Acta Botanica Brasilica 32(4): 642-655. Oct-Dec 2018.
doi: 10.1590/0102-33062018abb0174
Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): anatomy
and taxonomic implications
Danilo Marques1* , Rafael de Oliveira Franca2 , Massimiliano Dematteis1
and Juliana Marzinek3
Received: May 8, 2018
Accepted: June 5, 2018
.
ABSTRACT
Lepidaploa is a taxonomically complex genus of Vernonieae, which is difficult to delimit morphologically due to
vegetative and reproductive characters that overlap with Chrysolaena and Lessingianthus. Anatomical studies of
cypselae are taxonomically useful for delimiting subtribes, genera and species of Asteraceae, and especially within
Astereae and Eupatorieae. Given the importance of cypselae to the taxonomy of tribes of Asteraceae, we searched
for morphological patterns among the species of Lepidaploa. Using light microscopy, we analyzed fruits of 21 species
of Lepidaploa to evaluate the taxonomic position of the genus and species of questionable placement in the group.
Our results showed that the morphologies of the cypselae of species of Lepidaploa are homogeneous and similar to
other species of Vernonieae. However, pappus vascularization and the number of mesocarp layers could be useful
for differentiating the sister groups Chrysolaena, Lepidaploa and Lessingianthus, which present similar macro- and
micro-morphological, palynological and chromosomal characters. Also, the presence of glandular trichomes and
idioblasts in the cypsela, and lignified cells in the carpopodium exocarp, can be used to separate closely related species.
Keywords: carpopodium, Compositae, cypsela, floral disk, pappus, Vernonia
Introduction
Vernonieae is one of the most species-rich tribes of the
Compositae, comprising about 1500 species distributed
in Africa, Asia and the Americas (Keeley & Robinson
2009). Although Vernonieae exhibits a high degree of
morphological variability, the tribe is generally known for
its alternate leaves, discoid heads with violet flowers, acute
style branches and biseriate pappus (Keeley & Robinson
2009). The cypselae of Vernonieae are generally cylindrical
or turbinate, sometimes prismatic, and brown (Semir et
al. 2011; Marques & Dematteis 2014; Angulo et al. 2015;
Talukdar 2015; Redonda-Martínez et al. 2017; Pico et al.
2016). The pappus can be biseriate with an outer short
paleaceous series and an inner long bristle series (Marques
& Dematteis 2014; Angulo et al. 2015; Redonda-Martínez
et al. 2017; Pico et al. 2016), biseriate with two paleaceous
series (one short and one long) (Semir et al. 2011), or it can
be absent (Redonda-Martínez et al. 2017).
Due to the taxonomic importance of cypselae for the
delimitation of subtribes, genera and species of Vernonieae,
numerous anatomical studies have been performed with
taxa of this tribe (Misra 1972; Pandey & Singh 1980;
Mukherjee & Sarkar 2001; Martins & Oliveira 2007; Galastri
& Oliveira 2010; Jana & Mukherjee 2013; Freitas et al.
2015; Talukdar 2015; Redonda-Martínez et al. 2017). Most
of the African and Asian species of Vernonieae that have
been studied anatomically have revealed that the anatomy
of the cypselae is very important to the taxonomy valuable
1 Instituto de Botánica del Nordeste, Universidad Nacional del Nordeste-Consejo Nacional de Investigaciones Científicas y Técnicas,
W3400BCH, Corrientes, Argentina
2 Programa de Pós-graduação em Biologia Comparada, Universidade Estadual de Maringá, 87020-900, Maringá, PR, Brazil
3 Programa de Pós-graduação em Biologia Vegetal, Instituto de Biologia, Universidade Federal de Uberlândia, 38400-902,
Uberlândia, MG, Brazil
* Corresponding author: danilobioufu@gmail.com
Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): anatomy and taxonomic implications
of the tribe (Mukherjee & Sarkar 2001; Jana & Mukherjee
2013; Talukdar 2015). Some American species have also been
studied, and their anatomical characters have also proven
to be important to the taxonomy of the group (Martins &
Oliveira 2007; Galastri & Oliveira 2010; Freitas et al. 2015;
Redonda-Martínez et al. 2017).
Vernonieae is also known for the uncertain taxonomic
delimitations of its contained taxa (Funk et al. 2005; Keeley
et al. 2007). Part of the difficulty in defining generic limits
for this tribe has been due to the fact that Vernonia s.l. (ca.
1000 spp.) encompasses a large number of species with many
different vegetative and reproductive features (Keeley &
Jansen 1994; Keeley et al. 2007). Robinson (1999) compiled
previous studies on the genus and delimited several other
genera from Vernonia s.l. based on palynological, macro- and
micromorphological, and cytological data.
Chrysolaena, Lepidaploa and Lessingianthus are three
closely related genera that were thus segregated from
Vernonia s. l. (Robinson 1999; Keeley & Robinson 2009).
However, the delimitation of these three genera from
one another is still complex due to the superposition of
macro- and micromorphological characters, such as the
type of inflorescence, shape of the heads, number of florets,
absence or presence of a basal node, and indument of florets
and cypselae, for example. Martins & Oliveira (2007) and
Galastri & Oliveira (2010) have been the only studies to
provide anatomical data on Chrysolaena and Lessingianthus,
while such studies with Lepidaploa are practically nonexistent, except for anatomical studies o the cypsela of
Lepidaploa tortuosa (Redonda-Martínez et al. 2017).
The genus Lepidaploa contains about 150 species that
occur in the Neotropics (Pruski 2017), with Brazil and
Bolivia being the countries with the highest species richness
(Redonda-Martínez & Villaseñor 2011). Some species of
Lepidaploa that inhabit southern South America (Argentina,
Bolivia, Paraguay and southern Brazil) are of uncertain
taxonomic position due to the overlap of vegetative and
reproductive characters among species.
Given the limited anatomical knowledge about American
Vernonieae, we studied the anatomy of the cypselae of
some species of Lepidaploa that inhabit southern South
America. Therefore, this study describes and compares the
anatomy of the cypselae of species of Lepidaploa with the
aim of identifying morphological patterns for the genus
and its included species.
Materials and methods
A total of 21 species of Lepidaploa (Cass.) Cass. from
southern South America were sampled. Details, including
voucher information, are provided in Table 1.
For anatomical analysis, dried mature and immature
cypselae were rehydrated with 5 N NaOH solution (Anderson
1963, modified from 36 to 4 hours), dehydrated in an ethanol
series and embedded in historesin (Leica Microsystems,
Heidelberg, Germany). The samples were sectioned using a
rotary microtome at 10 μm thickness. The material was then
stained with 0.05 % toluidine blue in acetate buffer, pH 4.7
(O’Brien et al. 1964 modified) and mounted with synthetic
resin. The slides were analyzed under a light microscope
(Olympus BX41) and digital images acquired. For images
of the pericarp, we used sections of the median region of
the cypselae.
Results
All of the species analyzed had a prismatic cypsela in
cross section (Figs. 1-6). The ribs along the fruit can be
distinct (Figs. 1A, C, E, G; 2A, C, E, G; 3A, C, E, G; 4A, C, E,
G; 5A, C, E; 6A, D, F) or indistinct, as in some regions of the
cypsela of L. amambaia (Fig. 1A), L. psilostachya (Fig. 5A),
and L. sordidopapposa (Fig. 6D) (Tab. 2). The fruit comprises
exocarp and mesocarp; the endocarp is only intact in L.
balansae (Fig. 1H) and L. setososquamosa (Tab. 2).
Exocarp: All species possess a uniseriate exocarp with
periclinally elongated cells (Figs. 1B, D, F, H; 2B, D, F, H; 3B,
D, F, H; 4B, D, F, H; 5B, D, F; 6B, E, G). Generally, the cells of
the exocarp are smaller in the ribs of L. amambaia (Fig. 1B),
L. argyrotricha (Fig. 1D), L. balansae (Fig. 1H), L. buchtienii
(Fig. 2D), L. canescens (Fig. 2F), L. chamissonis (Fig. 2H),
L. costata (Fig. 3B), L. eriolepis (Fig. 3F), L. mapirensis,
L. myriocephala (Fig. 4B), L. psilostachya, L. remotiflora
(Fig. 5D), L. salzmannii (Fig. 5F), L. setososquamosa, and
L. tarijensis (see Tab. 2). All species have biseriate nonglandular trichomes (Figs. 1C, F; 2B, D, F; 3B, D, F; 4F; 5F;
6B, E) while only L. chamissonis, L. pseudomuricata, L.
salzmannii, and L. setososquamosa (Fig. 6C) possess glandular
trichomes. Stomata were observed among the cells of the
exocarp only in L. setososquamosa (Fig. 7A). Cells with
secretory appearance (idioblasts) are found in the exocarp
of most species. Compared with adjacent cells, idioblasts are
larger, spherical or, in a few cases, ovate-spherical, and have
dense content (Figs. 1D, F, H; 2B, D, H; 3B, D; 4D, F, H; 5F;
6E, G; 7 I). These cells are absent in L. amambaia (Fig. 1B),
L. canescens (Fig. 2F), L. eriolepis (Fig. 3F), L. mapirensis (Fig. 3H),
and L. myriocephala (Fig. 4B) (Tab. 2).
Mesocarp: This region comprises one to nine layers of
cells (Figs. 1B, D, F, H; 2B, D, F, H; 3B, D, F, H; 4B, D, F, H;
5B, D, F; 6B, E, G). Two distinct regions are observed in the
mesocarp. The outer mesocarp is formed, generally, of one
or two layers of cells, except in L. chamissonis (Fig. 2G, H),
L. myriocephala, and L. remotiflora (Fig. 5C, D), which, in
some regions, can have more than two layers of cells. The
cells of the outer mesocarp can be periclinally elongated or
isodiametric. They are small compared to the cells of the
inner mesocarp (i.e., L. balansae - Fig. 1H). The wall of the
mesocarp cells can be formed of primary or secondary walls.
Crystals are observed in the outer mesocarp of all species,
mainly in the cell layer closest to the exocarp (Figs. 1D;
4D, F, H; 5B, D, F) (Tab. 2). In most of the species, the
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Danilo Marques, Rafael de Oliveira Franca, Massimiliano Dematteis and Juliana Marzinek
Table 1. Voucher information for species of Lepidaploa used in the present study.
Species
L. amambaia H. Rob.
L. argyrotricha (Sch. Bip. ex Baker)
H.Rob.
L. bakerana (Britton) H. Rob.
L. balansae (Hieron.) H. Rob.
L. beckii H. Rob.
L. buchtienii (Gleason) H. Rob.
L. canescens (Kunth) H. Rob.
L. chamissonis (Less.) H. Rob.
L. costata (Rusby) H. Rob.
L. deflexa (Rusby) H. Rob.
L. eriolepis (Gardner) H. Rob.
L. mapirensis (Gleason) H. Rob.
L. myriocephala (DC.) H. Rob.
L. novarae (Cabrera)
L. pseudomuricata H. Rob.
Voucher
M. Dematteis & A. Schinini 867 (CTES)
Country and Locality
Paraguay. Amambay, 25 km of N de J. P. Caballero.
M. Dematteis et al. 3336 (CTES)
Paraguay. Concepción, 25 km W de San Carlos del Apa.
Estancia Arrecifes.
E. Barbosa et al.1012 (CTES)
Brazil. Paraná, Bocaiuva do Sul.
A. Fuentes et al. 7042 (CTES)
St. G. Beck 8317 (CTES)
E. Adenesky s.n. (FLOR 4542)
Bolivia. La Paz, Province Muñecas.
Bolivia. La Paz, Province Nor Yungas.
Brasil. Santa Catarina, Chapecó.
E. Valduga & E. Pasini 81 (FURB)
Brasil. Rio Grande do Sul, Bento Gonçalves-Vale dos
Vinhedos.
J.A. Jarenkow 1689 (FLOR)
St. G. Beck 21420 (CTES)
St. G. Beck 14931 (CTES)
St. G. Beck 29463 (CTES)
St. G. Beck 12108 (CTES)
L. A. Funez 1928 (FURB)
Brasil. Rio Grande do Sul, Lajeado, Vale do Arroio.
Bolivia. La Paz, Province Nor Yungas, Coroico.
Bolivia. La Paz, Province Nor Yungas.
Bolivia. La Paz, Provincia Larecaja.
Bolivia. La Paz, Sud Yuangas, Chulumani.
Brasil. Santa Catarina, Itajaí.
M. Verdi et al. 4028 (FURB)
Brasil. Santa Catarina, Imaruí, Parque Estadual da
Serra do Tabuleiro.
St. G. Beck 29455 (CTES)
Bolivia. La Paz, Province Larecaja.
St. G. Beck 28282 (CTES)
Bolivia. La Paz, Province Larecaja, Villaque Poroma,
Vale del rio Sapucuni.
J.R.I. Wood & D. Wasshausen 13906 (CTES)
Bolivia. La Paz, Larecajaca, 25-30 km N of Caravanito.
St. G. Beck 29174 (CTES)
Bolivia. La Paz, Province J. Bautista Saavedra, Apolo,
Yurilaya.
St. G. Beck 22758 (CTES)
Bolivia. Departamento La Paz, Province Sud Yungas.
A. Stival-Santos et al. 785 (FURB)
Brasil. Santa Catarina, Santo Amaro da Imperatriz,
Cova da Onça.
A. Korte & A. Kniess 4010 (FURB)
Brasil. Santa Catarina, Nova Trento, Valsugana.
J.C. Solomon 9656 (CTES)
Bolivia. La Paz, Province Nor Yungas, 0.9 km W of
Chuspipata.
J.C. Solomon 15318 (CTES)
M. Dematteis 1221 (CTES)
Bolivia. La Paz. Province Nor Yungas.
Bolivia. La Paz, Province Larecaja.
M. Dematteis 1116 (CTES)
Bolivia. La Paz, Provincia Nor Yungas, 2 km N
of Canavari.
O. Ahumada & J. Aguero 8365 (CTES)
Vervoorst 4581 (CTES)
Argentina. Salta, Santa Victoria, Parque San Martín.
Argentina. Salta, Santa Victoria, Parque San Martín.
M. Verdi et al. 5909 (FURB)
Brasil. Santa Catarina, Bom Jardim da Serra, Farm
Papagaios.
A. Korte et al. 5917 (FURB)
Brasil. Santa Catarina, Campo Alegre, Campinas dos
Faxinais.
M. Verdi et al. 5874 (FURB)
Brasil. Santa Catarina, Pouso Redondo, Corruchel.
A. Krapovickas & C.L. Cristóbal 44612 (CTES)
Argentina. Misiones, San Ignacio, Quiroga’s house.
L. psilostachya (DC.) H. Rob.
E. Cabral et al. 348 (CTES)
Argentina. Misiones, San Ignacio.
H. A. Keller 4096 (CTES)
Argentina. Misiones, General San Martín, Route 211.
L. remotiflora (Rich.) H. Rob.
H. A. Keller 6416 (CTES)
Argentina. Misiones, San Ignacio, Club del Río.
E. Guitierrez & E. Chavez 2185 (CTES)
Bolivia, German Busch., Rio Negro.
M. Dematteis 1020 (CTES)
Bolivia. Santa Cruz, Ichilo, 4 km E of San Carlos.
L. salzmannii (DC.) H. Rob.
M. Dematteis 3438 (CTES)
Bolivia. Tarija, O’Connor, 8,3 km E of Entre Rios.
L. J. Novara 10877 (CTES)
Argentina. Salta, Rosario de Lerma, Dique Las Lomitas.
V. S. Neffa et al. 1305 (CTES)
Bolivia. Santa Cruz. Chiquitos, 15 km E of Ipias.
L. setososquamosa (Hieron.) M.B. Angulo
& M. Dematt.
Paraguay. Boquerón, Parque Valle Natural, 25 km S of
A. Krapovickas & C. L. Cristóbal 44197 (CTES)
Filadelfia.
L. sordidopapposa (Hieron.) H. Rob.
L. tarijensis (Griseb.) H. Rob.
644
St. G. Beck 22672 (CTES)
St. G. Beck 17717 (CTES)
A. Krapovickas et al. 19425 (CTES)
A. G. Schinini 5189 (CTES)
Acta Botanica Brasilica - 32(4): 642-655. October-December 2018
Bolivia. La Paz, Province Nor Yungas.
Bolivia. La Paz, Province Nor Yungas.
Argentina. Salta, General San Martín, Pocitos.
Argentina. Salta, Quebrada de la Virgen.
Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): anatomy and taxonomic implications
Figure 1. Transversal sections of the fruit of the studied species of Lepidaploa: A-B. L. amambaia; C-D. L. argyrotricha, in D detail of
crystals in the outer mesocarp; E-F. L. bakerana; G-H. L. balansae, in H note the endocarp. cr: crystals; ex: exocarp; im: inner mesocarp;
om: outer mesocarp; se: seed; tr: trichome; vb: vascular bundles; arrowhead: vascular bundles in seed.
Acta Botanica Brasilica - 32(4): 642-655. October-December 2018
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Danilo Marques, Rafael de Oliveira Franca, Massimiliano Dematteis and Juliana Marzinek
Figure 2. Transversal sections of the fruit of the studied species of Lepidaploa: A-B. L. beckii; C-D. L. buchtienii; E-F. L. canescens;
G-H. L. chamissonis; arrow: disintegrating inner mesocarp; se: seed; vb: vascular bundles.
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Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): anatomy and taxonomic implications
Figure 3. Transversal sections of the fruit of the studied species of Lepidaploa : A-B. L. costata; C-D. L. deflexa, in D detail of idioblasts
in the exocarp. E-F. L. eriolepis; G-H. L. mapirensis. ex: exocarp; id: idioblasts; im: inner mesocarp; om: outer mesocarp; se: seed; tr:
trichome; vb: vascular bundles.
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Figure 4. Transversal sections of the fruit of the studied species of Lepidaploa: A-B. L. myriocephala; C-D. L. novarae, in D detail of
idioblasts in the exocarp and detail of the crystals in the outer mesocarp; E-F. Immature cypsela of L. pseudomuricata; G-H. Mature
cypsela of L. pseudomuricata. cr: crystals; id: idioblasts; se: seed; vb: vascular bundles.
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Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): anatomy and taxonomic implications
inner mesocarp is partially disintegrated (Figs. 2G; 5C) and
comprises two to seven layers of cells (Figs. 1B, D, F, H; 2B,
D, F, H; 3B, D, F, H; 4B, D, F, H; 5B, D, F; 6B, E, G). However,
the inner mesocarp is wholly consumed in mature cypselae
of L. psilostachya (Fig. 5B). The cells of the inner mesocarp
are parenchymatic with some intercellular spaces (Figs. 1B,
D, F, H; 2B, D, F, H; 3B, D, F, H; 4B, D, F, H; 5B, D, F; 6B, E,
G). Collateral vascular bundles are present in the mesocarp
of all species (Figs. 1C; 2E; 3A; 4A; 5E; 6A). The majority of
cypselae possess ten vascular bundles per cypsela, but in
some species the number of vascular bundles is variable.
For example, some samples of L. amambaia (Fig. 1A), L.
argyrotricha and L. beckii (Fig. 2A) had 11 vascular bundles
per cypsela.
Endocarp: The endocarp is consumed in the middle
region in most of the cypselae, except for L. balansae (Fig.
1H). Stomata are located in middle region of the fruit of
L. setososquamosa (Fig. 7A).
Floral disk: The floral disk is in the apical region of
the fruit where the pappus is inserted. In the analyzed
species, the floral disk is formed of uniseriate exocarp, with
periclinally elongated and juxtaposed cells (Fig. 7B, C). The
Figure 5. Transversal sections of the fruit of the studied species of Lepidaploa: A-B. L. psilostachya; C-D. L. remotiflora; E-F. L.
salzmannii; arrow: disintegrating inner mesocarp; cr: crystal; se: seed; vb: vascular bundles.
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Danilo Marques, Rafael de Oliveira Franca, Massimiliano Dematteis and Juliana Marzinek
periphery of the inner region of the floral disk is composed
of anticlinally elongated cells, while its center is formed of
lignified cells with crystals (Fig. 7B, C).
Pappus: The pappus of all the analyzed species is
biseriate (Fig. 7D, E). In the median transverse section,
the outer series has a fusiform shape, while the inner series
is composed of rounded bristles (Fig. 7D, E). Both series
of the pappus are formed by lignified rounded cells with
projections and vascularized bristles (Fig. 7D, E).
Carpopodium: In all the species studied, the
carpopodium is formed of uniseriate exocarp with
periclinally elongated and juxtaposed cells (Fig. 7F, G). The
wall of the cells of the exocarp, in most of the species, is
lignified (Fig. 7F) (Tab. 2), but in L. amambaia, L. argyrotricha,
L. buchtienii, L. myriocephala, L. salzmannii (Fig. 7G) (Tab. 2),
and L. setososquamosa, this wall is not lignified. Internally,
the carpopodium possesses rounded primary wall cells in
the periphery, while in its center there is a vascular bundle.
Seeds: All seeds are immature, except in L. psilostachya
and L. tarijensis. The exotesta of L. psylostachya (Fig. 5B)
possesses U-shaped thickening, while in L. tarijensis (Fig.
6G) lignification occurs only in the anticlinal wall of the
Figure 6. Transversal sections of the fruit of the studied species of Lepidaploa: A-C. L. setososquamosa, in C detail of a glandular
trichome; D-E. L. sordidopapposa; F-G. L. tarijensis, in G detail of lignified exotesta. co: cotyledon; cr: crystals; et: exotesta; id: idioblast;
vb: vascular bundles.
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Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): anatomy and taxonomic implications
exotesta. All of the species have only one vascular bundle
(Figs. 1G; 2G; 3G), which passes through the region of the
raphe to the region of the chalaza.
Maturation of cypsela: Differences between the outer
mesocarp cells of immature and mature cypselae occur in
eight species (L. canescens, L. mapirensis, L. myriocephala,
L. pseudomuricata, L. remotiflora, L. setososquamosa,
L. sordidoppaposa, and L. tarijensis). Immature cypselae
do not possess lignification in the outer mesocarp
(Fig. 7H, I), while in mature cypsela this region possesses
cells lignified (Fig. 7H, I).
Discussion
All of the species analyzed of Lepidaploa exhibited
the same structural pattern of the pericarp that has been
Figure 7. Middle region of cypsela, floral disk, pappus, carpopodium and ribs of the studied species in transversal section. A. L.
setososquamosa, detail of the stomata in the exocarp and endocarp; B. L. eriolepis, floral disk; C. L. salzmannii, detail of lignification
(asterisk) in the floral disk; D-F. L. amambaia, outer and inner series of the pappus; F: L. beckii, detail of the carpopodium with lignified
cells in the exocarp; G. L. salzmannii, detail of the carpopodium without lignified cells in the exocarp; H-I. L. balansae, detail comparing
non-lignified outer mesocarp and lignified outer mesocarp. oi: inner series of the pappus; os: outer series of the pappus; pa: pappus;
st: stomata; tr: trichome; vb: vascular bundles.
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Danilo Marques, Rafael de Oliveira Franca, Massimiliano Dematteis and Juliana Marzinek
reported for other genera of Vernonieae as in Bolanosa
(Redonda-Martínez et al. 2017), Bothriocline (Mukherjee
& Sarkar 2001), Chrysolaena (Martins & Oliveira 2007;
Galastri & Oliveira 2010), Centratherum (Mukherjee &
Sarkar 2001; Redonda-Martínez et al. 2017), Critoniopsis
(Redonda-Martínez et al. 2017), Cyanthillium (Pandey &
Singh 1980; Redonda-Martínez et al. 2017), Cyrtocymura
(Mukherjee & Sarkar 2001; Redonda-Martínez et al. 2017),
Elephantopus (Pandey & Singh 1980; Mukherjee & Sarkar
2001; Redonda-Martínez et al. 2017), Gymnanthemum
(Mukherjee & Sarkar 2001), Harleya (Redonda-Martínez
et al. 2017), Heterocoma (Freitas et al. 2015), Leiboldia,
Lepidonia (Redonda-Martínez et al. 2017), Lessingianthus
(Martins & Oliveira 2007), Piptocarpha, Pseudoelephantopus
(Redonda-Martínez et al. 2017), Rolandra (Mukherjee &
Sarkar 2001), Spiracantha, Stenocephalum, Stramentopappus
(Redonda-Martínez et al. 2017), Vernonanthura (Mukherjee
& Sarkar 2001; Redonda-Martínez et al. 2017), and Vernonia
s.s. (Misra 1972; Pandey & Singh 1980; Mukherjee & Sarkar
2001; Jana & Mukherjee 2013; Redonda-Martínez et al.
2017). In other words, the cypselae of Lepidaploa possess
four different regions, which were generally disintegrated:
exocarp, outer mesocarp, inner mesocarp and endocarp.
The uniseriate exocarp also exhibited the same pattern
as that found for other Vernonieae genera as in Bolanosa
(Redonda-Martínez et al. 2017), Bothriocline (Mukherjee
& Sarkar 2001), Chrysolaena (Martins & Oliveira, 2007;
Galastri & Oliveira 2010), Centratherum (Mukherjee &
Sarkar 2001; Redonda-Martínez et al. 2017), Critoniopsis
(Redonda-Martínez et al. 2017), Cyanthillium (Pandey &
Singh 1980; Redonda-Martínez et al. 2017), Cyrtocymura
(Mukherjee & Sarkar 2001; Redonda-Martínez et al. 2017),
Elephantopus (Pandey & Singh 1980; Mukherjee & Sarkar
2001; Redonda-Martínez et al. 2017), Gymnanthemum
(Mukherjee & Sarkar 2001), Harleya (Redonda-Martínez
et al. 2017), Heterocoma (Freitas et al. 2015), Leiboldia,
Lepidonia (Redonda-Martínez et al. 2017), Lessingianthus
(Martins & Oliveira 2007), Piptocarpha, Pseudoelephantopus
(Redonda-Martínez et al. 2017), Rolandra (Mukherjee &
Sarkar 2001), Spiracantha, Stenocephalum, Stramentopappus
(Redonda-Martínez et al. 2017), Vernonanthura (Mukherjee
& Sarkar 2001; Redonda-Martínez et al. 2017), and Vernonia
s.s. (Misra 1972; Pandey & Singh 1980; Mukherjee & Sarkar
2001; Jana & Mukherjee 2013; Redonda-Martínez et al.
2017). However, different sizes for the epidermal cells
in the ribs and inter-ribs is reported for the first time.
The presence of idioblasts and glandular trichomes in
some species is important for taxonomic differentiation,
whereas biseriate non-glandular trichomes, which were
found in all species, have no taxonomic value within
Vernonieae. According to Isawumi et al. (1966), idioblasts
are generally present in species of Vernonieae and they may
be characteristic structures of the tribe. Previous studies
report the presence of idioblasts in Asian and African
species of Vernonieae (Mukherjee & Sarkar 2001; Basak
& Mukherjee 2003; Jana & Mukherjee 2012; Mukherjee
& Nordenstam 2012), and American species of the tribe
(Angulo et al. 2015; Redonda-Martínez et al. 2017; Pico et
al. 2016). Despite their taxonomic importance at the tribal
level, idioblasts must be used with care in the delimitation of
Table 2. Morphological and anatomical features of the fruit of the studied species of Lepidaploa. ? = unknown.
Pericarp
Exocarp
Species
All ribs
defined
Glandular
trichome
Stomata
Idioblast
L. amambaia
L. argyrotricha
L .bakerana
L. balansae
L. beckii
L. buchtienii
L. canescens
L. chamissonis
L. costata
L. deflexa
L. eriolepis
L. mapirensis
L. myriocephala
L. novarae
L. pseudomuricata
L. psilostachya
L. remotiflora
L. salzmannii
L. setososquamosa
L. sordidopapposa
L. tarijensis
no
yes
yes
no
no
no
no
no
yes
no
no
no
no
yes
yes
no
no
yes
no
no
yes
absent
absent
absent
absent
absent
absent
absent
present
absent
absent
absent
absent
absent
absent
present
absent
absent
present
present
absent
absent
absent
absent
absent
present
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
absent
present
absent
absent
absent
present
present
present
present
present
absent
present
present
present
absent
absent
absent
present
present
present
present
present
present
present
present
652
Mesocarp
Carpopodium
Outer mesocarp:
number of layers
non-lignified
non-lignified
lignified
lignified
lignified
non-lignified
lignified
lignified
lignified
lignified
lignified
lignified
non-lignified
lignified
lignified
lignified
lignified
non-lignified
non-lignified
lignified
lignified
2
2
1-2
1-2
1-2
1
1-2
1-3
1-2
2
2
1-2
2-4
1
1-2
2
1-3
1-2
1-2
1-2
1-2
Acta Botanica Brasilica - 32(4): 642-655. October-December 2018
Endocarp
Crystals
Number of
vascular bundles
Stomata
present
present
present
present
present
present
present
present
present
present
present
present
present
present
present
present
present
present
present
present
present
10-11
10-11
10
10
10-11
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
?
?
?
present
?
?
?
?
?
?
?
?
?
?
?
?
?
?
present
?
?
Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): anatomy and taxonomic implications
species. The presence of a glandular trichome in four species
is an important taxonomic character for the differentiation
of some entities. For example, among the closely related
species L. amambaia, L. remotiflora and L. setososquamosa, the
last can be differentiated because it is the only one of this
group that possesses glandular trichomes on the cypsela.
Another species that also possesses this type of trichome
is L. chamissonis, differentiating it from L. argyrotrichia,
which does not possess glandular trichomes in the fruit.
The outer mesocarp exhibited two patterns: layers of
cells non lignified or layers of cells lignified. This variation
may be due to different stages of fruit development since we
analyzed immature and mature cypselae of eight species (L.
canescens, L. mapirensis, L. myriocephala, L. pseudomuricata,
L. remotiflora, L. setososquamosa, L. sordidoppaposa and L.
tarijensis). Ontogenic studies of the fruit of Chrysolaena
obovata (Galastri & Oliveira 2010) reported four stages of
maturation and demonstrated the structural differences
of the outer mesocarp in these stages. Galastri & Oliveira
(2010) observed that the outer and inner mesocarp differs
in shape and size, and that there is gradual lignification. We
also observed the pattern found in Chrysolaena obovata in
the eight species of Lepidaploa mentioned above. Crystals
were observed only in the outer mesocarp of all species.
In transversal section, these crystals have a quadratic or
rectangular shape. The presence of crystals is common
within Vernonieae (Misra 1972; Pandey & Singh 1980;
Mukherjee & Sarkar 2001; Martins & Oliveira 2007;
Galastri & Oliveira 2010; Redonda-Martínez et al. 2017).
According to King & Robinson (1987), the production of
crystals in fruits is possibly antagonistic to the production
of phytomelanin, a black substance found in the cypselae of
species of Eupatorieae (Robinson et al. 2009; De-Paula et al.
2013), Heliantheae (Baldwin 2009), and Heterocoma (Freitas
et al. 2015) (Vernonieae). Considering the antagonism
hypothesis of King & Robinson (1987), we did not find
phytomelanin in the cypselae of the species of Lepidaploa
studied here.
The outer mesocarp of all Lepidaploa studied is
continuous, and the number of layers present in this region
does not exhibit great interspecific variability. Therefore,
this region does not have taxonomic value among species
of Lepidaploa, as demonstrated for the genera and species
studied by Redonda-Martínez et al. (2017). In relation to
the taxonomic importance of the outer mesocarp at the
generic level, Chrysolaena (as seen in C. obovata and C.
platensis) possesses the same number of cell layers (Martins
& Oliveira 2007; Galastri & Oliveira 2010) as its sister
genus, Lepidaploa. Meanwhile, Lessingianthus brevifolius
(Martins & Oliveira 2007), a species of the sister genus
of Chrysolaena and Lepidaploa, exhibited only one layer
of cells in the outer mesocarp, and so may represent a
taxonomic difference between Chrysolaena + Lepidaploa
and Lessingianthus, if this same pattern is confirmed in the
other species of Lessingianthus. Although this character is
sufficient to differentiate Lessingianthus brevifolius from
the other two genera, the number of cell layers must be
used with care in the taxonomy of the group, since there
are records in the literature of variation in the number of
layers in different regions of the same fruit, as reported
for Cyanthillium cinereum (Tiagi & Taimni 1960; Pandey
& Singh 1980), V. fasciculata, V. missurica (Pandey & Singh
1980), and V. anthelmintica (Misra 1972; Pandey & Singh
1980; Talukdar 2015).
Variation in the number of ribs compared to the number
of vascular bundles of the cypselae was found among the
species analyzed. The number of vascular bundles does not
necessarily correspond to the number of ribs since there are
ribs in the fruits of Lepidaploa that are undefined. Differences
between the number of ribs and the number of vascular
bundles were also found for Vernonia bainesii, V. cistifolia
(Mukherjee & Sarkar 2001), V. galamensis (Jana & Mukherjee
2013), Cyanthillium cinereum (Pandey & Singh 1980),
Chrysolaena obovata, Lessingianthus brevifolius (Martins &
Oliveira 2007), and Chrysolaena platensis (Galastri & Oliveira
2010). According to Marzinek et al. (2010), the formation of
ribs is related to the position occupied by the flower in the
capitula, which would generate the variability in the ribs of
Lepidaploa. Our anatomical studies show that the number
of ribs must be used carefully in the delimitation of genera
and species, because several taxonomic studies have used the
number of ribs to separate species, and sometimes genera,
within the Vernonieae. However, in Lepidaploa the number
of ribs is not taxonomically informative, given that some
ribs are not conspicuous and cannot be seen with external
morphological study.
The shape of the cells and the type of cell wall of the
inner mesocarp found in the present study is similar
that found in other Vernonieae genera, such as Bolanosa
(Redonda-Martínez et al. 2017), Bothriocline (Mukherjee
& Sarkar 2001), Chrysolaena (Martins & Oliveira, 2007;
Galastri & Oliveira 2010), Centratherum (Mukherjee &
Sarkar 2001; Redonda-Martínez et al. 2017), Critoniopsis
(Redonda-Martínez et al. 2017), Cyanthillium (Pandey &
Singh 1980; Redonda-Martínez et al. 2017), Cyrtocymura
(Mukherjee & Sarkar 2001; Redonda-Martínez et al. 2017),
Elephantopus (Pandey & Singh 1980; Mukherjee & Sarkar
2001; Redonda-Martínez et al. 2017), Gymnanthemum
(Mukherjee & Sarkar 2001), Harleya (Redonda-Martínez
et al. 2017), Heterocoma (Freitas et al. 2015), Leiboldia,
Lepidonia (Redonda-Martínez et al. 2017), Lessingianthus
(Martins & Oliveira 2007), Piptocarpha, Pseudoelephantopus
(Redonda-Martínez et al. 2017), Rolandra (Mukherjee &
Sarkar 2001), Spiracantha, Stenocephalum, Stramentopappus
(Redonda-Martínez et al. 2017), Vernonanthura (Mukherjee
& Sarkar 2001; Redonda-Martínez et al. 2017), and Vernonia
s.s. (Misra 1972; Pandey & Singh 1980; Mukherjee & Sarkar
2001; Jana & Mukherjee 2013; Redonda-Martínez et al.
2017). It is worth pointing out that the pericarp of species
of Vernonieae is non-multiplicative, which is confirmed by
Acta Botanica Brasilica - 32(4): 642-655. October-December 2018
653
Danilo Marques, Rafael de Oliveira Franca, Massimiliano Dematteis and Juliana Marzinek
the consumed inner mesocarp of the cypselae of, mainly,
L. psylostachya and L. tarijensis. According to Martins &
Oliveira (2007), the small size of the pericarp of Chrysolaena
obovata and Lessingianthus brevifolius favors dispersion by
anemochory because the reduced number of layers of this
region makes the fruit lighter. The consumed of the inner
mesocarp during fruit maturation was also observed for
the species studied by Tiagi & Taimni (1960) and Misra
(1972), and in recent works with Chrysolaena obovata and
Lessingianthus brevifolius (Martins & Oliveira 2007) and
Chrysolaena platensis (Galastri & Oliveira 2010).
The floral disk is similar to the some species of Vernonia
s.s. (Pandey & Singh 1980), and in Chrysolaena platensis
(Galastri & Oliveira 2010). There were no significant
differences among the floral disks of the different species
analyzed in the present study, with the exception that some
possessed lignified exocarp lignified in this region. However,
this difference in lignin deposition in the exocarp wall may
be related to the degree of maturity of the fruit, as suggested
for the region of the outer mesocarp. Galastri & Oliveira
(2010) observed crystals on floral disks in Chrysolaena
platensis, but Marzinek & Oliveira (2010) and Silva et al.
(2018) described only phytomelanin in this structure of
species of Eupatorieae.
The basal region known as carpopodium is present in
all the species analyzed here. The carpopodium anatomy
was previously studied only for Chrysolaena obovata,
Lessingianthus brevifolius (Martins & Oliveira 2007) and
Chrysolaena platensis (Galastri & Oliveira 2010). The
carpopodium of Lepidaploa is similar to the carpopodium
found in Chrysolaena (Martins & Oliveira 2007) and
Lessingianthus (Galastri & Oliveira 2010). In other words,
this structure presents a uniseriate exocarp and its interior
has parenchyma cells containing a group of sclereids in the
center. Among the anatomical features studied, lignification
in the exocarp of the carpopodium is the one that proved
most useful for differentiating species. Some species
exhibited an exocarp with a non-lignified wall, while the
exocarp of other taxa possessed lignification of this region.
We observed this difference among cypselae at the same
stage of maturation, which indicates that it can be a useful
character for differentiating closely related species. For
example, L. remotiflora, a close relative of L. amambaia and
L. setososquamosa, is the only one that possesses lignified
cells of the exocarp of the carpopodium, while the others lack
lignification. This difference is also important for separating
L. argyrotricha (carpopodium with non-lignified exocarp)
from L. chamissonis (carpopodium with lignified exocarp).
The seeds of Lepidaploa provide important taxonomic
data, especially the characters of the testa. The exotesta of the
seeds of L. psylostachya and L. tarijensis possess a secondary
wall in the anticlinal and periclinal walls, and only in the
anticlinal wall, respectively. The presence of a secondary wall
of the exotesta was also reported in Vernonia anthelmintica,
which exhibited U-shaped lignification (Talukdar 2015).
654
It is worth mentioning that Jana & Mukherjee (2013)
did not observe the presence of a secondary wall in the
exotesta of the same specimen of V. anthelmintica, which
could be related to the degree of maturity of the cypsela. In
Chrysolaena platensis (Galastri & Oliveira 2010), the region
of the mesotesta and endotesta are consumed in the mature
seed, however, lignin deposition was observed in the stages
prior to the collapse of this structure.
The pappus is an important modification of the sepals
that acts in the dispersion of the fruit (Roth 1977). We
observed lignified cells with projections in the bristles of
Lepidaploa; both structures were also found in species of
Eupatorieae (Marzinek & Oliveira 2010) and in Chrysolaena
obovata and Lessingianthus brevifolius (Martins & Oliveira
2007) of Vernonieae. Similarly, the presence of vascular
bundles in the interior of each bristle of Lepidaploa was also
found in other genera of Eupatorieae (King & Robinson
1987; Marzinek & Oliveira 2010) and Vernonieae (Misra
1972). However, previous studies show that vascular
bundles are absent in the bristles of Chrysolaena obovata,
Lessingianthus brevifolius (Martins & Oliveira 2007) and
Chrysolaena platensis (Galastri & Oliveira 2010). Although
vascular bundles are absent in species of Chrysolaena and
Lessingianthus, more species of these genera need to be
studied in order to establish the taxonomic validity of this
absence. According to Mukherjee & Sarkar (2001), the
pappus is an important structure for the identification of
genera and species. The species of Lepidaploa exhibited the
same pattern for the pappus, and so the anatomy of this
structure cannot be used as a taxonomic tool to separate
these entities. On the other hand, the anatomy of the pappus
could be important for distinguishing Lepidaploa from
Chrysolaena and Lessingianthus. In Chrysolaena (Martins &
Oliveira 2007; Galastri & Oliveira 2010) and Lessingianthus
(Martins & Oliveira 2007), the bristles of the pappus do not
possess vascular bundles, which would differentiate these
two genera from the closely related genus Lepidaploa, which
possesses vascular bundles in the pappus.
Conclusion
The cypselae of Lepidaploa species exhibited biseriate
trichomes, uniseriate exocarp, outer mesocarp (generally
with one or two layers of cells and the presence of crystals),
and vascular bundles in the inner mesocarp; this morphology
is similar to that of other taxa of Vernonieae. However, there
are important taxonomic differences between species in
relation to idioblasts, glandular trichomes, lignification
of the carpopodium, and pappus vascularization. The
significance of carpopodium lignification for identifying
species of Lepidaploa is reported here for the first time.
In addition, the pappus vascularization and number of
mesocarp layers could provide important taxonomic data
for segregating Chrysolaena, Lepidaploa and Lessingianthus
genera.
Acta Botanica Brasilica - 32(4): 642-655. October-December 2018
Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): anatomy and taxonomic implications
Acknowledgements
We thank Consejo Nacional de Investigaciones Científicas y
Técnicas and Agencia Nacional de Promoción Científica y
Tecnológica for providing financial support.
References
Anderson LC. 1963. Studies on Petradoria (Compositae): anatomy, cytology,
taxonomy. Transactions of the Kansas Academy of Science 66: 632-684.
Angulo MB, Sosa MM, Dematteis M. 2015. Systematic significance of
cypsela morphology in Lessingianthus (Vernonieae, Asteraceae).
Australian Systematic Botany 28: 173-189.
Baldwin BG 2009. Heliantheae alliance. In: Funk VA, Susanna A, Stuessy
TF, Bayer RJ. (eds.) Systematics, evolution and biogeography of
Compositae. Vienna, IAPT. p. 689-711.
Basak N, Mukherjee SK 2003. Taxonomic significance of cypselar features
in some species of Vernonia (Vernonieae-Asteraceae). Journal of Hill
Research 1: 9-15.
De-Paula OC, Marzinek J, Oliveira DMT, Machado SRM. 2013. The role of
fibers and the hypodermis in Compositae melanin secretion. Micron
44: 312-316.
Freitas FS, De-Paula OC, Nakajima JN, Marzinek J. 2015. Fruits of
Heterocoma (Vernonieae-Lychnophorinae): taxonomic significance
and a new pattern of phytomelanin deposition in Asteraceae. Botanical
Journal of the Linnean Society 179: 255-265.
Funk VA, Bayer RJ, Keeley S, et al. 2005. Everywhere but Antarctica:
using a supertree to understand the diversity and distribution of the
Compositae. Biologiske Skrifter 55: 343-374.
Galastri N, Oliveira DMT. 2010. Morfoanatomia e ontogênese do fruto
e semente de Vernonia platensis (Spreng.) Less. (Asteraceae). Acta
Botanica Brasilica 24: 73-83.
Isawumi MA, El-Ghazaly G, Nordenstam B. 1996. Pollen morphology, floral
microcharacters and taxonomy of the genus Baccharoides Moench
(Vernonieae: Asteraceae). Grana 35: 205-230.
Jana BK, Mukherjee SK. 2012. Variations of cipselas of five taxa of the
tribe Vernonieae (Asteraceae). International Journal of Pharma and
Bio Sciences 1: 420-435.
Jana BK, Mukherjee SK. 2013. Cypselar anatomy of some taxa of
Compositae. Journal of Chemical and Pharmaceutical Research 2:
417-443.
Keeley SC, Forsman ZH, Chan R. 2007. A phylogeny of the ‘‘evil tribe’’
(Vernonieae: Compositae) reveals Old/New World long distance
dispersal: Support from separate and combined congruent datasets
(trnL-F, ndhF, ITS). Molecular Phylogenetics and Evolution 44: 89-03.
Keeley SC, Jansen RK. 1994. Chloroplast DNA restriction site variation
in the Vernonieae (Asteraceae), an initial appraisal of the relationship
of New and Old World taxa and the monophyly of Vernonia. Plant
Systematics and Evolution 193: 249-265.
Keeley SC, Robinson H. 2009. Vernonieae. In: Funk VA, Susanna A,
Stuessy TF, Bayer RJ. (eds.) Systematics, evolution and biogeography
of Compositae. Vienna, IAPT p. 439-469.
King RM, Robinson H. 1987. The genera of the Eupatorieae (Asteraceae).
Monographs in Systematic Botany 22. St. Louis, Missouri Botanical
Garden.
Marques D, Dematteis M. 2014. Lepidaploa (Cass.) Cass. In: Zuloaga FO,
Belgrano MJ, Anton AM. (eds.) Flora Argentina, flora vascular de la
República Argentina Dicotyledoneae Asteraceae: Senecio a Vernonieae.
Buenos Aires, IBODA CONICET. p. 243-249.
Martins MAG, Oliveira DMT. 2007. Morfoanatomia comparada dos frutos
em desenvolvimento de Vernonia brevifolia Less. e V. herbacea (Vell.)
Rusby (Asteraceae). Revista Brasileira de Botânica 30: 101-112.
Marzinek J, De-Paula OC, Oliveira DMT. 2010. The ribs of Eupatorieae
(Asteraceae): of wide taxonomic value or reliable characters only
among certain groups? Plant Systematics and Evolution 285: 127-130.
Marzinek J, Oliveira DMT. 2010. Structure and ontogeny of the pericarp
of six Eupatorieae (Asteraceae) with ecological and taxonomic
considerations. Anais da Academia Brasileira de Ciências 82: 279-291.
Misra BS. 1972. Floral Morphology of the family Compositae V. The seed
coat and pericarp in Verbesina encelioides (Cav.) Benth.and Hk. F. ex.
A Gray. Journal of the Indian Botanical Society 51: 332-341.
Mukherjee SK, Nordenstam B. 2012. Diversity of trichomes from mature
cypselar surface of some taxa from basal tribes of Compositae.
Compositae Newslett 50:78-125
Mukherjee SK, Sarkar AK. 2001. Study of macro-morphological and
anatomical structures of cypselas of eighteen taxa of the tribe
Vernonieae (Asteraceae). Journal of the National Botanical Society
India 55: 85-104.
O’Brien TP, Feder N, McCully ME. 1964. Polychromatic staining of plant
cell walls by toluidine blue O. Protoplasma 59: 368-373.
Pandey AK, Singh RP. 1980. Development and Structure of Seeds and
Fruits in Tribe Vernonieae - some Vernonia and Elephantopus species.
Flora 169: 443-452.
Pico GMV, Veja AJ, Dematteis M. 2016. Systematic consideration of floral
microcharacters of the South American genus Chrysolaena (Vernonieae,
Asteraceae). Systematics and Biodiversity 14: 224-243.
Pruski JF. 2017. Compositae of Central America-VIII. The genus Lepidaploa
(Vernonieae). Phytoneuron 50: 1-39.
Redonda-Martínez R, Terrazas T, Rojas-Leal A, Villaseñor JL. 2017. The
morpho-anatomy of cypselae in subtribe Leiboldiinae (Vernonieae,
Asteraceae). Brazilian Journal of Botany 40: 491-502.
Redonda-Martínez R, Villaseñor JL. 2011. El género Lepidaploa (Familia
Asteraceae, Tribu Vernonieae) en México. Revista Mexicana de
Biodiversidad 82: 782-797.
Robinson H. 1999. Generic and subtribal classification of American
Vernonieae. Smithsonian Contributions to Botany 89: 1-116.
Robinson H, Schilling E, Panero JE. 2009. Eupatorieae. In: Funk VA,
Susanna A, Stuessy TF, Bayer RJ. (eds.) Systematics, evolution and
biogeography of Compositae. Vienna, IAPT. p. 731-744.
Roth I. 1977. Fruits of angiosperms. Handbuch der Pflanzenanatomie.
Berlin, Stuttgart.
Semir J, Rezende AR, Monge M, Lopes NP. 2011. As Arnicas endêmicas das
Serras do Brasil: uma visão sobre a biologia e a química das espécies
de Lychnophora (Asteraceae). Ouro Preto, UFOP.
Silva TDG, Marzinek J, Hattori EKO, Nakajima JN, De-Paula OC. 2018.
Comparative cypsela morphology in Disynaphiinae and implications
for their systematics and evolution (Eupatorieae: Asteraceae). Botanical
Journal of the Linnean Society 186: 89-107.
Talukdar T. 2015. Taxonomic significance of cypsela in Vernonia
anthelmintica Willd. and V. cinerea Less. (Asteraceae; tribe - Vernonieae):
Structural manifestations. Plant Science Today 2: 107-115.
Tiagi B, Taimni S. 1960. Embryo-sac development in Vernonia cinerascens
Schult. and seed development in V. cinerea Less. Current Science
30: 406.
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Danilo Marques