Gayana Bot. 61(1): 6-17, 2004
ISSN 0016-5301
COMPARATIVE MORPHOLOGY AND ANATOMY OF THE LEAF AND
STEM OF PEPEROMIA DAHLSTEDTII C.DC., OTTONIA MARTIANA MIQ.
AND PIPER DIOSPYRIFOLIUM KUNTH (PIPERACEAE)
MORFOLOGIA Y ANATOMIA COMPARATIVA DE LA HOJA Y TALLO DE
PEPEROMIA DAHLSTEDTII C.DC., OTTONIA MARTIANA MIQ. Y PIPER
DIOSPYRIFOLIUM KUNTH (PIPERACEAE)
L. A. Souza, I. S. Moscheta & J. H. G. Oliveira1
1
Departamento de Biologia, Centro de Ciências Biológicas, Universidade Estadual de Maringá, Avenida Colombo,
5790 (87020-900) Maringá, Paraná, Brazil. E-mail: lasouza@uem.br
ABSTRACT
The genera and species of Piperaceae show a considerable structural diversity of leaves and especially stems. This
paper presents a comparative morphological and anatomical study of the leaves and stems of three common Brazilian
species of this family (Peperomia dahlstedtii C.DC., Ottonia martiana Miq. and Piper diospyrifolium Kunth), the
vegetative organs of which have previously been little studied. The collected plant material was fixed in FAA, cut
freehand and stained in safranin and astra blue. P. dahlstedtii is an epiphyte and has a herbaceous stem with whorled
leaves phyllotaxis and a polystelic structure, a multiseriate adaxial leaf epidermis and calcium oxalate monocrystals in
parenchyma and collenchyma petiole cells. O. martiana and P. diospyrifolium showed strong similarities, both being
terrestrial plants, with alternate phyllotaxis, stele with medullary bundles and dorsiventral leaves with an epidermis
and subepidermic layer. In O. martiana the stomatal complex is staurocytic and presented silica crystal sand in parenchyma petiole and midrib cells. In P. diospyrifolium the stomatal complex is tetracytic and there are calcium oxalate
raphide crystals in the parenchyma of the petiole and midrib cells. On the other hand, the three species show some
structural likenesses in that all have hypostomatic and dorsiventral leaves, oily cells in petiole and mesophyll, secretory trichomes and an endodermis with Casparian strips.
KEYWORDS: Crystal cells, epidermis, stele, petiole.
RESUMEN
Los géneros y las especies de Piperaceae muestran una notoria diversidad estructural en sus hojas, y en particular en
tallos. Este trabajo presente presenta un estudio comparativo morfológico y anatómico del tallo y hoja de tres especies
de esta familia (Peperomia dahlstedtii C.DC., Ottonia martiana Miq. y Piper diospyrifolium Kunth) que son frecuentes en los bosques brasileños, sin que sus órganos vegetativos hubiesen sido previamente examinados anatómicamente.
El material fue fijado en FAA, cortado a mano y coloreado con safranina y azul de astra. P. dahlstedtii es un epífito que
posee un tallo herbáceo con filotaxia verticilada y estructura polistélica, hoja con epidermis adaxial multiseriada y
monocristal de oxalato de calcio en células parenquimáticas y colenquimáticas del pecíolo. O. martiana y P.
diospyrifolium presentan muchas semejanzas, siendo ambas plantas terrestres con filotaxia alterna, estela con haces
medulares y hoja dorsiventral con epidermis y subepidermis. En O. martiana el aparato estomático es estaurocítico y
presenta cristal de sílice en células parenquimáticas del pecíolo y vena media. En P. diospyrifolium el aparato estomático es tetracítico con presencia de rafidios en la parénquima del pecíolo y vena media. Por otro lado, las tres especies
muestran cierta semblanza estructural, como hojas hipostomáticas y dorsiventrales, células con aceite en el peciolo y
lámina, tricomas glandulares y endodermis provista de banda de Caspary.
PALABRAS
6
CLAVES:
Cristal, epidermis, estela, pecíolo.
Vegetative morphology and anatomy of Piperaceae: SOUZA, L. A.
INTRODUCTION
The family Piperaceae is of considerable economic
importance, as a large number of its members are
of medicinal or culinary interest. The Piperaceae
are represented in Brazil by five genera and approximately 460 species (Barroso et al. 1978). They are
erect or scandent shrubs, small trees, or succulent,
terrestrial or epiphytic herbs, with nodose stems.
Leaves are petiolate or infrequently subsessile, and
stipules adnate to the petiole or absent (Yuncker
1972).
The genus Peperomia Ruiz & Pav. includes
both epiphytic and terrestrial species. It consists of
herbs and accounts for about 63 species in Paraná
State, with almost half of them associated with dense
ombrophila forest (Yuncker 1974; Takemori 2002).
The genus Ottonia Spreng. possesses shrubs or subshrubs, with leaves narrowly lanceolate to broadly
ovate or elliptic (Yuncker 1973). The genus Piper
L. includes shrubs or small trees, occasionally scandent, but rarely subherbaceous, with a nodose stem,
and simple, entire and alternate leaves (Yuncker
1972).
Morphological and anatomical studies of vegetative organs of Piperaceae are relatively scarce.
Datta & Dasgupta (1977) carried out work of broad
scope on the leaf anatomy of Piper and Peperomia,
but most other studies have focused on specific aspects of anatomy or morphology (Bond 1931;
Langhammer 1970; Nascimento & VilhenaPotiguara 1999; Silva & Machado 1999), or on a
more limited range of taxa (Salatino & Silva 1975;
Gobbi 2003).
The most outstanding anatomical character
in the Piperaceae is the nature of the vascular
bundles in the axis. These are usually scattered like
those of the Monocotyledons, but several more or
less distinct arrangements occur in the different genera and species (Metcalfe & Chalk 1957). Judd et
al. (1999) regarded the Piperales as paleoherbs, displaying some traits typically associated with monocots. The leaves of Piperaceae species also show
structural diversity, especially between Peperomia
and the genera Piper and Ottonia.
This paper presents a comparative morphological and anatomical study of three common Brazilian species of Piperaceae: Peperomia dahlstedtii
C.DC., Ottonia martiana Miq. and Piper
diospyrifolium Kunth. Although all three of these
ET AL.
species are common in forest remnants in the northwest region of Paraná State, their leaves and stems
have previously been little studied. The epiphyte
Peperomia dahlstedtii occurs on the bark of several tree species, including Gallesia integrifolia
(Spreng.) Harms (“pau-d’alho”), [Phytolaccaceae],
Cedrela fissilis Vell. (“cedro”) [Meliaceae],
Nectandra megapotamica (Spreng.) Mez (“canelinha-amarela”) [Lauraceae] and Cabralea
canjerana (Vell.) Mart. (“canjerana”), Meliaceae.
Ottonia martiana and Piper diospyrifolium are
terrestrial species, often forming small thickets in
the forest understorey.
MATERIALS AND METHODS
The collection of the botanical material and the field
observations of P. dahlstedtii, O. martiana and P.
diospyrifolium were carried out in “Horto Florestal
de Maringá”, Paraná State (Brazil), a 37 ha forest
remnant.
The morphological description of the leaves
of the species was based on Rizzini (1977). The
analysis of the stem and leaf structure was done
using freshly-collected material or material fixed
in FAA 50 (Johansen 1940). This material was cut
freehand or in a rotative microtome to make semipermanent and permanent slides for the microscopic
studies, carried out according to the usual techniques. Sections were stained in astra blue, safranin and hematoxylin (Johansen 1940; Dnyansagar
1958).
Specific microchemical tests were done in
stems and leaves for calcium oxalate (10% hydrochloric acid) (Chamberlain 1932), silica (phenol)
(Johansen 1940) and lipid substances (sudam IV)
(Johansen 1940; Cutler 1978).
Stomatal, epidermical cell and trichome frequency (mm-2) were counted in quadrats of 0.04
mm2, using a reflex camera. In the middle region
of the blade, five fields of ten leaves were observed,
totalling 50 fields for each leaf face per species.
The Salisbury formula was used to calculate the
stomatal index (Wilkinson 1979).
Drawings were made using an optical microscope equipped with a reflex camera. They were
prepared on the same micrometric scale for all
samples.
Exsiccata of the studied species were depos-
7
Gayana Bot. 61(1), 2004
ited in the Herbarium of Universidade Estadual
de Maringá (Paraná State, Brazil) and registered
as follows:
Peperomia dahlstedtii C.DC. - BRAZIL.
Paraná. Maringá, Horto Florestal, A. L. M.
Albiero 9134 (HUM).
Ottonia martiana Miq. - BRAZIL. Paraná.
Maringá, Horto Florestal, A. L. M. Albiero 8974
(HUM).
Piper diospyrifolium Kunth - BRAZIL.
Paraná. Maringá, Horto Florestal, A. L. M.
Albiero 9392 (HUM).
RESULTS AND DISCUSSION
STEM
AND LEAF MORPHOLOGY
The stem of Peperomia dahlstedtii develops adventitious roots at the nodes, that penetrate the bark of the
host plant. The stem is green and is pentangular in
cross-section, and has a marked nodal structure. Each
node presents three leaves, characterizing the
phyllotaxis as whorled (Fig. 1). Racemose inflorescences are axillary with two or three small green
bracteoles in the axial base. The leave is broadly lanceolate, with an acute base and apex (Fig. 1).
FIGURES 1-3. Branches of (1) P. dahlstedtii; (2) O. martiana; (3) P. diospyrifolium. (IN = inflorescence).
8
Vegetative morphology and anatomy of Piperaceae: SOUZA, L.
The whorled phyllotaxis and leaf morphology of
P. dahlstedtii are similar to the Paraná species analyzed by Takemori (2002): P. catharinae Miq. and
P. quadrifolia (L.) Kunth. P. dahlstedtii differs,
however, from the other two species investigated
by this author (P. emarginella (SW.) C.DC. and P.
rotundifolia (L.) Kunth.), which possessed alternate phyllotaxis and rounded leaves, with a frequently emarginate apex.
Ottonia martiana is a subshrub, with a green
cylindrical nodose stem, helicoidal alternate
phyllotaxis and leaf-opposed racemose inflorescences (Fig. 3). Piper diospyrifolium also presents
alternate phyllotaxis (Fig. 2) and it differs from O.
martiana by presenting a shrub habit and a woody
stem with lenticels. The two species present a pla-
ET AL.
giotropic organ similar to a stolon. The stolon is,
according to Font-Quer (1985), a lateral and horizontal branch that sprouts from the stem base. It
develops at the soil surface, takes root, and eventually gives rise to new individuals through death of
its intermediate portion, thus spreading the plant
vegetatively. However, it is necessary to analyze
the structure of this plagiotropic organ. Preliminary
observations suggested that it is stem nature in O.
martiana and root in P. diospyrifolium.
O. martiana and P. diospyrifolium have petiolate leaves (Figs. 2, 3). The blade was ovate or
lanceolate-ovate, with a non-equilateral base and
an apex varying from acuminate to cuspidate (Figs.
2, 3). Lanceolate leaves can also occur in O.
martiana.
FIGURES 4-8. Stem structure in cross-section. Figs. 4, 6, 7 show overall diagram detail and vascular bundle of P. dahlstedtii,
respectively. Figs. 5, 8 show overall diagram and detail respectively of O. martiana (CL = collenchyma, EN = endodermis, EP = epidermis, FI = fibers; PA = parenchyma, VB = vascular bundle).
9
Gayana Bot. 61(1), 2004
STEM
ANATOMY
The stem of P. dahlstedtii has a polystelic structure
(Fig. 4). Each collateral vascular bundle and fascicular cambium is covered with a uniseriate parenchymatous pericycle and an endodermis with
Casparian strips (Fig. 7). On the other hand, O.
martiana and P. diospyrifolium stems have steles
with two concentric rings of collateral vascular
bundles; the outer vascular bundles are interconnected by sclerenchyma (Figs. 5, 8). In these species, an endodermis with Casparian strips and a parenchymatous pericycle covered the central cylinder
(Fig. 8). Starting from the second or third node in
O. martiniana and P. diospyrifolium, a fascicular
cambium and periclinal divisions of the interfascicular cells of the pericycle were common.
Piperaceae in general, which can be considered paleoherbs (Judd et al. 1999), have steles that
approximate those of monocots (Metcalfe & Chalk
1957). Polysteles, as found in P. dahlstedtii (Fig.
4) are common in Poaceae (Gramineae) species. In
O. martiana and P. diospyrifolium, with medullary
bundles arranged in a circle (Fig. 5), the stele is
similar to that of other monocots. Eames &
MacDaniels (1953) consider anomalous stem structure in the dicotyledons to be sometimes due to the
presence of medullary bundles, as they occur in
Piperaceae.
An endodermis in the stem has also been recorded for other species of Piper (Bond 1931) and
Peperomia (Takemori 2002). However, there is no
record of stem endodermis for Ottonia species. Bond
(1931) tentatively concluded that the endodermis is
a vestigial structure of no primary importance in
the internal economy of the stem. Similarly, Lersten
(1997) revised the occurrence of the endodermis
with a Casparian strip in the stem and leaf of vascular plants and considered that this strip in aerial organs has no known functional role.
FIGURES 9-13. Petiole structure diagrams in cross-section. Figs. 9, 10 show P. dahlstedtii petiole base and apex. Fig. 11
shows O. martiana petiole base. Figs. 12, 13 show P. diospyrifolium petiole base and middle region (CL = collenchyma, PA = parenchyma, SC = sclerenchyma, VB = vascular bundle).
10
Vegetative morphology and anatomy of Piperaceae: SOUZA, L.
The P. dahlstedtii epidermis is unilayered (Fig.
6), with a cuticle, secretory trichomes and periclinal
thick-walled cells. The cortex of this species possesses
parenchyma and subepidermic collenchyma arranged
in continuous strata (Figs. 4, 6). The epidermis (Figs.
5, 8) of the other two species is also uniseriate with
glandular trichomes, but has cells with thinner outer
periclinal walls than those of P. dahlstedtii. In the
cortex of O. martiana and P. diospyrifolium, there is
also parenchyma and the collenchyma occur in longitudinal strips (Fig. 8). The O. martiana cortical collenchyma is subepidermic (Fig. 5) and that of P.
diospyrifolium is separated from the epidermis. Some
inner collenchymatous cells of these two species are
differentiated in the fibers (Figs. 5, 8). The differentiation of collenchymatous cells in the fibers (in
the lower nodes) is cited for the caulinar cortex of
Piper by Metcalfe & Chalk (1957) and not for
Ottonia species. Nascimento & Vilhena-Potiguara
(1999) also describe the sclerification of the cortical collenchyma in Piper hispidinervium C.DC.
Fahn (1990) considers the sclerification of the collenchyma common in dicot stems and petioles, describing how this process occurs through centripetal and centrifugal lamellation of the cell wall.
LEAF
ANATOMY
The P. dahlstedtii petiole resembles the stem, ex-
ET AL.
cept for the number and arrangement of vascular
bundles. In the petiole, there are three bundles
in the base (Fig. 9) and middle regions, and five
different-dimensioned bundles in the apex (Fig.
10). The epidermis presents thick-walled tector
trichomes with pointed extremities (Fig. 28). The
cortical region of the petiole is collenchymatous
and parenchymatous (Figs. 9, 10). The petioles
of Peperomia hispidula A. Dietr., P. langsdorfii
Miq., P. emarginella, P. quadrifolia and P.
rotundifolia also showed three vascular bundles
(Metcalfe & Chalk 1957; Takemori 2002), although the authors did not indicated the petiole
section level. Takemori (2002) recorded a single
vascular bundle in the P. catharinae petiole.
With reference to the petiole of the other
two species, the structural differences of the stem
are more significant. Unlike the stem, there is no
sclerenchyma in the cortex or in the central cylinder of the petiole (Figs. 11, 13). However, O.
martiana can present isolated or grouped sclereids in the petiole (Fig. 11). The vascular bundles
of the petiole are distributed in a single ring (Figs.
11-13) and not in two concentric rings as in the
stem. An endodermis with Casparian strips is not
observed in the petiole either. The epidermis of
O. martiana and P. diospyrifolium presented
glandular and tector trichomes similar to those
found in the blade (Figs. 29-31, 33, 34).
FIGURES 14-17. Crystals in the petiole cells. Figs. 14, 15 show monocrystals in parenchymatous and collenchymatous
cells of P. dahlstedtii. Fig. 16 shows crystal sand in parenchymatous cell of O. martiana. Fig. 17 shows raphides in
parenchymatous cell of P. diospyrifolium.
11
Gayana Bot. 61(1), 2004
Elongated parenchymatous cells in the face
outside the phloem can occur in the petiole or blade
of many plants (Esau 1959). These cells form thick
walls after the obliteration of the sieved elements,
characterizing the differentiation of collenchymatous or sclerenchymatous tissue. The inner
peripherical parenchyma of the xylem can also be
differentiated in a similar way (Esau 1959), and this
parenchyma can cover the vascular bundle completely like a sheath. In the petiole of P.
diospyrifolium, parenchymatous cells were observed
in the phloem and xylem faces (Figs. 12, 13), whose
walls remained thin. On the other hand, in the O.
martiana petiole, collenchymatous cells were distributed in a similar way in the vascular bundle (Fig. 11).
Crystal and oil cells were found in the leaves
of all three species. The crystal cells differ in content and occurrence among the species. In P.
dahlstedtii, prismatic calcium oxalate monocrystals
with a pyramidal base occur in parenchymatous and
collenchymatous petiole cells (Figs. 14, 15). In O.
martiana, the crystal cells are observed in the parenchyma of the petiole and midrib, containing large
amounts of silica crystal sand (Fig. 16). In P.
diospyrifolium, there are cells with calcium oxalate
raphides (Fig. 17) in the parenchyma of the petiole
and midrib. Metcalfe & Chalk (1957) reported the
presence of the three crystal types in Piperaceae
leaves. Crystals resembling sand (as observed in O.
martiana) were recorded by Metcalfe & Chalk
(1957) in Piper betle L. Gobbi (2003), in turn, found
granulated silica crystals in Piper amalago (Jacq.)
Yunck. and calcium oxalate raphides in P. arboreum
Aubl. and P. crassinervium Kunth..
Oil cells occur in the parenchyma, collenchyma and vascular tissues of the petiole and midrib of all three species. In the blade, they can appear
in the mesophyll or subepidermis. Oil secretory cells
are common in Piperaceae (Metcalfe & Chalk 1957;
Barroso et al. 1978), i. e. species of Peperomia
(Murty 1960; Takemori 2002) and Piper
(Nascimento & Vilhena-Potiguara 1999).
FIGURES 18-25. Midrib structure in cross-section. Figs. 18, 19 show basal and apical regions of P. dahlstedtii midrib.
Figs. 20-22 show basal, middle and apical regions of O. martiana; midrib. Figs. 23-25 show basal, middle and apical
regions of P. diospyrifolium midrib (AB = abaxial face epidermis, AD = adaxial face epidermis, CL = collenchyma, ME
= mesophyll, MU = multiseriate epidermis, PA = parenchyma, PP = palisade parenchyma, SJ = spongy parenchyma,
SC = sclerenchyma, SU = subepidermis, VB = vascular bundle).
12
Vegetative morphology and anatomy of Piperaceae: SOUZA, L.
The midrib in the leaf base of P. dahlstedtii,
unlike the petiole, presents just one vascular bundle
(Fig. 18), with a parenchymatous sheath lacking
Casparian strips. On the adaxial face of the midrib,
a multiple epidermis, palisade parenchyma and a
little spongy parenchyma occur (Fig. 18). On the
abaxial face, a uniseriate epidermis, collenchyma
(with thinner cell walls those the petiole collenchyma) and parenchyma are observed (Fig. 18). In
the midrib apex (Fig. 19), there are few cells in the
vascular bundle, the adaxial epidermis presents
more cellular layers and there are no collenchyma
in the abaxial surface.
The midrib in the leaf base of O. martiana
has 10-11 different-dimensioned collateral vascular bundles, with sclerenchymatous cells in the phloem and xylem faces (Fig. 20). On the abaxial surface of the midrib, an epidermis with tector and
glandular trichomes, subepidermic collenchyma
strands and parenchyma occurred. On in the adaxial
suface, in addition to the epidermis and
subepidermis, a few collenchyma, chlorenchyma
ET AL.
and parenchyma were observed (Fig. 20). Sclereids occur within the parenchyma tissue of the vein
(Fig. 20). The O. martiana midrib undergo structural modifications along the blade: the number of
vascular bundles is reduced to three or four in the
intermediary region (Fig. 21); to one middle-sized
bundle and to two very small bundles in the apical
region (Fig. 22).
The P. diospyrifolium midrib structure is
similar to that of O. martiana. In the former, there
are also several vascular bundles in the base, reduced to three in the intermediary portion and to
one or two in the apical region (Figs. 23-25). Collenchyma and parenchyma distribution on the
abaxial face, and the occurrence of parenchymatous or collenchymatous cells in the vascular bundle
of the P. diospyrifolium midrib, are similar to those
of the petiole.
The petiole and blade of the studied species
do not present an endodermis with Casparian strips,
as shown for other Piperaceae (Bond 1931; Lersten
1997; Takemori 2002; Gobbi 2003).
FIGURES 26-34. Leaf epidermis in cross-section. Figs. 26-28. Young multiseriate epidermis and tector trichomes of P.
dahlstedtii, respectively. Figs. 29-30. Tector trichomes of O. martiana. Fig. 31. Tector trichome of P. diospyrifolium.
Figs. 32-34. Secretory trichomes of P. dahlstedtii, P. diospyrifolium and O. martiana, respectively.
13
Gayana Bot. 61(1), 2004
In all three species, the blade also has glandular trichomes with a unicellular apex and short
pedicel (Figs. 32-34). The O. martiana and P.
diospyrifolium the pedicel occupies the same level
of the other epidermic cells (Figs 33, 34), while
that of P. dahlstedtii occurs in a small depression
in the epidermis (Fig. 32). The O. martiana and P.
diospyrifolium the pedicel cell has a somewhat
thicker wall (Figs. 33, 34) than in P. dahlstedtii (Fig.
32). The apical cell trichome is spherical in P.
dahlstedtii (Fig. 32), slightly pointed in O. martiana
(Fig. 34) and clavate in P. diospyrifolium (Fig. 33).
Tector trichomes with a variable number of cells
were present in the blade of the three species (Figs.
27-31), although they are more restricted to the epidermis that covers the midrib in O. martiniana and
P. diospyrifolium. Glandular and tector trichomes
similar to those of the study species were also recorded in other Peperomia (Takemori, 2002) and
Piper (Nascimento & Vilhena-Potiguara 1999) species.
The blade epidermis of P. dahlstedtii and P.
diospyrifolium has straight or slightly curved anticlinal cell walls (Figs. 35, 36). The cell walls of
the O. martiana epidermis are sinuous in both the
adaxial and abaxial leaf surfaces (Figs. 37, 38).
FIGURES 35-38. Leaf epidermis in frontal view. Figs. 35-37. Abaxial face of P. dahlstedtii, P. diospyrifolium and O.
martiana, respectively. Fig. 38. Adaxial face of O. martiana. (SB = subsidiary cell).
Leaves of all three species are hypostomatic
(Figs. 35-38), which seems to be common in
Piperaceae. However, some species with
amphistomatic leaves have been recorded
(Metcalfe & Chalk 1957; Nascimento & VilhenaPotiguara 1999).
Judd et al. (1999) claimed that tetracytic
stomatal complexes are common in the leaf epidermis of Piperaceae species. We did find
tetracytic stomatal complexes in P.diospyrifolium
14
(Fig. 36), and occasionally P. dahlstedtii. However, a staurocytic stomatal complex was found
in O. martiana (Fig. 37), and often also in P.
dahlstedtii (Fig. 35). Takemori (2002) mentions
types of anisocytic and anomocytic stomatal complexes in other species of the family. Nascimento
& Vilhena-Potiguara (1999) recorded a cyclocytic
complex in the Piper hispidinervium leaf, which
suggests that this character cannot be applied reliably in Piperaceae taxonomy.
Vegetative morphology and anatomy of Piperaceae: SOUZA, L.
O. martiana leaves have lower stomatal,
epidermic cell and trichome frequency than the
other two species (Table I). However, the data
obtained on the leaf epidermis of these plants
do not take into consideration environmental
ET AL.
conditions such as light and humidity, and intraspecific diversity. Therefore, the data only
have value in the characterization of the species and have no taxonomical or ecological importance.
TABLE I. Mean values of stomata, epidermal cells and trichomes mm-2 and stomatal index of leaves of three Brazilian
Piperaceae species.
Species
Stomata mm-2
Abaxial face
Epidermic cells mm-2
Adaxial face
Stomatal index Trichomes mm -2 Epidermic cells mm-2
Peperomia dahlstedtii
60.0
153
5.4
11.0
832.0
Piper diospyrifolium
142.5
1378
9.4
10.5
940.0
Ottonia martiana
35.5
581
5.8
2.0
642.5
The P. dahlstedtii blade shows a multiple
epidermis in the adaxial face (Fig. 39), also verif i e d i n o t h e r Peperomia species (e.g. P.
catharinae, P. emarginella, P. quadrifolia and P.
r o t u n d i f o l i a ) (Takemori 2002). The leaf
protodermis of these species undergo repeated
periclinal divisions (Fig. 26), forming a
multiseriate epidermis that functions as a water
reserve. Metcalfe & Chalk (1957) incorrectely
referred to this epidermis as hypoderm. The
abaxial surface, on the other hand, possess a
uniseriate epidermis (Fig. 39).
FIGURES 39-41. Details of leaf blade in cross-section of P. dahlstedtii, O. martiana and P. diospyrifolium, respectively.
(AB = abaxial face epidermis, AD = adaxial face epidermis, BS = bundle sheath, MU = multiseriate epidermis, PP =
palisade parenchyma, SJ = spongy parenchyma, SU = subepidermis).
15
Gayana Bot. 61(1), 2004
FIGURES 42-43. Details of blade margin in cross-section of Peperomia dahlstedtii and Piper diospyrifolium. (AB =
abaxial face epidermis, AD = adaxial face epidermis, CL = collenchyma, ME = mesophyll).
The O. martiana blade (Fig. 40) presents
a uniseriate epidermis and one or two
subepidermic layers with enlarged cells in the
abaxial face. However, this subepidermis can
occur in both faces in the leaf base and in the
midrib vicinity (Figs. 20-22). The P.
diospyrifolium blade has an epidermis and
subepidermic layer in both leaf surfaces (Fig. 41).
The subepidermic layer of Piper hispidinervium
C.DC. was interpreted by Nascimento & VilhenaPotiguara (1999) as hypoderm, although the authors did not study the origin of this leaf tissue.
Metcalfe & Chalk (1957) also considered the one
to numerous layers in Peperomia and Piper leaves
as hypoderm. Only leaf development analysis can
reveal the nature of this tissue in O. martiana
and P. diospyrifolium, i.e. having a hypoderm or
biseriate epidermis.
The studied plant leaves are dorsiventral (Figs.
39-41), a previously recorded Piperaceae character
(Metcalfe & Chalk 1957). The species have a heterogeneous mesophyll with a single palisade parenchyma layer (Figs. 39-41). P. dahlstedtii shows several spongy parenchyma strata (Fig. 39) and O.
martiana and P. diospyrifolium present three to four
layers (Figs. 40, 41). Funnel-shaped palisade cells,
observed in Peperomia spp. (Metcalfe & Chalk
1957; Takemori 2002) and Piper arboreum (Gobbi
2003), were recorded in the mesophyll of the leaf
16
base of P. dahlstedtii. In the other leaf regions of
this species, the palisade parenchyma cell patterns
were closer than in the other two species analyzed.
The blade margin is similar in the three study species. It consists of subepidermic cells that contain
no chloroplasts and acquire collenchymatous cell
walls (Figs. 42, 43).
ACKNOWLEDGMENTS
We thank UEM (Universidade Estadual de Maringá,
Brazil) for funding this research.
BIBLIOGRAFIA
BARROSO, G.M., E.F. G UIMARÃES, C.L.F. ICHASO, C.G.
COSTA & A.L. P EIXOTO . 1978. Sistemática de
Angiospermas do Brasil. Volume 1. Livros Técnicos e Científicos Editora e Editora da
Universidade de São Paulo. São Paulo. 443 pp.
BOND, G. 1931. The stem endodermis in the genus Piper.
Transactions of the Royal Society of Edinburgh
56: 695-724.
CHAMBERLAIN, C.J. 1932. Methods in Plant Histology. The
University of Chicago Press, Chicago. 416 pp.
CUTLER, D. F. 1978. Applied Plant Anatomy. Longman,
London. 103 pp.
DATTA, P.C. & A. DASGUPTA. 1977. Comparison of vegetative anatomy of Piperales. II. Leaves. Acta
Vegetative morphology and anatomy of Piperaceae: SOUZA, L.
Biologica Academiae Scientiarum Hungaricae
28: 97-110.
DNYANSAGAR, V.R. 1958. Embryological studies in the
Leguminosae VIII. Acacia auriculaeformis A.
Cunn., Adenanthera pavonina Linn., Calliandra
grandiflora Benth. Lloydia 21:1-25.
EAMES, A.J. & L.H. MACDANIELS. 1953. An Introduction
to Plant Anatomy. McGraw-Hill Book Company,
New York. 427 pp.
ESAU, K. 1959. Anatomía Vegetal. Ediciones Omega,
Barcelona. 729 pp.
FAHN, A. 1990. Plant Anatomy. Pergamon Press, Oxford.
588 pp.
FONT-QUER, P. 1985. Diccionario de Botánica. Editorial
Labor, Barcelona. 1244 pp.
GOBBI, A.P. 2003. Morfo-anatomia comparativa da folha de três espécies da família Piperaceae.
Monografia. Universidade Estadual de Maringá,
Maringá.
J OHANSEN , D .A. 1940. Plant Microtechnique. Tata
McGraw-Hill Book Company. Bombay. 523 pp.
J UDD , W.S., C.S. CAMPBELL , E.A. K E L L O G G & P.F.
STEVENS . 1999. Plant Systematics: a Phylogenetic Approach. Sinauer Associates, Sunderland.
465 pp.
LANGHAMMER, V.L. 1970. Piper auritum H.B.K.-an anatomical-histochemical study. Piperaceae used in
folk medicine-comparative anatomical-histochemical study I. Planta Medica 19: 63-70.
LERSTEN, N.R. 1997. Occurrence of endodermis with a
Casparian strip en stem and leaf. The Botanical
Review 63: 265-272.
METCALFE, C.R. & L. CHALK. 1957. Anatomy of the Dicotyledons – leaves, stem and wood in relation
to taxonomy with notes on economic uses.
Clarendon Press, Oxford. 1500 pp.
ET AL.
MURTY, Y.S. 1960. Studies in the order Piperales – I. A
contribution to the study of vegetative anatomy
of some species of Peperomia. Phytomorphology
10: 50-59.
NASCIMENTO, M.E. & R.C. VILHENA-POTIGUARA. 1999. Aspectos anatômicos dos órgãos vegetativos de
Piper hispidinervium C.DC. (Piperaceae) e suas
estruturas secretoras. Boletim do Museu Paraense
Emílio Goeldi, série Botânica 15: 39-104.
RIZZINI, C.T. 1977. Sistematização terminológica da folha. Rodriguésia 29: 103-125.
SALATINO, A. & J.B. SILVA. 1975. Anatomia e óleo essencial das folhas de Piper regnellii (Miq.) C.DC.
var. regnellii. Boletim de Botânica da Universidade de São Paulo 3: 95-106.
SILVA, E.M. J. & S.R. MACHADO. 1999. Estrutura e desenvolvimento dos tricomas secretores em folhas de
Piper regnellii (Miq.) C. DC. var. regnellii
(Piperaceae). Revista Brasileira de Botânica 22:
117-124.
TAKEMORI, N.K. 2002. Anatomia comparada de Peperomia
catharinae Miquel, P. emarginella (Sw.) C.DC.,
P. quadrifolia (L.) Kunth e P. rotundifolia (L.)
Kunth (Piperaceae). Dissertação (Mestrado). Universidade Federal do Paraná, Curitiba.
WILKINSON, H.P. 1979. The plant surface (mainly leaf). In:
Anatomy of the dicotyledons (eds. Metcalfe, C. R.
& L. Chalk). pp. 97-165. Clarendon Press, Oxford.
YUNCKER, T.G. 1972. The Piperaceae of Brazil – I. Piper
– group I, II, III, IV. Hoehnea 2: 19-366.
YUNCKER, T. G. 1973. The Piperaceae of Brazil – II. Piper
– group V; Ottonia; Pothomorphe; Sarcorhachis.
Hoehnea 3: 29-284.
YUNCKER, T. G. 1974. The Piperaceae of Brazil III:
Peperomia – taxa of uncertain status. Hoehnea 4:
71-413.
Fecha de recepción: 09.12.03
Fecha de aceptación: 16.03.04
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