Seasonality and growth rings in lianas of Bignoniaceae



Seasonality and growth rings in lianas of Bignoniaceae
DOI 10.1007/s00468-010-0476-z
Seasonality and growth rings in lianas of Bignoniaceae
André C. Lima • Marcelo R. Pace
Veronica Angyalossy
Received: 20 February 2010 / Revised: 14 July 2010 / Accepted: 22 July 2010
Ó Springer-Verlag 2010
Abstract Lianas are one of the most important components of tropical forest, and yet one of the most poorly
known organisms. Therefore, our paper addresses questions on the environmental and developmental aspects that
influence the growth of lianas of Bignoniaceae, tribe
Bignonieae. In order to better understand their growth, we
studied the stem anatomy, seasonality of formation and
differentiation of secondary tissues, and the influence of the
cambial variant in xylem development on a selected species: Tynanthus cognatus. Afterwards, we compared the
results found in T. cognatus with 31 other species of
Bignonieae to identify general patterns of growth in lianas
of this tribe. We found that cambial activity starts toward
the end of the rainy season and onset of the dry season, in
contrast to what is known for tropical trees and shrubs.
Moreover, their pattern of xylem formation and differentiation is strongly influenced by the presence of massive
wedges of phloem produced by a variant cambium. Thus,
the variant cambium is the first to commence its activity
and only subsequently does cambial activity progress
towards the center of the regular region, leading to the
formation of confluent growth rings. In summary, we
conclude that: the cambium responds to environmental
Communicated by R. Aloni.
A. C. Lima (&) M. R. Pace V. Angyalossy
Departamento de Botânica, Instituto de Biociências,
Universidade de São Paulo, Cidade Universitária,
Rua do Matão 277, São Paulo, SP 05588-090, Brazil
e-mail: [email protected]
Present Address:
M. R. Pace
Department of Biological and Environmental Sciences,
Institute of Biotechnology, University of Helsinki,
P.O. Box 56, 00014 Helsinki, Finland
changes; the xylem growth rings are annual and produced
in a brief period of about 2 months, something that may
explain why lianas possess narrow stems; and furthermore,
phloem wedges greatly influence cambial activity.
Keywords Anatomy Bignoniaceae Cambial variants Cambium Growth rings Lianas
Although substantial work exists on the seasonal formation
of growth rings in tropical trees, little is known about this
phenomenon in lianas. In temperate forests, temperature is
mainly responsible for tree ring formation, whereas, in
tropical trees, ring formation is mainly caused by either
periodic flooding or dry seasons (Worbes 1989). While this
has been repeatedly seen in studies with tropical trees, very
little is known about how lianas respond to seasonal
changes in their environment. Nonetheless, lianas are one
of the most important structural components differentiating
tropical from temperate forests (Croat 1978). Many works
(summarized by Schnitzer and Bongers 2002) have demonstrated the importance of lianas as a food source for
fauna, as structural parasites, and, more importantly, how
their dominance is increasing possibly as result of augmenting concentrations of atmospheric CO2 (Phillips et al.
2002). For all these reasons, studies that investigate how
lianas grow in their natural environment are critical to the
understanding of tropical forest dynamics as a whole.
Lianas have stems which are different from selfsupporting plants. Their narrow stems are formed by a
much lesser amount of xylem than that of trees of similar
crown size (Ewers and Fisher 1991). This feature is made
possible by the fact that the lianas is sustained by other
plants, hence the term ‘‘structural parasites’’ (Ewers and
Fisher 1991), and by the presence of vessels that are longer
and wider than those of other habits (Ewers et al. 1990).
Those larger and wider vessels are, moreover, associated
with narrow vessels, ensuring safety and efficiency in the
conductivity (Carlquist 1985, 1991; Ewers 1985; Ewers
et al. 1990; Ewers and Fisher 1991). Another distinctive
character among lianas, which has attracted the attention of
researchers since the nineteenth century (Schenck 1893;
Pfeiffer 1926; Obaton 1960; Isnard and Silk 2009), is the
widespread presence of cambial variants. Cambial variants
(also known as anomalous secondary growth) are unusual
types of secondary growth characterized by the differential
production of secondary tissues (xylem and phloem) by one
or many vascular cambia (Carlquist 2001), resulting in
stems with astonishing anatomical architectures.
All lianas that are members of tribe Bignonieae,
Bignoniaceae, are recognized by the presence of a cambial
variant that produces phloem wedges that furrow the
Fig. 1 Tynanthus cognatus
stem cross section. a General
view of regular (r) and variant
(v) portions of xylem and
phloem. Arrows indicate growth
ring boundaries. b Limiting
rays. The black portion of the
bar indicates the phloematic
portion of the limiting ray,
which is produced centrifugally
by an inner portion of the
cambium (black arrow), while
the white portion of the bar
indicates the xylematic portion
of the same limiting ray, which
is produced centripetally by an
outer portion of the cambium
(white arrow). The same
situation can be seen in the
limiting ray of the next step of
the phloem wedge, on the left.
c Growth ring boundaries. Black
arrows show the growth ring
boundaries in a stairstep fashion
in the variant xylem.
Arrowheads indicate growth
ring boundaries in the regular
xylem. Scale bars (a) 1 mm,
(b) 200 lm, (c) 500 lm
xylem. Aside from being a synapomorphy of Bignonieae
(Lohmann 2006), this cambial variant is thought to have
generated diversity of stem anatomical forms inside this
tribe (Pace et al. 2009). It is characterized by modification
of activity in four or multiples of four equidistant regions
of the cambium that start to produce much more phloem
than xylem. This breaks the continuity of an initially circular and continuous cambium and eventually generates
deep wedges of phloem (Solereder 1908; Dobbins 1971;
Pace et al. 2009) (Fig. 1a). Moreover, the phloem wedges
possess large rays, which are termed as limiting rays
(Schenck 1893), and these rays delimit the cambial variant.
Interestingly, the regions located between the phloem
wedges maintain a regular secondary growth, presenting a
cambium which, similar to most woody plants, produces
more xylem than phloem. Since such regions maintain a
regular secondary growth, they are termed regular cambia,
regular xylem and regular phloem in contrast to the variant
portions. However, it is still unknown how both regular and
variant growing cambia influence each other and, more
specifically, how they might respond to any seasonal aspect
during their development.
Bignonieae is the largest group of lianas in the Neotropics (Gentry 1991), and distinct growth rings are commonly found in their xylem. At first, growth rings were
encountered in 9 of the 31 traditionally recognized genera
by Gasson and Dobbins (1991), but afterwards, in a study
that investigated and described the wood anatomy of 73
species belonging to all genera in Bignonieae, the growth
rings were shown to be ubiquitous in the tribe (Dos Santos
1995). However, these studies never mentioned the time of
growth ring formation or whether they were influenced by
the presence of a cambial variant. The two main studies that
examined the seasonal formation of secondary xylem in
tropical lianas were conducted by León-Gómez and
Monroy-Ata (2005) and Brandes (2007). León-Gómez and
Monroy-Ata (2005) have followed the cambial activity in
Mexican lianas throughout the year, albeit in a region with a
marked dry season, and they found seasonality of cambial
activity in three out of four of them. Brandes (2007) studied
four Brazilian Fabaceae lianas in a region with a marked dry
season using the method known as Mariaux’s window
(Mariaux 1967). He found that the growth rings in all species were annual and that they responded to the alternation
of wet and dry seasons. However, these works have not
studied the possible influence of the cambial variants in the
development of the xylem. Thus, there is a considerable
lack of information about the formation of xylem growth
rings and cambial seasonality in tropical lianas.
The goal of the present work is to investigate seasonality
in the formation of secondary tissues in the stems of Bignonieae and how such formation is, in turn, influenced by
the cambial variant present in their stems. For this purpose,
we first examined the seasonality of cambial activity and
the differentiation of its products in a selected species:
Tynanthus cognatus Miers. Afterwards, we compared the
results found in this species with 31 other species
belonging to 16 of the 21 presently recognized genera of
Bignonieae (Lohmann 2010) to identify general patterns of
growth in the lianas of this tribe.
Materials and methods
Plant material
The species T. cognatus Miers was chosen as a model by
the presence of well-marked growth rings in its xylem and
its abundance in the Biosciences Institute Forest Reserve of
the Universidade de São Paulo.
T. cognatus, study area
Stem growth periodicity of T. cognatus was studied in the
Biosciences Institute Forest Reserve of the Universidade de
São Paulo, Brazil. The area has a mean temperature of
21.2°C and an annual precipitation of 1,300 mm with a
well-marked seasonal dry period (sensu Worbes 1995) that
lasts from April to September (Fig. 2). The vegetation has
been related to both the Atlantic Rain Forest and inland
mesophytic semideciduous forests of São Paulo (Gomes
Comparison between T. cognatus regular
and variant tissues
We compared both the xylem and the phloem of the regular
and variant regions of T. cognatus in terms of general
anatomy and diameter of the conductive cells of xylem and
phloem. For the measurements, 100 vessel elements and
100 sieve tube elements of each of these two regions of
three specimens had their tangential diameter measured.
T. cognatus seasonality
Stem samples from ramets ascending to the forest canopy
at least 3 cm in diameter at breast height were collected in
the dry season months of April, May, June and July, and
the wet season months of October, November, December,
January and March, from 2006 to 2008 (Fig. 2). Since the
complete stem of this species has a diameter of about
3–4 cm, the entire stem was collected each month. The
samples presenting periderm, secondary phloem, cambium
Fig. 2 Climatic diagram of
forest reserve of Instituto de
Biociências of Universidade de
São Paulo, showing mean
temperature and precipitation
from 1998 to 2007. The dashed
line indicates 60 mm
precipitation. Arrowheads
indicate the months in which
samples were taken, i.e.,
collection months
and secondary xylem were then fixed in CRAF III (Berlyn
and Miksche 1976) under vacuum for 10 days, embedded
in PEG 1500 (Rupp 1964), cross-sectioned from 8 to
15 lm thick with a slide microtome and stained in 1%
Astra blue and 1% Safranin (Bukatsch 1972). In order to
avoid tearing apart phloem and xylem during the sectioning, expanded polystyrene dissolved in butyl acetate
(Barbosa et al. 2010) was brushed on the samples, and an
adhesive tape was attached before a section was cut. In
addition, small sub-samples containing just the cambium
and narrow portions of adjacent phloem and xylem were
prepared and fixed in Karnovsky (1965) for 10 days under
vacuum. These sub-samples represented three portions of
the cambium: the variant cambium, regular cambium next
to the wedge, and center of the regular region. Subsequently, these sub-samples were embedded in HistorresinÒ
(Leica Mycrosystem) after dehydration in ethanol and then
cross-sectioned 3 lm thick in their transverse, radial and
tangential faces in a rotary microtome. The sections were
then stained in 0.05% Toluidine blue in acetate buffer pH
4.7 (O’Brien et al. 1964).
The cambial activity was characterized by indirect
parameters, i.e., the presence of cambial initials with
slender tangential walls, greater number of radial cell
layers in the cambial zone, and the presence of differentiating cells next to the cambium.
The climatological data were obtained from the meteorology station of the Astronomy, Geophysical and Atmospheric Sciences Institute located inside the campus of the
Universidade de São Paulo.
Growth rings analysis
To analyze the presence and pattern of xylem growth rings
and their relationship with the phloem wedges in
Bignonieae stems, 32 species representing 16 genera and
having a wide geographic distributional range were studied
(‘‘Appendix’’). Stem samples of all species were collected
at breast height in their natural habitats, or living collections, and samples presenting periderm, secondary phloem,
cambium and secondary xylem were processed as described for T. cognatus.
vessels in the earlywood, while displaying a line of radially
flattened fibers and narrow vessels in the latewood. While
this is true for the xylem produced by the regular and
variant cambium, growth rings produced by the variant
cambium are usually less visible than those produced by
the regular cambium. The growth rings of variant xylem
are discontinuous with the growth rings of the regular
xylem (Fig. 1c) because the variant cambium that has
formed these growth rings is at different depths in comparison with the regular cambium, in a stairstep fashion.
Remarkable differences can be observed in the anatomy
of the xylem produced by the regular and variant cambium.
The most notable of these involves the diameter of the wide
vessels. Vessel diameters were divided into two categories:
narrow vessels of less than 120 lm and wide vessels
exceeding this value. While the narrow vessels possess
statistically the same mean width, both in the regular and
the variant xylem (49.1 and 51.1 lm, respectively, ranging
from 9 to 115 lm), the wide vessels are far wider in the
regular than in the variant xylem (Table 1). In fact, in the
regular xylem, the wide vessels range from 131 to 804 lm,
possessing an average of 429 lm, while in the variant
xylem, the wide vessels range from 126 to 440 lm, having
an average of 290 lm (Table 1).
T. cognatus phloem anatomy
Two distinct phloems are present in the stems of T. cognatus: variant and regular phloem. Unlike the xylem, growth
rings are not distinguishable in either secondary phloem.
However, similar to the xylem, the phloem anatomy of the
variant portion differs from that of the regular phloem. The
main difference involves the sieve tube diameters. Indeed,
the sieve tubes are much wider in the variant than in the
regular phloem, where they appear radially flattened in
Table 1 Tynathus cognatus regular and variant cellular dimensions
Vessels diameter (lm)
49.1 ± 16.3
51.1 ± 18.5
428.8 ± 175.3
229.1 ± 85.7
Diameter (lm)
17.2 ± 5.1
82.2 ± 25.4
Diameter range (lm)
Occupied area (%)
Frequency (/mm2)
65 ± 19
16 ± 2
Frequency (/mm2)
150 ± 23
67 ± 12
Occupied area (%)
T. cognatus xylem anatomy
The stem of T. cognatus is marked by the presence of four
phloem wedges that deeply furrow the secondary xylem, as
a result of cambial variant activity (Fig. 1a). Moreover, the
xylem in this species presents growth rings that can be
distinguished by a band of axial parenchyma and wide
Sieve tube
contrast to the round shape of the sieve tubes in the variant
phloem (Fig. 3b, c). More specifically, in the variant
phloem, the sieve tube diameters range from 11 to 146 lm,
with an average of 82 lm, while in the regular phloem,
they range from 7 to 33 lm, with an average of 17 lm
(Table 1). Furthermore, sieve tubes in the variant phloem
are arranged in multiples of 3–4 cells and display a
tangential arrangement. Each sieve tube element is normally accompanied by one to three companion cells lying
on the same corner (Fig. 3c).
The arrangement of sieve tubes in the regular phloem is
usually found in multiples of two or three cells, sometimes
solitary, and normally in radial disposition. The sieve tubes
are accompanied by one or two companion cells, always
one at each corner. The sieve tubes in the regular phloem
may also be arranged in assemblages, which comprise an
ensemble of sieve tubes and phloem parenchyma cells, all
derived from the same fusiform cambial initial. The entire
assemblage is as large as a neighboring phloem parenchyma cell (Fig. 3b).
While in the variant phloem, the parenchyma is
restricted to a sheath of cells around the sieve tubes
(Fig. 3c), the parenchyma is the most abundant cell type in
the regular phloem (Fig. 3b), constituting the ground tissue
and forming radially organized rows that depart from the
cambium. Nonetheless, the ground tissue of the variant
phloem is composed of fibers, while these cells in the
regular phloem are restricted to bands 1–3 cells in width,
alternating with the sieve tubes with their companion cells
and parenchyma.
The rays also differ between regular and variant
portions. The rays produced by the variant cambium are
uni- and biseriate (excluding the limiting rays), while the
regular cambium produces uni- and multiseriate rays 3–4
cells in width. It was also found that the limiting rays are
produced by two different portions of cambia: a phloematic
portion is produced centrifugally by a more internal fragment of the variant cambium, while a xylematic portion is
produced centripetally (Fig. 1b).
T. cognatus cambial seasonality
Cambial activity in T. cognatus was detected only at the
end of the rainy season, in mid-March and April (Fig. 2). In
other months, May to early March, corresponding to the
dry and rainy seasons (Fig. 2), the cambium was inactive.
During the period of cambial inactivity, fully differentiated
latewood of the xylem and phloem cells was encountered
next to the cambium (Fig. 4a–f), although undifferentiated
smaller sieve tube elements were seen next to the variant
cambium in all collections (Fig. 4d, f). The variant phloem
is formed by sieve tube elements plus parenchyma cells
Fig. 3 Stem transverse sections
of Tynanthus cognatus.
a General view of the regular
(rp) and variant phloem (vp).
Arrows point to steps of variant
phloem. b Regular phloem. The
pointer points to a companion
cell of a solitary sieve tube
element. Arrowheads point to
companion cells of two small,
radially flattened sieve tube
elements radially arranged. The
arrow points to an assemblage
formed by sieve tubes with their
companion cells and
parenchyma cells. Phloem
parenchyma cells (asterisks) are
predominant and radially
arranged. c Variant phloem.
Large sieve tubes tangentially
arranged; multiple sieve tubes
with two to three companion
cells in the same corner
(arrowhead) and surrounded by
a sheath of parenchyma cells
(asterisks). The pointer
indicates undifferentiated sieve
tube elements. Note also the
ground tissue formed by fibers.
Scale bars (a) 800 lm,
(b) 100 lm, (c) 200 lm
Fig. 4 Tynanthus cognatus inactive regular and variant cambial
zones in different collections. May: a regular cambial zone; b variant
cambial zone. November: c regular cambial zone; d variant cambial
zone. January: e regular cambial zone; f variant cambial zone.
c cambium, lw differentiated latewood, arrows differentiated sieve
tubes of regular phloem, arrowheads undifferentiated sieve tube
elements of variant phloem, asterisks differentiated fibers of variant
phloem. Scales bars (a, c–f) 50 lm, (b) 25 lm
embedded in a fiber matrix (Fig. 1b). Therefore, we believe
that these undifferentiated sieve tubes were probably
formed in the previous growth season and remained
undifferentiated during the cambial dormant season, particularly since no differentiating phloem fibers were seen,
except in those samples collected in March and April
(Fig. 6a).
In mid-March, the first cells of the parenchyma band
that bounds the earlywood could be detected next to the
variant cambium (Fig. 5a, b). The cambial zone, on the
other hand, still consisted of only two layers of cells
(Fig. 5a, b). Furthermore, the regular cambium was inactive, and differentiated cells of latewood and phloem were
present on its margins (Fig. 5c). In April, the variant
cambium was active, consisting of five to seven layers of
tangentially narrow walled cells (Fig. 6a, c, e). In addition,
the large vessels of the earlywood were differentiated, and
the parenchyma band was differentiating next to the cambium. Regarding the phloem, fibers and sieve tube elements were differentiating, as evidenced by the deposition
of fiber walls and enlarging sieve tubes (Fig. 6a). It was the
only collection in which differentiating phloem fibers could
be seen, reinforcing the finding that immature sieve tube
elements remained undifferentiated during the cambial
dormant season.
Meanwhile, in April, the regular cambium was also
found to be active, being composed of six to eight layers of
cells (Fig. 6c, e). In the regular cambial portions that lie
Fig. 5 Tynanthus cognatus
cambial zone in March. Variant
cambial zones: a transverse
section showing the first layers
of newly formed earlywood
parenchyma cells. b Radial
section showing the transverse
walls of the newly formed
parenchyma cells (arrows).
c Inactive regular cambium.
c cambium, ewp earlywood
parenchyma, lw latewood, ph
phloem. Scale bars 50 lm
Fig. 6 Cambial activity of Tynanthus cognatus in April. a Active
variant cambium composed of many cellular layers (c): below the
parenchyma band of the earlywood (ew) is differentiating next to the
latewood (lw) of the previous growth season; above in the differentiating phloem (dp) can be seen differentiating fibers (black arrows)
and differentiating sieve tube elements (white arrows). b, c Regular
cambium next to the phloem wedge: b general view of the cambial
zone (c), the newly formed growth ring, with the earlywood (ew)
totally differentiated and differentiating latewood (dlw); c detail of the
cambial zone (c), differentiating phloem (dp) and differentiating
latewood (dlw). d, e Central portion of the regular cambium between
two phloem wedges: d general view of the cambial zone (c),
earlywood parenchyma band (pb) and the latewood (lw) of the
previous growth season; e detail of the cambial zone (c), differentiating phloem (dp), and earlywood parenchyma band (pb) just
formed. Scale bars (a, c, e) 100 lm, (b, d) 250 lm
close to the phloem wedges, the earlywood was fully differentiated, being composed of large vessels and a parenchyma band, while the latewood was in the process of
differentiating, with narrow vessels and fibers (Fig. 6b, c).
These events occurred in the regions close to the phloem
wedges. However, in the regions that are central, i.e.,
between two phloem wedges, the process of differentiation
was delayed, with the earlywood just starting its differentiation and the xylem parenchyma band just being formed,
but with no sign of vessels being produced (Fig. 6d, e).
Finally, in May, the cambium was inactive again and
consisted of two or three layers of cells, as well as differentiated latewood and phloem fibers that could be seen on
its margins (Fig. 4a, b). Since we observed the formation of
a growth ring next to the phloem wedge at the same time
that we saw complete formed growth rings in the center of
the regular region in May, we concluded that the formation
of the growth rings occurs in the short period between
March and April of each year.
were present both in the regular and in the variant xylem,
but generally more visible in the regular xylem as a result
of the discontinuity of their growth markers. As the variant
xylem is produced by a frequently fragmented cambium,
the xylem produced at the same time may be at different
positional depths, causing the growth markers to also stay
at different positions in the stem radius (Fig. 1c).
More than 50% of analyzed species with growth rings,
representing 15 species in 9 genera (Table 2), presented
well-marked semi-porous growth rings (Fig. 7). Another
14 of the 32 analyzed species also presented growth rings,
although some were nearly indistinguishable (Fig. 8a). The
main initial markers were parenchyma bands (C3 cells
wide) or lines (1–2 cells wide) (Figs. 1c and 8c) present in
21 species (Table 2). The presence of wide vessels was
also found as an initial marker in semi-porous ring species
(Fig. 7a, b), although sometimes the large vessels could not
be considered initial markers as they tend to be mixed
throughout the growth ring (Fig. 7c). In the latewood, the
main terminal markers were lines of radially flattened
fibers (Fig. 8b–d), present in 24 species (Table 2), and
radially shorter ray cells (Fig. 8b, d), present in 18 species.
Other terminal markers were narrow vessels and dilated
rays (Fig. 8d).
Nonetheless, terminal, as opposed to initial, wood
markers proved to be a more reliable means of recognizing
Bignonieae growth rings analysis
Anatomical markers
Among the 32 analyzed species, 29 presented growth rings
(Table 2). As in T. cognatus (Fig. 1c), the growth rings
Growth rings
Amphilophium crucigerum
Amphilophium elongatum
Amphilophium magnoliifolium
Amphilophium paniculatum
Bignonia binata
Mansoa difficilis
Mansoa onohualcoides
Perianthomega vellozoi
Pleonotoma tetraquetra
Stizophyllum riparium
Tanaecium bilabiatum
Tanaecium pyramidatum
Tynanthus cognatus
Growth rings
Manaosella cordifolia
Pyrostegia venusta
Lundia damazioi
Radially flattened
fibers (cells)
Late wood markers
Early wood markers
Lundia virginalis
Lundia cordata
Growth rings
Fridericia platyphylla
Fridericia samydoides
Fridericia chica
Dolichandra unguis-cati
Callichlamys latifolia
Cuspidaria convoluta
Bignonia magnifica
Bignonia campanulata
Amphilophium crucigerum
Adenocalymma divaricatum
Adenocalymma comosum
Adenocalymma flaviflorum
Adenocalymma bracteatum
Adenocalymma nodosum
growth rings
Table 2 Analyzed species and wood characters
Radially shorter
ray cells
10; 10; 14; 14;
11; 11; 16
Number of
growth rings
13; 20; 25; 28;
19; 25; 50
Stem diameter
Fig. 7 Stem transverse sections
showing different degrees of
semi-ring porosity in
Bignonieae. a Tynanthus
cognatus, b Cuspidaria
convoluta, c Pyrostegia venusta.
Scale bar 250 lm
Fig. 8 Growth rings in the
regular xylem of Bignonieae.
Arrows point to the growth rings
boundary. Mansoa dificilis:
a barely distinct growth rings in
low magnification; b growth
markers detail: flattened fiber
line and radially short ray
cells in the latewood.
c Amphilophium elongatum.
Parenchyma line in the
earlywood and flattened fiber
line in the latewood.
d Perianthomega vellozoi. Wide
vessels in the earlywood and
flattened fiber line, narrow
vessels, dilated rays and radially
short ray cells in the latewood.
Scale bars (a) 1 mm, (b, c)
200 lm, (d) 250 lm
the growth increments in Bignonieae. In fact, five analyzed
species lack any initial markers, while all of these present
radially flattened fibers as terminal markers (Table 2): one
out of six Adenocalymma, A. nodosum; two out of three
Bignonia species, B. binata and B. campanulata; and the
two Mansoa species, M. difficilis (Fig. 8a, b) and M. onohualcoides, also presented narrow vessels as terminal
markers (Table 2). On the contrary, all 29 species that
presented growth rings showed terminal markers.
Confluent growth rings
Of the total number of species that presented growth rings,
23 of 29 presented confluent growth rings (Table 2). A
confluent ring disappears at a certain point when being
followed across its circumference. These growth rings have
the same boundary markers as the regular ones and were
always encountered departing from the phloem wedges,
getting narrower as they withdrew. The confluent growth
Fig. 9 Confluent growth rings
in the regular xylem of different
species of Bignonieae.
a A. flaviflorum, b Tynanthus
cognatus, c Lundia virginalis.
Scale bars (a) 250 lm,
(b) 1 mm, (c) 500 lm
rings end where their terminal markers join with the terminal markers of the previous growth ring (Fig. 9).
Owing to their relative position, some confluent growth
rings arising from different variant regions could be identified as being the same growth ring. In fact, many confluent growth rings were very regular, arising from both
sides of all variant regions of the specimen. Analyzing
Fig. 10a, b, we can see, for example, that the fifth growth
ring is similarly confluent in all of the regular regions,
which makes it to be easy recognizable as the same growth
ring among different regular regions. As another example,
growth rings 7 and 8 in the same figure are continuous in
the regular regions I and II, but confluent in regions III and
IV. Since we could easily recognize growth rings 6 and 9 in
all regular regions, we could recognize the identity of
growth rings 7 and 8.
Based on these findings, it is reasonable to conclude that
(1) the cambial activity starts near the phloem wedges and
then spreads from there to the center of the regular region
Fig. 10 Transsection diagram
showing the regular xylem
growth rings of an adult stem of
Tynanthus cognatus. Each of the
inter-wedge zones had its
growth rings numbered from the
oldest (in the center) to the
newest (in the periphery).
Continuous growth rings have
their number in the inter-wedge,
while the confluent ones have
their number located at the
region of the phloem wedge
zone, and (2) this pattern of cambial activity is ubiquitous
in the tribe.
In the stem of T. cognatus, we could find anatomical differences between the regular and variant regions of xylem
and phloem. It is common among lianas to find the presence of two distinct classes of vessel diameter: large and
narrow. This character is related to conduction, whereby
the narrow vessels associated with wide vessels act as an
alternative water pathway in case wide vessels suffer
embolism. Wide vessels, in turn, guarantee effective water
transport. The stem of lianas thus ensures both safety and
efficiency for the conduction of water to the crown (Carlquist 1985, 1991; Ewers 1985; Ewers et al. 1990; Ewers
and Fisher 1991), a feature critical for the long and narrow
stems of lianas.
This vessel dimorphism is present in both regular and
variant regions. Nevertheless, we found differences in the
wide vessel dimensions of these two xylems. Thus, two
hypotheses are suggested for the presence of narrower
dimensions of wide vessels in the variant xylem. First, a
developmental constraint, caused by the presence of fully
differentiated regular xylem bordering the differentiating
variant xylem, would inhibit the expansion of the variant
vessel elements. A second hypothesis states that slow
production of xylem is coupled with the differentiation of
narrower conducting elements in the same way that a
higher production of phloem is coupled with the differentiation of wider conducting elements.
Moreover, the differences between variant and regular
phloem are even greater. It was proposed that the formation
of variant sieve tube elements, which can be five-fold wider
than regular ones, involves fewer mitotic divisions in the
phloem derivatives of the variant phloem, resulting in wider
sieve elements (Dobbins 1971). Pace (2009) has, moreover,
found that, unlike the regular phloem, which tends to be
very similar across the Bignonieae, the variant phloem
displays greater phloem diversity, with features exclusive to
certain clades inside the tribe. It is interesting to remark that
the narrow and distinctly arranged sieve tubes in the regular
phloem of Bignonieae greatly resemble the terminal
markers of late phloem of many arboreal species (Schneider
1945; Derr and Evert 1967; Deshpande and Rajendrababu
1985; Rajput and Rao 1998; Angyalossy 2006).
The anatomy of the species raises yet another interesting
question. Since the limiting rays are formed by two different cambia, in opposite directions, how do the cells of
the phloematic portion of the ray slide by the stationary
cells of the xylematic portion of the ray? Schenck (1893)
hypothesized that some kind of mucilage or other secretion
would be released in the intercellular spaces between the
phloematic and xylematic portions of the limiting ray in
order to facilitate such sliding. However, another hypothesis proposes that these two portions of the limiting rays
stay together and that divisions, distension, and oblique
disposition of the axial elements maintain the continuity of
the tissues (Hovelaque 1887, according to Schenck 1893,
p. 221).
Indeed, similar to the variant xylem, the variant phloem
is distinct from the regular phloem. It remains to be seen
whether this is caused by a distinct genetic program of the
variant cambium, by a difference in hormonal transport
between the regular and variant cambium, or even by the
different availability of nutrients that should be transported
by the variant phloem.
The Biosciences Institute Forest Reserve of the
Universidade de São Paulo presents a well-marked dry
season (following the criteria of Worbes 1995), which is a
condition sufficient to promote seasonal growth ring formation in trees (Worbes 1995). Although seasonal cambial
activity and the formation of growth rings have been well
studied in trees, virtually nothing has so far been reported
about the effects of seasonal rainy periods on lianas.
The cambium of T. cognatus presents a long inactive
period, ranging from May to March in the Forest Reserve.
Sieve tube elements were found throughout the year
undifferentiated next to the variant cambium, but they
clearly represent sieve tubes formed by the end of the
previous growth season that remained undifferentiated,
since no phloem fibers, which alternate with the sieve tubes
and parenchyma cells forming the variant phloem, were
seen differentiating, except in April. The presence of sieve
tube elements that remain undifferentiated next to the
cambial zone for an entire season is a situation well known
both for trees and lianas (Esau 1948; Davis and Evert 1968,
The time span during which the cambium is active in
T. cognatus (1 month) is less than that reported in trees, or
even plants growing in temperate climates. In fact,
4 months of activity were reported for apples (Pyrus malus;
Evert 1963), 5 months for Robinia pseudoacacia and
3 months for three pine species (Pinus; Derr and Evert
1967; Alfieri and Evert 1968). Similarly, in tropical species, Paliwal and colleagues (1975) reported a 5-month
span of cambial activity for Polyalthia longifolia; Coradin
(2000) reported 4–5 months of cambial activity for deciduous species and up to 8 months of cambial activity for
evergreen species; Angyalossy (2006) and Amano and
Angyalossy (2005) reported about 5 months for Citharexylum myrianthum, Copaifera langsdorffii and Caesalpinia echinata; and Marcati et al. (2006) reported at
least 5 months for Cedrela fissilis.
Of the few works treating cambial activity in lianas of
temperate regions, Esau (1948) reported only 2 months of
cambial activity in Vitis vinifera, and Davis and Evert
(1970) reported 1.5–4 months in four liana species found in
the State of Wisconsin in the United States. These time
spans of cambial activity are much less than those reported
for temperate trees. As such, one might suppose that this
reported reduction in cambial activity could be directly
related to the acknowledged narrow stems of lianas (Ewers
and Fisher 1991), even though a broader sampling would
be desired to confirm this hypothesis.
Lianas were shown to produce 19 times less xylem than
shrubs and trees with similar crowns, but this has been
directly correlated to the liana growth habit, as lianas rely
on other plants to sustain themselves, reducing the need for
mechanical tissues (Ewers and Fisher 1991). We believe
that the reduced time span of cambial activity in the stems
of lianas may be one of the developmental causes that led
to narrower stems.
Moreover, unlike trees and shrubs that start their cambial activity at the beginning of the rainy season, the liana
T. cognatus initiated its cambial activity towards the end of
the rainy season and the onset of the dry season. Borchert
(1999) states that moisture availability is the main condition that controls cambial activity in tropical forests, and in
locations with seasonal droughts, the cambium restarts its
activity right after the first rainfalls. This statement was
confirmed in studies with P. longifolia (Paliwal et al.
1975), Tectona grandis (Tomazello and Cardoso 1999), 10
species growing in the Brazilian cerrado (Coradin 2000),
C. fissilis (Marcati et al. 2006), and Schizolobium parahyba
(Marcati et al. 2008).
Another remarkable characteristic of the species is the
influence of the phloem wedges in cambial activity, as
evidenced by the markers of the xylem growth rings.
Indeed, the variant phloem is probably the site of most
photosynthates conduction, mainly by its wide sieve tubes.
Very likely, this is the reason why cambial activity first
starts in these regions in early March.
In the April collections, we observe latewood and
phloem fibers differentiating in the variant region. Meanwhile, in the regular regions next to the phloem wedges,
latewood is also differentiating, while in the center of the
regular regions between two phloem wedges, it is the
earlywood that is being formed. This finding indicates that
the cambial activity in the regular region starts right beside
the phloem wedges and progresses towards the center of
the regular region. Such progress towards the center is,
moreover, thought to be slow, since a large amount of
differentiated cells is found in the xylem close to the
phloem wedges long before the first cells start to be formed
in the center of the regular region.
Such desynchronized cambium activity reveals the
magnitude to which the cambial variants influence wood
growth and regulation. Because of the uncommon
arrangement of the stem vascular tissues typical of
Bignonieae, with phloem wedges deeply immersed in the
xylem, it was possible to illustrate the importance of phloem
in cambial activity. For this reason, Bignonieae species may
be the proper subjects for future studies addressing questions involving the relationship between secondary phloem
and cambial activity.
Another work treating the different onsets of cambial
activity is that of Esau (1948) in grape (V. vinifera), but
across a longitudinal gradient. The author showed that the
cambial activity starts right below the sprout bud meristems and progresses basipetally, slowly becoming homogeneous across the entire stem. This progressive pattern of
cambial activity has been related to the descent of auxins
produced in the leaves in differentiation (Aloni et al. 2003).
Similarly, the auxins, together with the food supply, may
somehow be related to the diminished wood formation in
the center of the regular regions seen here, especially
considering that both food and auxins are known to descend by the phloem, the latter previously supposed to be
part of a coordinated system between source and sink tissues (Baker 2000).
As a result of the seasonal formation of xylem, growth
rings are formed. However, only a few studies have
reported the presence of distinct growth rings in lianas
(Schenck 1893; Baas and Schweingruber 1987; Gasson and
Dobbins 1991; Carlquist 1995; Dos Santos 1995; Brandes
2007). The first to note the presence of growth rings in the
stems of lianas in Bignoniaceae was Schenck (1893),
suggesting that, even though such growth rings should
reflect some seasonal aspect of these plants’ growth pathways, they would be too irregular to represent annual
growth markers. After that, Gasson and Dobbins (1991)
found growth rings in nine genera of Bignonieae
(Bignoniaceae), but Dos Santos (1995), studying 73 species
of Bignonieae, found growth rings in all genera analyzed,
but not reporting any information about their period of
formation. In the present paper, we also found that the
presence of growth rings is ubiquitous in the tribe, with just
three species, Amphilophium paniculatum, Fridericia
platyphylla and Manaosella cordifolia, lacking them. Furthermore, we found growth ring markers different from
those found by Dos Santos (1995), who only reported the
presence of thick-walled flattened fibers and parenchyma
band, as well as a few species presenting semi-ring
porosity. In the present paper, we show that the great
majority of Bignonieae species present semi-ring porosity
at different degrees of distinctiveness, shorter ray cells
marking the growth ring boundary, and dilated rays and
wide or narrow vessels. Moreover, we found that terminal
markers are more reliable as a means of recognizing
growth rings in the tribe than initial markers.
The growth rings were shown to be annual in T. cognatus. This result is in agreement with a number of works
that report the periodicity of growth ring formation in
arboreal species in the tropics, both in India (Paliwal and
Prasad 1970; Paliwal et al. 1975) and in Brazil (Luchi
1998; Tomazello and Cardoso 1999; Coradin 2000;
Marcati 2000; Marcati et al. 2006, 2008). Dendrochronological works also recount similar results (Worbes 1985,
2002; Jacoby 1989). To the best of our knowledge, only a
single study has analyzed the formation of growth rings in
lianas (Brandes 2007). This author studied the formation of
xylem in four lianas of Fabaceae by periodical cambium
wounds in order to analyze the time of formation of its
products throughout the year. The study found the formation of annual growth rings in all four species, and the
onset of formation at the beginning of the rainy season. In
contrast, we found the onset of cambial activity in
T. cognatus toward the end of rainy season and the
beginning of the dry season. However, compared to our site
of study having a dry season which ranges from April to
September, Brandes (2007) worked with species growing
from June to August in side hills located at an altitude
of 700 to 1,100 m and slightly different climatic conditions, with the lowest annual mean temperature equal to
18.2°C and a highest precipitation mean equal to
1,699 mm/year.
Nonetheless, the present study is the first to show the
presence of confluent growth rings in lianas. The confluent
rings differ from discontinuous growth rings generally
found in trees. In trees, the growth ring markers disappear
at some point of the stem circumference, while in the
pattern of confluent growth rings, the terminal boundary
marker joins the previous terminal boundary marker. Here,
we chose to term such growth rings as confluent rather than
wedging rings, as proposed by Worbes (2002) to describe
similar rings present in understorey trees, in order to avoid
confusing them with wedges of phloem produced by the
cambial variant, a phenomenon addressed at length above.
Worbes (2002) still states that such growth rings are more
frequently found in trees of the families Annonaceae,
Bignoniaceae and Tiliaceae. The confluent growth rings
found here possess a unique feature: all of them start their
production and differentiation beside the phloem wedges
and progress towards the center of the regular regions.
Discontinuous growth rings are commonly found in arboreal species. Hymenaea courbaril, a tropical species, for
example, possesses discontinuous growth rings, in which
the growth rings’ marker is not present across the entire
stem circumference (Luchi 1998). Discontinuous growth
rings may be annual (Lev-Yadun and Liphschitz 1986), and
they may be formed in temperate climates at the onset of
drought (Fritts 1976), by the loss of leaves (Krause and
Morin 1995) and shadowing (Bormann 1965; Roberts
1994), or, especially, during cold seasons at high altitudes
(Colenutt and Luckman 1991).
The growth of lianas is usually sustained by other plants,
but they may sustain themselves when crossing from one
tree to another. The excess of stems supported by one
another very often results in the collapse of entire individuals (A.C. Lima, personal observation). However, even
after suffering a period of damage by dropping, most lianas
recover from injuries (Fisher and Ewers 1991), resprout,
and once again take up their growth, a process which itself
could lead to the formation of confluent growth rings, much
like other stressful situations cited earlier. However, precisely what causes confluent growth rings in lianas remains
largely unknown at this time.
Our work illustrates that the secondary growth in lianas of
Bignoniaceae is seasonal. In T. cognatus, the initial cambial activity starts toward the end of the rainy season and
the onset of the dry season, the opposite of what is
known for tropical shrubs, trees, and for the only work that
studied the time of formation of growth rings in lianas.
Furthermore, the period of cambial activity lasts only
2 months. More importantly, the pattern of xylem formation and differentiation in Bignonieae is strongly influenced by the presence of phloem wedges, and because of
that, the variant cambium is the first to start its activity. The
regular cambium subsequently starts its activity, right
beside the variant regions and progresses towards the
center of the regular regions. This process may lead to the
formation of confluent growth rings, a pattern never
described before. Growth rings were shown to be annual.
Because confluent growth rings may not present initial
markers in some species, we also concluded that terminal
markers are more reliable as a means of recognizing
growth rings in the Bignonieae tribe.
Moreover, this work raises some new questions. (1) Is
the start of cambial activity toward the end of the rainy
season a feature common to most Bignonieae lianas or
particular to T. cognatus? (2) What is the exact role of the
secondary phloem such that it influences the cambium so
strongly, and is such role related to either food transport or
hormone translocation? (3) In the context of development,
does the short period of cambial activity explain why lianas
have such narrow stems? All these questions should be
addressed in future research.
Acknowledgments The authors thank ACF Barbosa for help with
anatomical procedures; M. Groppo, A. Zuntini, M. Souza-Baena,
M. Lopes, H. Lorenzi, D. Sampaio and D. Villaboel for collections in
Brazil and Bolivia; an anonymous reviewer for helpful suggestions;
the São Paulo Research Foundation (FAPESP, 07/51677-0), and the
National Counsel of Technological and Scientific Development
(CNPq, grant 481034/2007-2) for financial support.
Pace 39, Brazil, São Paulo. B. magnifica W. Bull, Pace 51,
Brazil, Plantarum’s living collection São Paulo. Callichlamys latifolia (Rich.) K. Schum, Zuntini 175, Brazil,
Espı́rito Santo; Pace 42, Plantarum’s living collection
Brazil, São Paulo. Cuspidaria convoluta (Vell.) A.H.
Gentry: Pace 48, Brazil, Plantarum’s living collection São
Paulo. Dolichandra unguis-cati (L.) L.G. Lohmann, Ceccantini 2687, Brazil, Minas Gerais; Groppo 322, Brazil,
São Paulo. Fridericia chica (Bonpl.) L.G. Lohmann, Pace
50, Brazil, São Paulo. F. platyphylla (Cham.) L.G.
Lohmann, Pace 22, Pace 23, Brazil, Minas Gerais.
F. samydoides (Cham.) L.G. Lohmann, Pace 49, Brazil,
São Paulo. Lundia cordata (Vell.) DC.: Zuntini 1, Brazil,
Espı́rito Santo. L. damazioi C. DC.: Pace 55, Pace 56,
Brazil, São Paulo. L. virginalis Kraenzl: Zuntini 126.
Manaosella cordifolia (DC.) A.H. Gentry, Pace 41, Brazil,
Plantarum’s living collection São Paulo. Mansoa difficilis
(Cham.) Bureau & K. Schum., Pace 35, Brazil, São Paulo;
Zuntini 4, ‘Brazil, Espı́rito Santo. M. onohualcoides A.H.
Gentry, Zuntini 276, Brazil, Espı́rito Santo. Perianthomega
vellozoi Bureau: Pace 10, Pace 15, Brazil, Minas Gerais;
Pace 28, Pace 29, Bolivia, Santa Cruz. Pleonotoma tetraquetra (Cham.) Bureau: Ozório-Filho 11, Brazil, São
Paulo. Pyrostegia venusta (Ker Gawl.) Miers, Pace 17,
Brazil, São Paulo; Pace 36, Brazil, São Paulo. Stizophyllum
riparium (Kunth) Sandwith: Pace 16, Pace 33, Brazil, São
Paulo; Zuntini 9, Brazil, Espı́rito Santo. Tanaecium bilabiatum (Sprague) L.G. Lohmann, Lohmann 850, Brazil,
Amazonas. T. pyramidatum (Rich.) L.G. Lohmann, Pace
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Pace 9a, Pace 9b, Lima 2 Lima 3, Lima4, Lima 5, Lima 6,
Lima 7, Brazil, São Paulo.
Appendix: analyzed species
Adenocalymma bracteatum (Cham.) DC., Castanho 153,
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Gerais. A. salmoneum J.C. Gomes, Lohmann 658, Brazil
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A. elongatum (Vahl) L.G. Lohmann, Pace 45, Brazil,
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