deciduous C.myrianthum, probably because the cambial activity isreduced when trees are leafless (Shrestha et al. 2007;O’Brien et al. 2008). Besides leaf changes, fruiting(positive correlation in C. myrianthum) was alsocorrelated with stem growth. This suggests that theuse of resources for DBH growth does not limitreproduction in C. myritanthum (as measured byfruiting). Water and nutrients are factors that mayalso affect the relative carbon allocation to thedifferent plant parts, in particular, the shoot: root ratio(Lacointe 2000).

The considerable difference observed in the growth ofC. myrianthum in relation to soil types was supportedby PCA, since growth is correlated to high concentrationsof soil nutrients (specially Ca,Mg and P), low acidity andtoxicity (lower Al and C content) and high silt contents;all characteristics of Cambisol. Furthermore, Al wasalways associated with leaf fall, possibly due to itstoxicity (Joslin and Wolfe 1989). Elevated clay levelsand reduced silt levels promoted flushing and/orflowering in temperate climate species (Wielgolaski2001), and this may also be true for the speciesstudied here. Calcium content and pH, which seem topromote flushing and flowering in S. multijuga, werealso mentioned by Wielgolaski (2001) as factors thatmodify plant phenology. Additionally, nutrient acqui-sition may explain the opposite relationship of thenutrients Ca and Mg with leaf fall, as occurred in S.multijuga. Acquisition of these nutrients, for example,is driven by transpiration, so it should be roughlyproportional to the presence of leaves on the tree(Nord and Lynch 2009).

Tropical forest phenology has been traditionallyexplained from the perspective of the role ofclimate seasonality driving plant growth andreproduction (Fenner 1998; Bendix et al. 2006;O’Brien et al. 2008). This interpretation, while itallows us to understand the general phenologicalpattern for a specific region, does not explaindivergence between species sharing the same com-munity. Our findings show that fine adjustments infactors such as soil characteristics are also importantin the regulation of tree phenology. Soil wateravailability and nutrient content vary both spatiallyand temporally in tropical ecosystems (Longman and

Fig. 4 Principal Components Analysis (PCA) of soil character-istics and phenology of a Axes 1 (32.9%) and 2 (22.8%) forCitharexylum myrianthum and b Axes 1 (39.1%) and 2 (23.9%)for Senna multijuga in southern Brazil

Plant Soil (2012) 354:269–281 279

Jeník 1987) and potentially affect plant distribution.Thus, we suggest that factors working at differentlevels (both micro- and macro) must be consideredwhen explaining the phenological diversity of tropicalforests, and that this, in turn, is important inunderstanding species distribution (Chuine 2010).

Acknowledgements This work was supported by the BrazilianResearch Council (CNPq) [Solobioma Project, 690148/01-1] andthe German Federal Ministry of Education and Research [BMBFproject number 01LB0201]. M.C.M. Marques received aproductivity grant from CNPq [Processo 308597/2008-7]. Wethank Sociedade de Pesquisa em Vida Selvagem e EducaçãoAmbiental (SPVS) for their support and for allowing us to work atCachoeira Reserve and their staff for assistance during field work.

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