Acta Botanica Brasilica 27(4): 730-736. 2013.

Ontogeny, allometry and architecture

of Psychotria tenuinervis (Rubiaceae)

Vanessa Rosseto1,2, Magda Silva Carneiro3, Flavio Nunes Ramos3,4 and Flavio Antonio Maës dos Santos1

Received: 10 May, 2013. Accepted: 19 July, 2013

ABSTRACT
We evaluated the ontogeny of the understory shrub Psychotria tenuinervis Müll.Arg., considering morphological and
morphometric characters. Four ontogenetic stages were identified: seedling, juvenile, immature and adult (vegetative
and reproductive phases). Size measurements and allometric relationships of the stem and crown were compared
between the immature and adult stages. Diameter and total height of the stem, as well as crown depth and width,
increased throughout the ontogenetic stages and differed among immature, vegetative adult and reproductive adult
individuals. The number of branches was lower in immature individuals than in vegetative and reproductive adult
individuals but did not differ between the last two. The bifurcation ratio did not vary during ontogenetic develo-
pment. In general, allometric relationships between the stem and the crown were similar among the ontogenetic
stages. Although there was a progressive increase in size during ontogenetic development, there was no change in
the allometric relationships between the size variables and architecture of P. tenuinervis, indicating that the form of
individuals does not change over the course of ontogeny.

Key words: allometry, architecture, branching pattern, ontogenetic stages, understory

Introduction 2007), which describes the inherited branching pattern of

species, such as their characteristics related to the direction
In population biology studies, age, developmental stage of growth, activity in time and destiny (Barthélémy & Ca-
and size can be used, either separately or in combination, to raglio 2007; León Enriquez et al. 2008).
categorize plants (Begon et al. 1996; Silvertown & Lovett- Morphometric characteristics, such as stem and crown
-Doust 1993). The sequence of developmental phases of size, and allometry have been used to facilitate the charac-
an individual is called ontogeny (Gatsuk et al. 1980). The terization and delineation of ontogenetic stages (Souza et
average duration of the ontogenetic stages of each species al. 2000; 2003). The allometric relationship between height
is genetically fixed. However, given that environmental and stem diameter indicates the amount of support that
conditions can vary greatly, different individuals can reach the plant requires within given environmental conditions
certain ontogenetic stages at different times (Gatsuk et al. (Claussen & Maycock 1995). Morphometric characteristics
1980). Therefore, the study of ontogenetic stages in plant include total height; stem diameter; number and size of the
populations supplies much more information with ecolo- leaves; rosette diameter; and number of branches (Souza et
gical meaning than does the study of age and the size of al. 2000, 2003; Lienert & Fischer 2003; Logofet et al. 2006;
structures (Silvertown & Lovett-Doust 1993). Miranda-Melo et al. 2007; Bernacci et al. 2008; Fidelis et
Structural differences during ontogenetic development al. 2008; Schmucki & de Blois 2009).
in different plant groups involve the presence/absence of Plant ontogeny studies have been carried out with
cotyledons, ramification patterns, stem type, stipe, repro- palms (Souza et al. 2000, 2003; Bernacci et al. 2008) and
ductive structures, and the root system (Souza et al. 2000, herbaceous species (Lienert & Fisher 2003; Logofet et al.
2003; Lienert & Fischer 2003; Logofet et al. 2006; Miranda- 2006; Fidelis et al. 2008, Schmucki & de Blois 2009). Howe-
-Melo et al. 2007; Bernacci et al. 2008; Fidelis et al. 2008; ver, there have been few studies on shrub and tree species
Schmucki & de Blois 2009). Morphological changes during (Gatsuk et al. 1980; Miranda-Melo et al. 2007). Due to its
ontogenetic development can be evaluated through the stu- dominance in the tropical and subtropical forest unders-
dy of plant architecture (Bell 1991; Barthélémy & Caraglio tory, the genus Psychotria has been used as a model to infer

1
Universidade Estadual de Campinas, Instituto de Biologia, Departamento de Biologia Vegetal, Campinas-SP, Brazil
2
Universidade Federal do Pampa, Bagé, RS, Brazil
3
Universidade Federal de Alfenas, Laboratório de Ecologia de Fragmentos Florestais Alfenas, MG, Brazil
4
Author for correspondence: [email protected]
 Ontogeny, allometry and architecture of Psychotria tenuinervis (Rubiaceae)

patterns of speciation (Hamilton 1989); the specialization we measured the fork height, crown diameter (east-west
of habitats (Kinupp & Magnusson 2005); the association and north-south cross sections), total number of branches,
between crown architecture and light capture efficiency crown depth, crown width, and bifurcation ratio. Individuals
(Pearcy et al. 2004); and the plastic phenotypic response to were monitored for a period of 18 months.
light (Valladares et al. 2000). Fork height was defined as the vertical distance between
The aim of this study was to identify and describe the the stem base and lowest major branch, which itself is defi-
ontogenetic stages of the shrub Psychotria tenuinervis Müll. ned as a branch that is at least half as thick as the main stem
Arg. and evaluate changes in individual size, allometry and at the same height (Osunkoya et al. 2007). Crown depth was
architecture during ontogenetic development. Because calculated as the difference between total height and fork
P. tenuinervis is a shade-tolerant shrub species, we expected height (Osunkoya et al. 2007). Crown width was determined
differences during ontogenetic development, mainly rela- as the average diameter of the east-west and north-south
ted to architecture, given that species adapted to low-light cross sections of the crown (Poorter et al. 2003).
conditions have a crown that is wide in order to intercept To evaluate the number of branches, the branches were
light over a large area and shallow in order to minimize ordered, with each terminal branch designated the first order
self-shading (Givnish 1988). (Strahler 1957, cited in Steingraeber et al. 1979, Sposito & San-
tos 2001a). Where two first-order branches met, the resulting
segment was designated the second order. For the meeting of
Materials and methods two branches of unequal order, the resulting branch retained
the name of the class of the next-highest order. Therefore, the
Study site and species stem would be the class of higher order for the plant. The
This study was carried out in the Serra de Palmital coas- bifurcation ratio was calculated with the Motomura formula
tal mountain range, near the municipality of Saquarema, in (Motomura 1947, cited in Steingraeber et al. 1979):
southeastern Brazil. The study site (22°50’S; 42°28’W) com- Br = (N − Nmax)/(N − N1)
prised 1200 ha of Atlantic Forest at an elevation of 30-400 m.
where Br is the bifurcation ratio; N is the total number of
According to the Köppen system of classification, the climate
branches; Nmax is the number of higher-order branches, and
is type Cwa (Veanello & Alvez 1991), defined as warm (up to
N1 is the number of first-order branches.
18°C) and semi-humid (with 4-6 dry months per year). In
2003, minimum and maximum monthly temperatures ran-
ged from 12.6°C to 19.0°C and 23.8°C to 34.2°C respectively Statistical analysis
(Ramos & Santos 2006). The vegetation in the study area is After testing for normality and homoscedasticity (Zar
evergreen forest, with 39 families and 132 morphospecies 1996), we used ANOVA to compare morphometric charac-
sampled in a 0.75 ha area (Ribeiro et al. 2009). ters among ontogenetic stages. Analyses were performed
Rubiaceae has a pantropical distribution, comprising
with the Systat program, version 10.2 (SPSS 2000).
approximately 550 genera and 9000 species (Souza & Lo-
For each ontogenetic stage, we compared the allometric
renzi 2005). Psychotria is the largest genus in Rubiaceae,
relationships between total height and diameter at ground
with approximately 2000 species (Davis et al. 2001), and
level using ANCOVA, in which the angular and linear co-
contains mainly shrubs and small trees, which are dominant
efficients of each regression analysis are compared. When
in the tropical and subtropical forest understory (Hamilton
the difference was significant, we used post hoc Scheffé tests
1990; Valladares et al. 2000). Psychotria tenuinervis is a
through the program Ancova33 (Santos 1997).
shrub that reaches 1-5 m height, endemic to fragments of
Atlantic Forest in the state of Rio de Janeiro, and common
in the understory (Gomes et al. 1995). Flowers are produced
within 1-3 months, whereas the fruiting lasts for 3-6 months
Results
per year (Ramos & Santos 2005). Vegetative growth has been Ontogenetic stages
observed for a few individuals of P. tenuinervis.
On the basis of the morphological and morphometric
characteristics observed over the 18-month study period, we
Data collection
defined the four ontogenetic stages for Psychotria tenuinervis:
In order to characterize the ontogenetic stages of Seedling (Fig. 1a)—In the seedling stage, the coty-
Psychotria tenuinervis individuals (Gatsuk et al. 1980), we ledons are green or dry and are darker than are the
registered the presence/absence of cotyledons, ramifications other leaves. Some individuals exhibit cotyledons
and reproductive structures, such as flowers and fruits. with a whitish color along the midrib. Some seedlings
We also registered the total height and diameter at ground present one or more pairs of opposing primary leaves,
level of immature and adult individuals. To evaluate the without stem ramification. Growth is monopodial,
architectural pattern of immature and adult individuals, and the stem can be lignified or not.

Acta bot. bras. 27(4): 730-736. 2013.

731
 Vanessa Rosseto, Magda Silva Carneiro, Flavio Nunes Ramos and Flavio Antonio Maës dos Santos

Juvenile (Fig.1b)—In the juvenile stage, there are no Stem and crown relationships
cotyledons, growth is monopodial, and the stem has
In general, the relationships between the stem and crown
no branches. Some individuals present flexible, green
remain constant during ontogenetic development in Psycho-
stems, whereas others have woody stems, especially
tria tenuinervis. Linear regression analyses revealed that
near the base.
nearly all of the associations between the crown and stem
Immature (Fig. 1c)—In the immature stage, growth is
parameters were significant (p<0.001), the exception being
sympodial and the stem is fully lignified, with orthotro-
the relationship between the number of branches and crown
pic and plagiotropic branches. The total height is < 1 m.
Adult (Fig. 1d and 1e)—In the adult stages, growth is depth in reproductive adults (ANOVA: F1,13=2.70, p=0.12).
sympodial and the stem has orthotropic and plagio- No significant differences were found among the imma-
tropic branches. The total height is ≥ 1 m. This stage ture and adult stages (vegetative and reproductive phases)
was divided into two phases: in terms of the relationship between stem diameter and
• Vegetative (Fig. 1d)—In the vegetative adult phase, total height, neither for the angular coefficient (ANCOVA:
individuals present no flowers or fruits. F2,72=0.15, p=0.86; Tab. 2) nor for the linear coefficient
• Reproductive (Fig. 1e and 1f)—In the vegetative adult (intercept; ANCOVA: F2,74=0.20, p=0.82; Tab. 2).
phase, individuals present flowers, fruits or both. The relationship between total height and crown depth
Leaf shape was similar among the ontogenetic stages did not differ among immature, vegetative and reproductive
(Fig. 1). Analyses of morphometric data showed that total adult individuals, for the angular coefficient (ANCOVA:
height, diameter at ground level, crown depth and crown wi- F2,74=3.69, p=0.03; Tab. 2), whereas the linear coefficient
dth increased during ontogenetic development and differed differed significantly between immature and reproductive
among immature, vegetative adult and reproductive adult adult individuals (ANCOVA: F1,53=5.79, p=0.02; Tab. 2), but
individuals (Tab. 1; Fig. 2). Individuals presented between 3 not between vegetative and reproductive adult individuals
and 2020 first- to seventh-order branches. Although imma- (ANCOVA: F1,46=0.51, p=0.49; Tab. 2). This suggests that
ture individuals showed fewer branches than did vegetative crown depth increases in parallel with the increase in total
and reproductive adult individuals, there was no difference height during the immature stage. The relationship betwe-
between vegetative and reproductive adults in terms of the en total height and crown width did not differ between
number of branches (Tab. 1; Fig. 2). The bifurcation ratio ontogenetic stages for the angular coefficient (ANCOVA:
did not vary during ontogenetic development (Tab. 1; Fig. 2). F2,74=0.004, p=0.99, b=0.76; Tab. 2) or the linear coefficient
(ANCOVA: F2,76=0.008, p=0.98; a=−0.23; Tab. 2).
The relationship between total height and the number
of branches did not differ during ontogenetic development,
for the angular coefficient (ANCOVA: F2,54=2.11, p=0.13,
common b=2.18; Tab. 2) or the linear coefficient (ANCOVA:
F2,56=0.39, p=0.68, common a=1.96; Tab. 2)
The angular coefficient for the relationship between
the number of branches and crown depth differed betwe-
en immature and vegetative adult individuals (ANCOVA:
F2,54=14.37, p<0.001; Tab. 2). The angular coefficient for the
relationship between the number of branches and crown
width differed only between immature and vegetative adult
individuals (ANCOVA: F2,54=3.68, p=0.03; Tab. 2). The li-
near coefficient for that same relationship differed between
immature and reproductive adult individuals (ANCOVA:
F1,42=0.66, p=0.43; Tab. 2) but not between vegetative and
reproductive adults (ANCOVA: F1,27=2.69, p=0.11; Tab. 2).

Discussion
Ontogenetic stages
The overlap of some measurements of size and allo-
metric relationships among immature, vegetative and
Figure 1. Schematic representation of the ontogenetic stages of Psychotria tenui- reproductive adult individuals indicates that size does not
nervis Müll.Arg.: (A) seedling; (B) juvenile; (C) immature; (D) adult (vegetative
phase); and (E) adult (reproductive phase). In F, detail of branch with fruit. always correspond to individual age. Hence, individuals of
a – cotyledon; b – primary leaves; c – unbranched stem. the same size may be at different ontogenetic stages and

Acta bot. bras. 27(4): 730-736. 2013.

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 Ontogeny, allometry and architecture of Psychotria tenuinervis (Rubiaceae)

Table 1. Morphometric characteristics of Psychotria tenuinervis Müll.Arg. (immature and adult individuals), in a fragment of Atlantic Forest in the Serra de Palmital
coastal mountain range of southeastern Brazil.*

Ontogenetic stage Height Diameter Crown depth Crown width Number of Bifurcation
(m) (cm) (m) (m) branches ratio
range 0.16-0.99 0.08-1.29 0.01-0.99 0.13-0.71 3-200 2.00-4.00
Immature mean 0.51a 0.53a 0.37a 0.35a 36.33a 3.05a
n 31 31 31 31 30 30
Adult
range 1.13-3.05 0.94-3.98 0.67-2.48 0.53-2.00 38-1962 2.63-3.45
Vegetative phase mean 1.75b 1.72b 1.23b 0.92b 481.93b 3.02a
n 24 24 24 24 15 15
range 1.05-4.40 0.85-4.46 0.69-4.22 0.58-2.15 126-2020 2.71-3.48
Reproductive phase mean 2.53c 2.43c 1.96c 1.22c 742.80b 3.01a
n 25 23 25 25 15 15
distribution F2,77=91.41 F2,75=49.92 F2,77=57.98 F2,77=64.35 F2,57=16.59 F2,57=0.07
ANOVA
p 0.000 0.000 0.000 0.000 0.000 0.932
*Means sharing the same letter within a column do not differ significantly (ANOVA and Tukey’s test).

may differ in terms of their use of environmental resources

at a given time and in a given space (Gatsuk, et al. 1980).
The identification and characterization of the ontogenetic
stages of Psychotria tenuinervis is partly consistent with the
classification system devised by Gatsuk et al. (1980): seed,
seedling, juvenile, immature, virginile, reproductive (young,
mature, old), subsenile and senile.
Seedlings have cotyledons, characteristically with par-
tial heterotrophic nutrition showing vestiges of embryonic
structures (Gatsuk et al. 1980). We found that, during the 18
months of our study period, Psychotria tenuinervis seedlings
showed low density in comparison with the subsequent
stages (Rosseto et al., unpublished data). In a study of eight
Psychotria species, Paz & Martínez-Ramos (2003) found
that, at two months after emergence, individuals no longer
presented cotyledons and developed a pair of true leaves,
indicating that the seedling stage is ephemeral in this genus.
Juveniles presented monopodial growth and stems
without embryonic structures, although the leaf shape
remained similar in the subsequent stages. In Psychotria
tenuinervis, the change from monopodial to sympodial
growth occurs at the immature stage and is likely associated
with greater lignification of the stem, resulting in improved
resistance. The immature stage can be characterized by
considerable growth, in terms of the total height and the
crown parameters, especially crown depth.
It was necessary to use a size descriptor in order to
differentiate between the pre-reproductive and reproduc-
tive stages in Psychotria tenuinervis, because of the lack of
visible macro-morphological markers. In addition, because
no permanent reproductive markers were found, it was
necessary to adapt the classification of Gatsuk et al. (1980)
Figure 2. Box-plot of morphometric characters for the ontogenetic stages of
Psychotria tenuinervis Müll.Arg. The length of each box encompasses the two
by creating an adult ontogenetic stage (vegetative and
central quartiles (50% of the central values), in which the narrowest part of the reproductive phases). The vegetative adult phase includes
box represents the median and the narrowing region is the confidence interval the pre-reproductive, reproductive and post-reproductive
(McGill et al. 1978). Asterisks and circles are outliers. Where confidence inter-
vals overlap, the median is equal between the stages.
periods because it includes individuals who did not repro-
A-vp – Adult-vegetative phase; A-rp – Adult-reproductive phase. duce, individuals who already have reproduced, and senile

Acta bot. bras. 27(4): 730-736. 2013.

733
 Vanessa Rosseto, Magda Silva Carneiro, Flavio Nunes Ramos and Flavio Antonio Maës dos Santos

Table 2. Linear regressions (log10) and statistical parameters for morphometric characteristics of Psychotria tenuinervis Müll.Arg. (immature and adult individuals),
in a fragment of Atlantic Forest in the Serra de Palmital coastal mountain range of southeastern Brazil.*

Comparison
b SE1 a SE2 r2 N
Ontogenetic stage
Height vs. Diameter
Immature 1.01a ±0.12 −0.01b ±0.05 0.71 31
Adult
Vegetative phase 1.03a ±0.19 −0.03b ±0.05 0.58 24
a b
Reproductive phase 1.14 ±0.17 −0.06 ±0.07 0.68 23
Height vs. Crown Depth
Immature 1.79a ±0.24 0.01a ±0.10 0.66 31
Adult
Vegetative phase 0.98a ±0.12 −0.16b ±0.03 0.74 24
a
Reproductive phase 1.14 ±0.15 −0.18b ±0.06 0.72 25
Height vs. Crown Width
Immature 0.77a ±0.08 −0.23b ±0.04 0.74 31
Adult
Vegetative phase 0.76a ±0.16 −0.23b ±0.04 0.51 24
a b
Reproductive phase 0.76 ±0.10 −0.22 ±0.04 0.70 25
Height vs. Number of Branches
Immature 2.01a ±0.20 1.96b ±0.08 0.77 30
Adult
Vegetative phase 3.10a ±0.58 1.71b ±0.14 0.69 15
a
Reproductive phase 2.13 ±0.56 1.93b ±0.23 0.53 15
Number of Branches vs. Crown Depth
Immature 0.86a ±0.10 −1.71 ±0.14 0.73 30
Adult
Vegetative phase 0.19b ±0.06 −0.39 ±0.15 0.44 15
Reproductive phase 0.21a ±0.13 −0.32 ±0.36 0.17 15
Number of Branches vs. Crown Width
Immature 0.36a ±0.03 −0.96a ±0.04 0.86 30
Adult
Vegetative phase 0.22b ±0.06 −0.60b ±0.13 0.54 15
ab ab
Reproductive phase 0.29 ±0.07 −0.73 ±0.20 0.56 15

*Means sharing the same letter within a column/comparison do not differ significantly (ANCOVA and Scheffé test, p=0.05).
b – angular coefficient; SE1 – standard error (angular coefficient); a – linear coefficient; SE2 – standard error (linear coefficient); r2 – coefficient of determination;
N – sample size.

individuals. The reproductive adult phase includes the re- that energy accumulation is necessary before reproducing,
productive and post-reproductive periods. In the adult stage, and that this accumulation could only be achieved by an
sexual maturation occurs and there is an increase in the size increase in size.
of the organs, although this does not change the growth
pattern in comparison with the pre-reproductive period.
Stem and crown relationships
Plant size is an important component of plant fitness,
having consequences for survival and fecundity (Harper Various studies have demonstrated significant differen-
& Bell 1979; Weiner & Thomas 1986). Size is related to fe- ces among ontogenetic stages in terms of stem diameter-
cundity because plants flower and fruit only after reaching -height relationships (Niklas 1993; Claussen & Maycock
a certain size (Harper & White 1974). A size difference 1995; O’Brien et al. 1995; Sterck & Bongers 1998; Sposito
between vegetative and reproductive adults would indicate & Santos 2001b; Alves & Santos 2002; Bohlman & O’Brien

Acta bot. bras. 27(4): 730-736. 2013.

734
 Ontogeny, allometry and architecture of Psychotria tenuinervis (Rubiaceae)

2006; Osunkoya et al. 2007). For small-sized understory might be associated with the minimal structural variations
species, the increase in stem diameter provides the improved during ontogenetic development, which could be an energy-
mechanical stability needed to survive in the lower strata -saving strategy.
(Kohyama et al. 2003). However, for Psychotria tenuinervis,
no change was observed between immature and adult indi-
viduals in terms of the stem diameter-height relationships. Acknowledgments
This indicates that there is an isometric relationship be-
The authors thank Maíra Taquiguthi Ribeiro, Carolina
tween those variables, meaning that structures of different
Virillo, Élcio and Antônio Rosa, for their help with the
sizes have the same shape (Rich et al. 1986). That might
fieldwork, as well as Jim Hesson, for correcting the English.
be associated with the fact that understory species are less
This work received financial support from the Fundação de
exposed to lateral wind, so that, with a minimal biomass
Amparo à Pesquisa do Estado de São Paulo (FAPESP, São
investment in branches, stem diameter is proportional to
Paulo Research Foundation; Grant no. 02/01803-5).
height (Norberg 1988; Osunkoya et al. 2007).
Some authors have shown that understory tree species
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