ORIGINAL PAPER

Dendrochronology of lianas of the Leguminosae familyfrom the Atlantic Forest, Brazil

Arno Fritz Neves Brandes • Claudio Sergio Lisi •

Claudia Franca Barros

Received: 1 November 2010 / Revised: 30 November 2010 / Accepted: 3 December 2010 / Published online: 29 December 2010

� Springer-Verlag 2010

Abstract Information about plant growth, development

and age forms the basis for understanding complex forest

ecological processes. Although lianas play an important

role in tropical forests, little is known about their growth

and development from either climatic or ecological per-

spectives. Therefore, we studied the growth rings in

Legume liana species collected in a mountainous Atlantic

Forest in southeastern Brazil. Four of the eight studied

species did not show cambial variants, three had a lobed

stem, and one had a furrowed xylem. Distinct growth rings

were observed in all species. Semi-ring porosity, marginal

parenchyma, fibrous zone and radially flattened latewood

cells were the main characteristic features of these

growth rings. Species without cambial variants, including

Dalbergia frutescens, Piptadenia adiantoides, P. micra-

cantha and Senegalia tenuifolia, showed very distinct

growth rings visible in macroscopic and microscopic anal-

ysis. Ring-width time series and cambial wound assessment

were performed to analyze periodicity and dendrochronol-

ogy. The species with cambial variants, S. grandistipula,

S. lacerans, S. martiusiana and S. pedicellata, also showed

distinct growth rings, however, sometimes barely detectable

or not detected at all. Cambial wounding, cross-dating and

climate-growth relationships indicated the annual nature of

growth rings in species without cambial variant. Cross-

dating between radii within one individual and between

individuals was successful, and the synchronized series

enabled us to build species chronologies and a mean chro-

nology. Climate-growth analysis revealed significant cor-

relations between chronologies and precipitation, indicating

that available moisture is the main factor determining

growth rates of lianas in the Atlantic forest.

Keywords Lianas � Tropics � Wood anatomy � Cambial

variants � Dendroecology � Growth rings � Leguminosae

Introduction

Lianas are an essential component of tropical forest eco-

systems. As such, lianas represent about 25% of the

abundance and species richness (Gentry 1991; Perez-Sali-

crup et al. 2004; Schnitzer and Bongers 2002). During the

past two decades awareness and interest in this growth

form have increased. However, in many respects, lianas are

still poorly understood, particularly liana ecology at the

species level and the response of lianas to the environment

(Gerwing 2004; Isnard and Silk 2009). In addition, little

attention has been given to the anatomy of lianas (Bamber

and Ter Welle 1994) and to the analysis of growth rings,

although a few older reports do exist (e.g., Schenck 1893).

So far, dendrochronological studies on lianas were devel-

oped only in temperate climate regions, especially with

Hedera helix (Garfi and Ficarrotta 2003; Heuze et al. 2009;

Nola 1997; Schnitzler and Heuze 2006; Verheyden et al.

Communicated by A. Braeuning.

Contribution to the special issue‘‘Tropical Dendroecology’’.

A. F. N. Brandes (&) � C. F. Barros

Instituto de Pesquisas Jardim Botanico do Rio de Janeiro,

Diretoria de Pesquisas, Laboratorio de Botanica Estrutural,

Rua Pacheco Leao 915, Jardim Botanico, Rio de Janeiro,

RJ 22460-030, Brazil

e-mail: arnofnb@jbrj.gov.br

C. S. Lisi

Departamento de Biologia, CCBS, Universidade Federal de

Sergipe, Av. Marechal Rondon s/n, Rosa Elze, Sao Cristovao,

SE 49100-000, Brazil

e-mail: arnofnb@jbrj.gov.br

123

Trees (2011) 25:133–144

DOI 10.1007/s00468-010-0529-3

2006), which have improved our understanding of liana–

host interactions and climate–growth relationships of liana

species. Another notable growth ring analysis in lianas was

done at the beginning of the twentieth century, and it

reported the estimated age in Clematis vitalba L. (Kann-

giesser 1906 apud Schweingruber and Poschlod 2005).

Information about growth rings in trees is available, but

it is scarce for other growth forms. Schweingruber and

Poschlod (2005) studied growth rings in herbs and shrubs,

proving the great value of dendrochronology for the tem-

poral understanding of other growth forms and for eco-

logical studies. Nonetheless, studies reporting the growth

and age of lianas are sparse, and they are mostly restricted

to indirect methods (Ewers et al. 1991; Gerwing 2004;

Nabe-Nielsen 2002; Putz 1990). Therefore, dendrochro-

nology may be a valuable tool in future research with

lianas. Specifically, growth ring analysis can contribute

chronological information that can be used for growth

analysis, wood production, population age structure and

forest dynamics, liana–host interaction, forest manage-

ment, as well as conservation and restoration studies

(Braker 2002; Brienen and Zuidema 2006; Eckstein et al.

1995; Grau et al. 2003; Jacoby 1989; Nola 1997; Priya and

Bhat 1999; Worbes 2002; Worbes et al. 2003). Still, these

analyses can only be performed for lianas if anatomical and

dendrochronological studies are also performed.

In the past few decades, many dendrochronological

studies of tropical tree species have reported the occurrence

of seasonal growth rings that are correlated, in many cases,

with precipitation or some other seasonal climatic varia-

tions (Baas and Vetter 1989; Bormann and Berlym 1981;

Eckstein and Baas 1999; Eckstein et al. 1995). In Brazil,

some studies were developed in the Amazon Forest

(Botosso 1984; Schongart et al. 2005; Schongart 2008; Vetter

and Botosso 1989; Worbes 1985, 1989) and the Atlantic

Forest biomes (Callado et al. 2001a, b, 2004; Estrada et al.

2008; Lisi et al. 2008; Oliveira et al. 2009, 2010; Seitz and

Kanninen 1989). These studies and others showed the via-

bility of growth ring research in the tropics, and an excellent

thematic overview was presented by Worbes (2002).

Lianas are woody climbers whose development begins

on the ground. However, since their ability to self-support

dissipates with growth, they need additional support in

order to ascend to the canopy and thrive in mature forests

(Gentry 1991; Gerwing et al. 2006). Most lianas show

cambial variants that are variations of cambial conforma-

tions, products and number. The most common condition

in woody species is a single and cylindrical cambium,

which produces secondary xylem (internally) and second-

ary phloem (externally) with similar amounts around stem

circumference (Carlquist 2001). Some species of lianas

do not show cambial variants (Carlquist 1991, 2001;

Caballe 1993), but frequently, such lianas do show wood

anatomical tendencies correlated to the habit, e.g., wide

vessels, higher conductive area, low proportion of sup-

portive tissues, and high amount of parenchyma (Brandes

and Barros 2008; Carlquist 1991). Only a few papers have

reported the growth ring anatomy of lianas (Baas and

Schweingruber 1987; Carlquist 1995; Gasson and Dobbins

1991; Lima et al. 2010; Schweingruber 2007).

Leguminosae are the third largest family of climbers in the

New World. Additionally, along with Bignoniaceae, they

represent the dominant climbing families in Neotropical

lowland forests (Gentry 1991). Lianas compete with trees for

nutrients, light and water (Gentry 1991). As a consequence of

their thin stems and low-density wood, lianas capture less

carbon than tree species. Moreover, infestations of lianas

inhibit the regeneration of forest trees which also reduces the

amount of carbon that would otherwise be assimilated in the

biomass (Schnitzer and Bongers 2002).

In this study, we analyzed eight liana species from a

well-preserved remnant of the Atlantic Forest located in a

mountainous region (Serra da Mantiqueira–Itatiaia Massif).

These species represent almost all legume lianas previously

recorded in this place and registered in the Programa Mata

Atlantica database. In the course of our study, we asked (1)

if Atlantic Forest lianas have growth rings, (2) what ana-

tomical features distinguish such growth rings, (3) what

periodicity applies to the formation of growth rings, and (4)

whether ring-width patterns reflect precipitation variations.

Materials and methods

Study site

The samples were collected from the Parque Nacional do

Itatiaia, municipality of Itatiaia, State of Rio de Janeiro,

southeastern Brazil. The park is located between the geo-

graphical coordinates of 22�150–22�300 S and 44�300–44�450 W, with an area of 28,155.97 ha (Morim 2006). Its

type of vegetation can be classified as Atlantic Forest

(Oliveira-Filho and Fontes 2000). Most of the Parque

Nacional do Itatiaia lies in a mountainous area with several

well-delimited climatic and vegetation belts related to

altitudinal gradients. The samples were taken between 700

and 1,100 m elevation. At 816 m elevation, the annual

mean precipitation is around 1,700 mm, and the annual

mean temperature is 18.2�C. The warm and rainy season is

between December and February, when 50% of the annual

precipitation occurs. January is the rainiest month, with a

mean of 290 mm. During these months, the mean tem-

perature is 20.8�C. The dry cold season is between June

and August, with only 5% of the annual precipitation. The

driest month is June, with a mean of 32 mm. During these

months, the mean temperature is 15.1�C, but an absolute

134 Trees (2011) 25:133–144

123

minimum of 0�C has been registered (Segadas-Vianna and

Dau 1965).

The precipitation data used in our dendrochronological

analysis were collected during 1986–2005 at the meteoro-

logical station of Resende (22� 270 S, 44� 260 W) and were

provided by the Instituto Nacional de Meteorologia

(INMET) (National Institute of Meteorology)—Sixth Meteo-

rological District (Fig. 1). The meteorological station of

Resende is 453 m elevation, around 18 km distance from

study site, and the precipitation data are very similar of study

site (Segadas-Vianna and Dau 1965).

Wood anatomy

We sampled 57 lianas from eight Leguminosae species

(subfamilies Mimosoideae and Papilionoideae). Of these,

four had cambial variants and four did not. The cambial

variants that occur in these species are the non-fragmented

lobed stem and the xylem-furrowed stem (Brandes and

Barros 2008) (Table 1). Both are products of a single

cambium with unequal activity on some regions (Carlquist

2001).

For this study, we selected lianas larger than 2.0 cm in

diameter at approximately 1.3 m above the ground, without

wounds or deformations at this height. The number of

samples per species differed because of the difficulty in

finding individuals with the characteristics cited above and

the different abundance of each species. For each indi-

vidual sampled, a voucher was collected, representing

reproductive and other vegetative parts as well. They were

stored at the herbarium Jardim Botanico do Rio de Janeiro

(RB).

Wood samples of the stems were collected at approxi-

mately 1.3 m above the ground. We collected partial or

complete cross-sections, including bark, wood and pith.

Blocks were polished for macroscopic observation through

an Olympus SZ11 stereomicroscope. The images were

taken by a photographic camera (Olympus C5050) attached

to the same stereomicroscope and analyzed with Image Pro

Plus version 3.0 for Windows. For light microscopy,

boiling water and glycerine were used to soften part of the

blocks; 12 to 30 lm-thick sections were made in trans-

versal, tangential and radial plains, using a Spencer 860

sliding microtome. After cleaning, they were stained with

safranin and astra blue (Bukatsch 1972), dehydrated,

and mounted on Permount resin in permanent slides.

Slides were observed using an Olympus BX50 microscope,

and images were captured with Image Pro Plus version 3.0

for Windows linked to the microscope through a Media

Cybernetics CoolSNAP-Pro video camera. The Zeiss

0

25

50

75

100

125

150

0

50

100

150

200

250

300

JAN

FE

B

MA

R

AP

R

MA

Y

JUN

JUL

AU

G

SE

P

OC

T

NO

V

DE

C

Tem

pera

ture

(C

)

Pre

cipi

tatio

n (m

m)

°

Fig. 1 Mean (1986–2005) monthly precipitation (bars) and temper-

ature (line) for Resende-RJ Meteorological Station

Table 1 Studied species, anatomical features of the growth rings, cambial variant types, analyzed samples RBw

Species Anatomical features

of growth rings

Cambial

variants

Samples RBw

Mimosoideae

Senegalia grandistipula 1a, 3a, 4a, 5a Lobed stem 8,627, 8,643, 8,644

Senegalia lacerans 1a, 2a, 3a, 4a, 5a Xylem furrowed 8,607, 8,608, 8,610, 8,611, 8,612, 8,624, 8,625,

8,629, 8,631, 8,641, 8,642

Senegalia martiusiana 1a, 3a, 5a Lobed stem 8,653, 8,655, 8,656, 8,657, 8,659, 8,660, 8,661

Senegalia pedicellata 1a, 3a, 5a Lobed stem 8,609, 8,615, 8,662, 8,663, 8,664

Senegalia tenuifolia 1, 2, 3a, 4a Absent 8,628, 8,658

Piptadenia adiantoides 1a, 2, 3a, 4 Absent 8,634, 8,635, 8,636, 8,646, 8,647, 8,648, 8,652

Piptadenia micracantha 1, 2, 3, 4a Absent 8,605, 8,632, 8,637, 8,645, 8,650, 8,651, 8,654

Papilionoideae

Dalbergia frutescens 1, 2, 3a, 4a Absent 8,606, 8,613, 8,614, 8,616, 8,617, 8,618, 8,619,

8,620, 8,621, 8,622, 8,623, 8,626, 8,630, 8,633, 8,649

1 semi-ring-porous, 2 marginal parenchyma, 3 fiber zone, 4 radially flattened latewood cells, 5 pith fleck and traumatic canalsa Features not present in all growth rings

Trees (2011) 25:133–144 135

123

polarized light microscope with red filter k was also used to

observe calcium oxalate crystals.

Wood samples and permanent slides were incorporated

into the wood collection from the Jardim Botanico do Rio

de Janeiro (RBw). The terminology complies with the

IAWA Committee (1989).

Cambial wounding

The technique of repeated wounding of the vascular cam-

bium, the so-called ‘‘Mariaux Window’’ (Mariaux 1967),

was used to analyze the characteristics of the secondary

xylem produced during the year, as well as confirm the

presence of annual growth rings. In the procedure, the bark

and the cambium at 0.5 cm in width and approximately

5 cm in height were removed, and a Bordeaux mixture was

applied to avoid the action of pathogenic microorganisms.

Four markings were performed throughout the year (one in

each season), and 1 year after the first wound, a section of

the area appointed for analysis was collected. Fifteen

individuals of Dalbergia frutescens, seven Piptadenia

adiantoides, seven Piptadenia micracantha, and two

Senegalia tenuifolia were analyzed.

Dendrochronology

For dendrochronological studies, samples of 29 lianas from

Piptadenia adiantoides, Piptadenia micracantha, and

Dalbergia frutescens species were analyzed (Table 2).

Senegalia tenuifolia, one species that shows a distinctive

growth ring, was not used because we could not find

enough specimens to study.

Four rays (temporal series) were measured per liana.

Growth ring measurements and image processing were

performed with Image Pro Plus version 3.0 for Windows,

with a precision of 0.01 mm. The cross-dating of the

temporal series was performed, following the recom-

mendations of Stokes and Smiley (1996) and Fritts (1976)

and was supported by graphs and statistical analysis. The

COFECHA (Holmes 1983) program was used to verify

the precision of the measurements and the cross-dating.

The growth ring series was standardized (de-trended)

using a spline curve (cubic smoothing spline 50%

wavelength cutoff; 5 years rigidity of spline for filtering).

A flexible spline was used to minimize undesirable signal

(e.g., competition and local disturbance). The flexible

spline is an appropriate de-trending method for trees from

closed-canopy stands, as previously reported (Brienen and

Zuidema 2005; Cook and Peters 1981), and it may also

be applicable to lianas, taking into account ecological

conditions. For each of these species, a reference, or

master, chronology was produced, calculating the mean

value of all standardized series (de-trended series). Each

temporal series was tested in relation to the reference

chronology. A final growth ring chronology was produced

for each species by averaging the best correlated series.

Successful cross-dating indicates the influence of an

external growth factor on tree growth in a region. By

identifying the common signal that represents the climatic

factor in a growth rings time series, it is possible to retain

the highly correlated series in the final chronologies.

Finally, a mean reference chronology (master chronology)

of lianas from the Parque Nacional de Itatiaia was pro-

duced from the species chronologies. For the time series

analysis and building the chronologies, software from the

Dendrochronology Program Library (Holmes 1994) was

used.

Pearson correlation analyses were performed between

the chronologies produced and annual precipitation (Janu-

ary–December), monthly precipitation and the precipitation

total of December–January–February (summer), March–

April–May (autumn), June–July–August (winter), and

September–October–November (spring). The correlation

analyses were executed using Statistica 8.0 software.

Correlation analysis is also the most common method to

measure the association between growth rings and climate

(Fritts 1976). The methods described above for the treat-

ment and analysis of data are an attempt to follow the

Table 2 Ring-width data

Chronology Number

of lianas

Number

of series

Intercorrelation Sensitivity Chronology

extension

Samples RBw

Mimosoideae

Piptadenia adiantoides 7 (7) 28 (21) 0.69 0.57 1993–2005 8,634, 8,635, 8,636, 8,646, 8,647, 8,648, 8,652

Piptadeniamicracantha

7 (6) 28 (14) 0.48 0.37 1987–2005 8,605, 8,632, 8,637, 8,645, 8,650, 8,651, 8,654

Papilionoideae

Dalbergia frutescens 15 (15) 60 (37) 0.50 0.51 1970–2005 8,606, 8,613, 8,614, 8,616, 8,617, 8,618, 8,619, 8,620,

8,621, 8,622, 8,623, 8,626, 8,630, 8,633, 8,649

Species, number of lianas before and after cross-dating (), number of series before and after cross-dating (), intercorrelation, sensitivity,

chronology extension, and analyzed samples RBw

136 Trees (2011) 25:133–144

123

methodological steps recommended by Braker (2002)

which visualize, explore, test, and relate data.

Results

Wood anatomy

Distinct growth rings were observed in all studied species.

The four species without cambial variants revealed easily

detectable and well-delimited growth rings (Figs. 2a–d,

3a–d). Anatomical ring boundaries of species with cambial

variants were sometimes detectable, sometimes barely

detectable rings or even undetectable (Figs. 4a–d, 5a–d).

The most evident anatomical features of growth rings were

semi-ring porosity, fibrous zones, marginal parenchyma

bands, and radially flattened latewood cells. Species with

cambial variants also exhibited traumatic canals and pith

flecks within the growth boundaries. The features listed

above were not present concomitantly in all growth rings

(Table 1). In combination, the macroscopic and micro-

scopic observations enabled a proper distinction of growth

rings. Usually, the macroscopic view facilitated the

detection of growth ring boundaries because of a broader

field view.

Among the species without cambial variants, Dalbergia

frutescens (Vell.) Britton var. frutescens (subfamiliy Pap-

illionideae) (Figs. 2a, 3d), P. adiantoides (Spreng.) J. F.

Macbr. (Figs. 2b, 3b), P. micracantha Benth. (Figs. 2c, 3c)

and Senegalia tenuifolia (L.) Britton and Rose (subfamily

Mimosoideae) (Figs. 2d, 3a) exhibited semi-ring porosity,

marginal parenchyma, fibrous zones in latewood, and

radially flattened latewood cells. However, a fibrous zone

and radially flattened latewood cells were not present in all

growth rings of D. frutescens (Figs. 2a, 3d) and S. tenui-

folia (Figs. 2d, 3a). Within P. adiantoides (Figs. 2b, 3b)

some growth rings did not present semi-ring porosity and

fiber zone. In P. micracantha (Figs. 2c, 3c) few growth

rings showed radially flattened latewood cells. Abundance

of prismatic calcium oxalate crystals was observed near

growth ring boundaries of all Mimosoideae without cam-

bial variants.

The other studied species of genus Senegalia revealed

cambial variants. Although all species exhibit distinct

growth ring boundaries, they are sometimes difficult to

detect or, in some stem portions, even undetectable. The

main distinctive features of growth rings for this genus

included semi-ring porosity and fibrous zone. S. grandi-

stipula (Benth.) Seigler and Ebinger revealed a square-like

lobed stem cambial variant. In addition to the features

mentioned above, some growth rings had radially flattened

latewood cells, pith flecks and traumatic canals (Figs. 4a, 5a).

S. lacerans (Benth.) Seigler and Ebinger showed a

xylem-furrowed cambial variant. Beyond the features for

genus, some growth rings had marginal parenchyma,

radially flattened latewood cells, pith flecks and traumatic

canals (Figs. 4c, 5b). S. martiusiana (Steud.) Seigler and

Ebinger, a lobed stem cambial variant with cylindrical

lobes, presented the features cited above for the genus,

including pith flecks and traumatic canals (Figs. 4d, 5c).

Finally, S. pedicellata (Benth.) Seigler and Ebinger, a

lobed stem cambial variant with flattened lobes, showed

pith flecks and traumatic canals (Figs. 4b, 5d). Occasion-

ally, semi-ring porosity and fibrous zone were also

presented.

Cambial wounding

The four studied species showed a clear periodicity in

radial growth, with the formation of one growth ring per

year. At the beginning of the rainy season in September,

the cambium produced large vessels. As the dry season

approached, vessels with gradually smaller diameters were

Fig. 2 Transverse sections (light microscopy) of a D. frutescens,

b P. adiantoides, c P. micracantha, d S. tenuifolia. Arrows indicate

growth ring boundaries, scale bars 100 lm

Trees (2011) 25:133–144 137

123

produced (Fig. 6a–d). Through the experimental delinea-

tion employed, it was not possible to determine whether the

vascular cambium became inactive for a determined

period; however, we noticed that the products of the vas-

cular cambium (cells composing the secondary xylem) and

the size of these cells varied throughout the year.

Dendroecology

All studied species included discontinuous rings (wedging

rings), which may cause serious difficulties for proper syn-

chronization between tree-ring series. Since we mainly used

complete or partial sections of liana stems and not samples

collected with an increment borer, it was possible to validate

the cross-dating of radii and to identify discontinuous rings

with a certain ease and precision. Both, graphical analysis

and statistics provided by COFECHA software were very

important to synchronize the measured growth ring series.

Thus, the cross-dating procedure was successful between

most radii and individuals, as indicated by a high intercorre-

lation between the tree-ring series of 0.69 for P. adiantoides,

0.50 for D. frutescens and 0.48 for P. micracantha (Table 2),

for which three growth ring chronologies were produced

(Fig. 7). The mean sensitivity was 0.57 in P. adiantoides, 0.51

in D. frutescens and 0.37 in P. micracantha (Table 2),

revealing a high inter-annual growth variability that might be

related to climate sensitivity (Fritts 1976). Finally, a mean

chronology of lianas from Itatiaia was built by averaging the

three individual species chronologies (Fig. 7d).

Correlation analysis between the individual species

chronologies and total annual precipitation revealed sig-

nificant correlation coefficients for D. frutescens (r = 0.63;

p = 0.003), P. adiantoides (r = 0.53; p = 0.062) and

P. micracantha (r = 0.39; p = 0.096), respectively. The

correlation between the mean chronology of lianas from

Itatiaia and total annual precipitation was even higher than

Fig. 3 Transverse sections

(stereomicroscopy) of

a S. tenuifolia, b P. adiantoides,

c P. micracantha,

d D. frutescens. Arrows indicate

growth ring boundaries, scalebars 1 mm

Fig. 4 Transverse sections (light microscopy) of a S. grandistipula,

b S. pedicellata, c S. lacerans, d S. martiusiana. Arrows indicate

growth ring boundaries, scale bars 100 lm

138 Trees (2011) 25:133–144

123

that found for the individual species (r = 0.66; p = 0.001)

(Table 3, Fig. 7).

Highest correlation coefficients of the chronologies with

monthly and seasonal precipitation were generally

observed for the summer months of the previous growing

season and the spring months of the current growing sea-

son. Lowest correlations were observed for autumn and

winter, except for P. micracantha. The P. adiantoides

chronology was significantly correlated with precipitation

of February of the previous growing season, October of the

current season, and summer of the previous growing season

(Table 3). For D. frutescens, positive correlations occurred

with January of the previous growing season, September of

the current season, and summer of the previous growing

season. In contrast to these species, growth of P. micra-

cantha was positively correlated with June and July of the

previous growing season, winter of the previous growing

season and May of the current growing season (Table 3,

Fig. 7).

Discussion and conclusions

The anatomical results demonstrate that P. micracantha,

P. adiantoides, S. tenuifolia and D. frutescens form clear

annual rings, which is fundamental for precise ring counting

and ring-width measurements. In contrast, Senegalia gran-

distipula, S. lacerans, S. martiusiana and S. pedicellata are

species with cambial variants that may form distinct growth

rings, which are sometimes indistinct and difficult to detect

or absent in some stem portions. Beyond that, species which

show lobate growth should not be used in an analysis of

growth rings (Worbes 1989). Growth rings were detected in

other liana species, but they were rarely analyzed in detail.

Baas and Schweingruber (1987) observed that climbers from

temperate climates show ring porous and semi-ring porous

wood anatomy. Other examples of lianas with distinct

growth rings from temperate and tropical regions were pre-

sented by Schweingruber (2007). Gasson and Dobbins

(1991) report distinct growth rings in lianas from the genera

Capsis, Schlegelia nine other genera of the Bignociaceae

family. A detailed description of growth rings in tropical

lianas from the Bignonieae tribe was provided by Lima et al.

(2010). In lianas from Venezuela, growth rings marked by

marginal parenchyma were observed in Anomospermun

schomburgkii Miers (Menispermaceae) and Strycnos

brachistantha Standley (Loganiaceae) (Araque et al. 2000).

The main anatomical markers for growth rings observed by

these authors were semi-ring porosity, parenchyma bands,

radially flattened latewood fibers and radially shorter ray

cells. Semi-ring porosity and marginal parenchyma were

also important features observed in the present study. They

were present in all studied species without cambial variants

and having a distinct growth ring. These studies show that

growth rings in lianas are not exceptional and have common

anatomical features.

Based on the evidence from wood anatomy, vascular

cambium wounds (Worbes 1995), cross-dating, intercor-

relation between ring-width time series, correlations

between chronologies and precipitation data (Stahle 1999),

as well as the seasonal rainfall regime of the study area, we

conclude that growth rings of the studied species are

formed annually. According to Worbes (1995), areas with a

dry season of 3 months or more with a monthly precipi-

tation below 60 mm are favorable for the occurrence of

species that form annual growth rings. This holds true for

Fig. 5 Transverse sections

(stereomicroscopy) of

a S. grandistipula,

b S. lacerans, c S. martiusiana,

d S. pedicellata. Arrowsindicate growth ring boundaries,

scale bars 1 mm

Trees (2011) 25:133–144 139

123

the Parque Nacional do Itatiaia, where the dry season lasts

3 months. Supporting this evidence, Schweingruber (2007)

reported growth rings in tropical lianas from seasonal cli-

mates. The occurrence of annual growth rings and annual

growth seasonality was also reported in arboreal species

from the Atlantic Forest (Callado et al. 2001b; Estrada

et al. 2008; Lisi et al. 2008; Oliveira et al. 2009, 2010), in

lianas from the Atlantic Forest of the Bignoniaceae family

(Lima et al. 2010) and in lianas of the Leguminosae from a

Mexican tropical rainforest (Leon-Gomez and Monroy-Ata

2005).

The successful cross-dating and the high intercorrelation

values between ring-width series showed that liana species

of this study share a common growth pattern and respond

to a common environmental signal. Importantly, the den-

drochronological results suggest that the growth of tropical

lianas is sensitive to variations in local climate. Specifi-

cally, positive correlations between the chronologies and

annual, monthly and seasonal precipitation were observed.

Strongest relationships were observed between chronolo-

gies and annual precipitation. Precipitation was also

reported as the most important factor for the secondary

growth of tropical tree species (Worbes 1989). Schongart

et al. (2006) studied six arboreal species in Africa, among

them four species of the Leguminosae family and observed

significant correlations (p \ 0.01) between growth rates

and annual precipitation. In a tropical dry forest in Costa

Rica, Enquist and Leffler (2001) observed a significant

relationship between growth of the evergreen Capparis

indica and annual precipitation. Fichtler et al. (2004)

studied two leguminous species from a semiarid forest in

Namibia and found a positive relationship between a

Burkea africana chronology and the rainfall total of all

months to the growth year (August–July). Worbes (1999)

studied several species in Venezuela and detected a high

correlation coefficient (r = 0.75; p \ 0.05) of annual pre-

cipitation with the mean chronology of all studied species.

Besides, significant correlations of 0.62 (p \ 0.05) and

0.68 (p \ 0.05) between chronologies of Cedrela odorata

and Terminalia guianensis and annual rainfall were found.

Similar to these reports, the present study demonstrates that

a mean chronology of several species shows a higher

relationship to annual precipitation than chronologies of

individual species.

Climate during certain periods of the year may have a

greater influence on growth than during other periods

(Fritts 1976). For example, D. frutescens and P. adianto-

ides show significant correlations with precipitation during

summer of the previous growing season and with some

spring months of the current growing season. On the other

hand, P. micracantha shows significant correlations with

precipitation in winter of the previous growing season.

Thus, in some of the studies noted above, a controversial

picture arises with correlation between growth and pre-

cipitation between dry and rainy seasons, as well as with

transitional months.

Brienen and Zuidema (2005) related tree growth in a

Bolivian rain forest with rainfall. While they did not find

any correlation between chronologies and annual precipi-

tation, they documented a positive relationship between

tree growth and precipitation during certain periods of the

year. Three species showed a relationship to precipitation

at the beginning of the rainy season, one species with

precipitation in the transition from the rainy to the dry

Fig. 6 Macroscopic cross-sections of cambial wounds set in Decem-

ber 2005. Collection of the samples was conducted after 1 year

(December 2006). a S. tenuifolia, b P. adiantoides, c P. micracantha,

d D. frutescens. Scale bars 1 mm

140 Trees (2011) 25:133–144

123

season, and two species were correlated with precipitation

in the transition period from dry to rainy. Dunisch et al.

(2003) observed the highest correlation coefficients of

Swietenia macrophylla with rainfall in November,

December, January and May, and in Cedrela odorata in

March, April and May, and rainy months of the previous

growth period. Fichtler et al. (2004) studied the leguminous

trees Burkea africana and Pterocarpus angolensis in

Namibia. P. angolensis from Katima Mulilo was highly

correlated to rainfall in April and total precipitation of

April and May, the beginning of the dry season. The

chronology B. africana from Ondangwa responded to

rainfall in January and February, the rainy season, and the

chronology from Katima Mulilo responded to rainfall of

August, September and November, the end of dry season,

as well as the total rainfall for October and November, the

beginning of the rainy season. Eshete and Stahl (1999)

observed high correlations in Acacia species with precipi-

tation total from June to September, the rainy season. In

Venezuela, Worbes (1999) noticed significant correlations

between dry season precipitation and five species and

between rainy season precipitation and four species stud-

ied. Two of these species showed correlations with both the

dry season and rainy season rainfall. Enquist and Leffler

(2001) noticed correlations of growth of Genipa americana

with the precipitation of the dry season and of Capparis

indica with the rainy season of the previous year. The

different reaction pattern of the two species is explained by

individualistic response and differences in the root system.

Regarding lianas, Lima et al. (2010) detect cambial activity

in Tynanthus cognatus (Bignoniaceae) only at the end of

the rainy season. To summarize, precipitation is an

important climatic factor related to the growth of woody

species in the tropics, being it trees or lianas. Moreover, it

50

150

250

350

450

- 4

- 3

- 2

- 1

0

1

2

3

Pre

cipi

tatio

n (m

m)

Inde

xed

ring

wid

th

P. adiantoides February precipitation

0

10

20

30

1970

1972

1974

1976

1978

1980

1982

1984

1986

1988

1990

1992

1994

1996

1998

2000

2002

2004S

ampl

ing

dept

h

Year

500

1000

1500

2000

2500

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-3

-2

-1

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2

Pre

cipi

tatio

n (m

m)

Inde

xed

ring

wid

th

Lianas Itatiaia Total annual precipitation

020406080

1970

1972

1974

1976

1978

1980

1982

1984

1986

1988

1990

1992

1994

1996

1998

2000

2002

2004S

ampl

ing

dept

h

Year

0

50

100

150

200

250

- 4

- 3

- 2

- 1

0

1

2

3

Pre

cipi

tatio

n (m

m)

Inde

xed

ring

wid

th

P. micracantha Winter precipitation

0

10

20

1970

1972

1974

1976

1978

1980

1982

1984

1986

1988

1990

1992

1994

1996

1998

2000

2002

2004S

ampl

ing

dept

h

Year

500

1000

1500

2000

2500

- 4

- 3

- 2

- 1

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cipi

tatio

n (m

m)

Inde

xed

ring

wid

th

D. frutescens Total annual precipitation

010203040

1970

1972

1974

1976

1978

1980

1982

1984

1986

1988

1990

1992

1994

1996

1998

2000

2002

2004S

ampl

ing

dept

h

Year

a b

c d

Fig. 7 Ring-width chronologies and their sampling depth and

comparison with precipitation. a D. frutescens and total annual

precipitation, b P. adiantoides and February precipitation,

c P. micracantha and winter precipitation, d Mean chronology of

lianas from Itatiaia and total annual precipitation

Trees (2011) 25:133–144 141

123

appears that growth can be related to precipitation of either

a short period (seasons or months) or a long period (year).

In an interesting study about the abundance patterns of

lianas, Schnitzer (2005) found that lianas are more abun-

dant in dry seasonal forests. He suggested that lianas can

maintain their growth activity during the dry season, by

gathering enough water resources with their deep roots to

continue their photosynthesis and growth. Thus, lianas

confer an adaptive advantage over trees. This community-

level explanation can be supported by our results for

P. micracantha. At the same time, however, the present study

shows that the growth of D. frutescens and P. adiantoides is

confined mostly to the rainy season. These results corroborate

Enquist and Leffler’s (2001) hypothesis of individualistic

response to climate, as well as the idea that some tropical

assemblages may in fact be structured by species-specific

differences in soil–water use.

It is possible that lianas respond well to precipitation

variations, as a result of their peculiarities regarding the

conduction of sap in the xylem. In lianas, vessels of large

diameter are a common feature (Carlquist 1985; Ewers

et al. 1990; Ewers et al. 1991), which is also a character-

istic in the species of this study (Brandes and Barros 2008).

The large liana vessels are more susceptible to embolism

during the dry season than vessels of smaller diameter

(Zimmermann 1983). During the dry season, drought-

sensitive species show a reduction in their growth in

comparison with drought-tolerant species, and in the rainy

season, they show an increase in growth. Thus, it is

expected that drought-sensitive species show a better

correlation with climatic parameters, especially during the

rainy season (Gebrekirstos et al. 2008). While precipitation

is an important factor for the secondary growth of liana

species, other environmental factors, such as temperature,

solar radiation, day length and phenological phases, may

also influence the formation of growth rings (Callado et al.

2001b; Clark and Clark 1994; Devall et al. 1995; Oliveira

et al. 2009, 2010; Schweingruber 2007). Their relevance

for controlling growth rings in lianas has to be tested in

further studies.

In this study, wedging rings were detected in all species

during the cross-dating procedure of time series of radial

growth series within individuals. The analysis of stem discs

facilitated the detection of problematic growth rings

(Worbes 1999). Absent and wedging rings may lead to age

underestimation and hence growth overestimation (Lorimer

et al. 1999). The presence of wedging rings was reported

from several neotropical arboreal species, and it was

observed that they are more common in small understory

trees growing under competition with diminished light

conditions (Lorimer et al. 1999; Worbes 2002). Ecological

studies on lianas report a strong competition pressure with

trees for nutrients, light, and water during the dry season

(Schnitzer and Bongers 2002). The presence of wedging

rings documented in our study reinforces the idea that

lianas are subject to competition processes which may

initiate alterations of cambial activity in determined stem

regions.

Thus, we conclude that the lianas studied do have growth

rings, detectable by wood anatomical features like semi-ring

Table 3 Correlation coefficients between chronologies and monthly precipitation (Jan–Aug previous growing season; Sep–Jun current growing

season), total precipitation in summer (SUM), autumn (AUT), winter (WIN), spring (SPR) and total annual precipitation (TAP)

Previous growing season

Jan Feb Mar Apr May Jun Jul Aug

Piptadeniaadiantoides

0.33 0.57 -0.18 -0.21 0.11 -0.24 0.34 -0.12

Piptadeniamicracantha

0.36 0.12 0.14 0.27 -0.24 0.56 0.52 -0.16

Dalbergiafrutescens

0.51 0.37 -0.06 0.11 0.30 0.05 -0.01 -0.41

Lianas Itatiaia 0.56 0.31 -0.03 0.21 0.06 0.32 0.31 -0.36

Current growing season

Sep Oct Nov Dec Jan Feb Mar Apr May Jun SUM AUT WIN SPR TAP

Piptadenia adiantoides 0.32 0.53 -0.21 0.42 -0.24 -0.28 0.43 0.50 -0.32 0.11 0.52 -0.21 0.04 0.28 0.53

Piptadenia micracantha 0.17 -0.44 -0.06 0.34 -0.32 -0.30 -0.03 0.07 0.45 -0.41 0.13 0.25 0.54 -0.17 0.39

Dalbergia frutescens 0.55 0.11 0.22 0.00 -0.18 -0.28 0.32 -0.11 -0.57 -0.01 0.58 0.12 -0.25 0.38 0.63

Lianas Itatiaia 0.49 0.01 0.05 0.17 -0.37 -0.34 0.24 -0.02 -0.16 0.25 0.50 0.15 0.12 0.21 0.66

Significant correlations: Italic value p \ 0.08; Bold value p \ 0.05; Bold italic value p \ 0.005

142 Trees (2011) 25:133–144

123

porosity, fibrous zone, marginal parenchyma and radially

flattened latewood cells. The four species without cambial

variants had well-delimited growth rings, which were easily

detectable. The periodicity of growth ring formation and

correlation of ring-width time series proved the annual nat-

ure of their growth rings. Climate-growth analyses revealed

that growth is conditioned by precipitation. Future ecologi-

cal studies, particularly dendroecological studies, will be an

important source of information about the role played by

lianas in the Atlantic Forest of Brazil and in other tropical

forest ecosystems.

Acknowledgments Our thanks go to the Instituto de Pesquisas

Jardim Botanico do Rio de Janeiro, Petrobras and CAPES (Coorde-

nacao de Aperfeicoamento de Pessoal de Nıvel Superior) for financial

support; Parque Nacional do Itatiaia for logistical support and Dr.

Achim Braeuning for the revision of the paper and valuable sugges-

tions and comments.

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