Acta Botanica Brasilica, 2023, 37: e20220208

doi: https://doi.org/10.1590/1677-941X-ABB-2022-0208

Original article

Pollen morphology of the early branching papilionoid legume genera

Harleyodendron, Holocalyx and Uribea
Débora Cavalcante de Oliveira1* , Luis Carlos Casas Restrepo1, Márcio Ferreira dos Santos1, 2,
Luciano Paganucci de Queiroz1 and Francisco de Assis Ribeiro dos Santos 1

Received: August 12, 2022

Accepted: November 01, 2022

ABSTRACT
.

In this study, pollen grains of Harleyodendron unifoliolatum, Holocalyx balansae, and Uribea tamarindoides, three
monospecific genera with Neotropical distribution belonging to the clade Exostyleae, one of the basal lineages of
the family Leguminosae, subfamily Papilionoideae, were analyzed. The palynological material was acetolyzed and
analyzed under light microscopy (LM) and scanning electron microscopy (SEM). Under LM, small and medium-sized
pollen grains were observed, which showed a prolate-spheroidal to prolate shape, 3-colporate, microreticulate and
reticulate exine, sexine and nexine of equal thickness in Harleyodendron and Holocalyx, while the sexine was thicker
than nexine in Uribea. Analysis under SEM showed finely granulate, psilate, and granulate apertural membrane, while
the exine ornamentation varied from perforate-microechinate in Harleyodendron, to perforate in Holocalyx, while
in Uribea showed an irregular relief and granular projections on the perforate tectum. The pollen morphology of
these species is similar to each other, varying in sexine/nexine ratio, apertural membrane, and exine ornamentation.
Harleyodendron has a finely granulate apertural membrane, sexine and nexine of equal thickness, and a perforate-
microreticulate exine ornamentation, Holocalyx shows a psilated apertural membrane, sexine and nexine of equal
thickness, and exine ornamentation perforate, and Uribea has a granulate apertural membrane, sexine thicker than
nexine, and exine ornamentation with granular projections.

Keywords: Palynology, Exostyleae, Pollen grains, Papilionoideae, Leguminosae.

1 Programa de Pós-Graduação em Botânica, Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, 44036-900, Feira de
Santana, BA, Brazil
2 Plataforma de Microscopia Eletrônica, Instituto Gonçalo Moniz, Fiocruz Bahia, 40296-710, Salvador, BA, Brazil

* Corresponding author: debora.cavalcante7@gmail.com

 Débora Cavalcante de Oliveira, Luis Carlos Casas Restrepo, Márcio Ferreira dos Santos,
Luciano Paganucci de Queiroz and Francisco de Assis Ribeiro dos Santos

Introduction Neuw. & Nees), and sharing the serrate to spinescent leaf
or leaflet margins, basifixed anthers, and drupaceous fruits
(Herendeen 1995; Mansano et al. 2004; Cardoso et al. 2013).
The Exostyleae clade is one of the early-diverging The monospecific genera Harleyodendron, Holocalyx, and
lineages of the papilionoid legumes (Cardoso et al. 2012; Uribea are trees distributed in humid and seasonally dry
2013; Zhang et al. 2020; Zhao et al. 2021). It includes six forests through South and Central America (Cardoso et al.
species-poor neotropical genera characterized by non- 2012) that exhibit a very different floral morphology (Fig. 1).
papilionate flowers varying from truly radially symmetrical Harleyodendron is endemic to the Atlantic Forest of South-
(Exostyles Schott, Lecointea Ducke, Harleyodendron R.S. Central Bahia, Brazil (Cowan 1979; Mansano & Tierno
Cowan, and Holocalyx Micheli) to somewhat bilaterally 2020a), while Holocalyx is present in Bahia, Distrito Federal,
symmetrical (Uribea Dugand & Romero and Zollernia Wied- Mato Grosso do Sul, Southeastern and Southern Brazil,


Figure 1. Flowers Harleyodendron unifoliolatum R.S.Cowan (A), Holocalyx balansae Micheli (B), and Uribea tamarindoides Dugand &
Romero (C), Leguminosae. Photos: A. Luciano P. de Queiroz; B. Domingos Cardoso; C. Reinaldo Aguilar Fernández - 3799, taken from
https://www.gbif.org/occurrence/1258470890.

2 Acta Botanica Brasilica, 2023, 37: e20220208

 Pollen morphology of the early branching papilionoid legume
genera Harleyodendron, Holocalyx and Uribea

Eastern Bolivia, Paraguay, and Northern Argentina, were measured and microphotographed using a Leica
distributed in Humid Forests and areas of Seasonally Dry ICC50 W light microscope. All slides were deposited in the
Tropical Forests and Woodlands (SDTFWs) (Mansano & Palinoteca of the Laboratory of Plant Micromorphology at
Viana-Filho 2010; Mansano & Tierno 2020b). Finally, Uribea the Universidade Estadual de Feira de Santana (PUEFS).
is found from Costa Rica to Colombia in Lowland Tropical Under light microscopy (LM), the main morphometric
Forests (Dugand 1962; Allen & Allen 1981; Lewis et al. parameters (equatorial diameter, polar diameter, and
2005). equatorial diameter in polar view) were measured, when
Several studies have indicated that the Exostyleae clade is possible, for 25 pollen grains randomly distributed among
monophyletic, based on molecular and macromorphological at least three slides in order to standardize the sampling.
character analysis, which has allowed the precise delimitation Other parameters (aperture diameter, and thickness of the
of each of its genera (Cardoso et al. 2012; 2013; LPWG 2017; exine, sexine, and nexine) were measured for ten pollen
Zhang et al. 2020; Zhao et al. 2021). Nonetheless, there is grains, also taken at random.
still a gap in the knowledge of the intergeneric relationships For analysis under Scanning Electron Microscopy (SEM),
in the clade, whose doubts arise as a consequence of the the acetolyzed pollen grains were washed in 70% acetone
divergent vegetative and reproductive morphology within and dripped directly onto the specimen holder of the SEM,
each genus, their distant pattern of distribution, and the after total drying, they were metalized by evaporation
lack of phylogenetic resolution regarding the intergeneric of gold in high vacuum and electromicrographed in the
relationships within the clade. For that reason, further JEOL 6390LV microscope from the Electronic Microscopy
research to provide additional information is needed, since Platform of the Oswaldo Cruz Foundation – Gonçalo Moniz
a broader and more comprehensive analysis of the clade and Research Center.
the relationships between its members would be carried All pollen descriptions followed the palynological
out (Cardoso et al. 2012). nomenclature proposed by Punt et al. (2007) and Halbritter
Palynological studies involving representatives of the et al. (2018).
Exostyleae clade (Ferguson & Skvarla 1981; Skvarla &

Results
Ferguson 1988; Ferguson & Schrire 1994; Ferguson et
al. 1994) have shown variation in pollen morphology,
mainly regarding their exine ornamentation. Therefore,
the palynological study of the genera Harleyodendron, Pollen grains of Harleyodendron unifoliolatum, Holocalyx
Holocalyx, and Uribea allows us to understand part of the balansae, and Uribea tamarindoides are monads, isopolar,
micromorphological diversity that exists in the clade and showing sizes ranging from small (Holocalyx) to medium
can be useful as a basis for further and more comprehensive (Harleyodendron and Uribea) (Tab. 1) and shape varying from


research to clarify the intergeneric and interspecific prolate-spheroidal (Harleyodendron and Uribea) to prolate
relationships in the clade Exostyleae. (Holocalyx) (Fig. 2; Tab. 1), amb circular, 3-colporate (Fig. 2),
Thus, this work aims to describe the pollen morphology ectoapertures with tapered ends and constrictions in
of the monospecific genera Harleyodendron, Holocalyx, and the equatorial region (Fig. 2G-L). The endoapertures are
Uribea, aiming to increase the knowledge about them and lalongate with rounded ends, hardly visualized since the
other related genera. constriction of the ectoaperture is positioned upon the
endoaperture. The apertural membrane is finely granulate

Materials and methods

in Harleyodendron, psilate in Holocalyx, and granulate in
Uribea (Fig. 2D, J, O).
Regarding the sexine/nexine ratio, Harleyodendron and
Flower buds from nine specimens belonging to Holocalyx showed pollen grains with sexine and nexine of
Harleyodendron unifoliolatum R.S.Cowan, Holocalyx balansae equal thickness, while in Uribea the sexine is thicker than
Micheli, and Uribea tamarindoides Dugand & Romero the nexine. Under LM, a finely microreticulate exine was
were collected in duplicates of specimens deposited in the observed in Harleyodendron (Fig. 2C). In Holocalyx, the exine
herbaria HUEFS (Herbário da Universidade Estadual de ranged from finely microreticulate to reticulate (Fig. 2H),
Feira de Santana), HUA (Herbario de la Universidad de whereas in Uribea the exine is microreticulate (Fig. 2M).
Antioquia), COL (Herbario Nacional Colombiano), and Furthermore, when analyzed under SEM, pollen grains
CR (National Museum of Costa Rica) (Acronyms following of Harleyodendron are perforate-microechinate (Fig. 2E),
Thiers 2022 [continuously updated]). The analyzed material while those from Holocalyx are perforate with perforations
is cited in Appendix 1. of different sizes (Fig. 2J). On the other hand, the exine
Pollen grains were subjected to the acetolysis method ornamentation in Uribea showed an irregular relief with
(Erdtman 1960), mounted between slides and coverslips granular projections on the perforate tectum and slightly
with glycerin gelatin, and sealed with paraffin for observation rugulate areas (Fig. 2O). The presence of Ubisch bodies in
under Light Microscopy (LM). Under LM, pollen grains the three genera analyzed was registered (Fig. 2D, I, O).

Acta Botanica Brasilica, 2023, 37: e20220208 3

 Débora Cavalcante de Oliveira, Luis Carlos Casas Restrepo, Márcio Ferreira dos Santos,
Luciano Paganucci de Queiroz and Francisco de Assis Ribeiro dos Santos


Figure 2. Pollen grains of Harleyodendron unifoliolatum R.S.Cowan, Holocalyx balansae Micheli, and Uribea tamarindoides Dugand &
Romero (Leguminosae). A-E. H. unifoliolatum: A. Optical section in polar view. B. Optical section in equatorial view. C. Exine (LM).
D. Equatorial view, surface (SEM), apertural membrane (arrow). E. Exine detail (SEM). F-J. H. balansae: F. Optical section in polar view.
G. Aperture. H. Exine (LM). I. Equatorial view, surface (SEM). J. Exine detail (SEM), apertural membrane (arrow). K-O. U. tamarindoides:
K. Optical section in polar view. L. Aperture. M. Exine (LM). N. Equatorial view (SEM). O. Exine detail (SEM), apertural membrane (arrow).

4 Acta Botanica Brasilica, 2023, 37: e20220208

 Pollen morphology of the early branching papilionoid legume
genera Harleyodendron, Holocalyx and Uribea

Table 1. Morphometric data of the pollen grains of species of Harleyodendron unifoliolatum R.S.Cowan, Holocalyx balansae Micheli,
and Uribea tamarindoides Dugand & Romero.
PD ED EDp
Species/Specimen P/E Ecto Endo Sex Nex
x±Sx Range x±Sx Range x±Sx Range
Harleyodendron R.S. Cowan
Harleyodendron unifoliolatum
R.S. Cowan
D. Cardoso 2501 & P.L.R.
25.2±0.27 22.5-27.5 21.8±0.26 20.0-25.0 22.8±0.28 20.0-25.0 1.15 16.8x1.7 4.5x7.5 0.7 0.7
Moraes (HUEFS)
A. Amorim 398 (HUEFS) 23.8±0.20 22.5-25.0 20.4±0.20 17.5-22.5 20.5±0.25 17.5-22.5 1.17 16.9x1.7 4.5x6.2 0.7 0.7
A. Amorim 1254 (HUEFS) 22.2±0.30 20.0-25.0 20.0±0.20 17.5-22.5 20.7±0.22 20.0-22.5 1.10 15.5x2.3 4.4x11.0 0.8 0.8
Holocalyx Micheli
Holocalyx balansae Micheli
J.M. Silva & E. Barbosa 5040
23.1±0.50 17.5-27.5 17.8±0.24 15.0-20.0 18.9±0.30 15.0-21.2 1.29 17.6x1.9 4.2x6.8 0.9 0.9
(HUEFS)
J.M. Silva 3027 (HUEFS) 22.2±0.20 20.0-23.8 16.8±0.22 15.0-17.5 17.1±0.27 15.0-20.0 1.35 16.8x2.2 4.6x8.0 0.5 0.5
M.V. Ferrari Tomé 1052
23.8±0.22 22.5-25.0 17.5±0.18 15.0-20.0 18.6±0.22 17.5-20.0 1.36 18.0x1.8 4.2x6.9 0.6 0.6
(HUEFS)
Uribea Dugand & Romero
Uribea tamarindoides
Dugand & Romero
N. A. Zamora Villalobos
25.6±0.29 22.5-27.5 23.6±0.23 22.5-25.0 23.7±0.25 22.5-25.0 1.08 18.1x2.4 5.5x9.5 1.0 0.7
1588 (CR)
H. David 5869 (HUA) 24.7±0.16 22.5-26.2 22.4±0.15 20.0-25.0 22.8±0.17 21.2-25.0 1.10 18.8x2.4 4.8x10.3 0.8 0.8
R. Romero-Castañeda
25.0±0.31 22.5-27.5 21.4±0.23 20.0-22.5 21.7±0.23 20.0-22.5 1.17 17.6x1.8- 5.7x7.1 0.9 0.9
8519 (COL)
Note: PD= Polar diameter; ED= Equatorial diameter; EDp= Equatorial diameter in polar view; x= Arithmetic mean; Sx= Standard
deviation of the mean; P/E= Polar diameter-Equatorial diameter ratio; Ecto= Length x Width of the ectoaperture; Endo= Length x
Width of the endoaperture; Sex= sexine; Nex= nexine; measurements in μm and indices in absolute numbers.


Discussion Under SEM, the exine of the pollen grains of

Harleyodendron is perforate-microechinate, which coincides
with the description presented by Skvarla & Ferguson (1988),
Pollen morphology and taxonomy and it is different from that reported by Cowan (1979),
who described the exine as finely reticulate with numerous
Our results regarding the pollen morphology of the rounded projections on the murus. Skvarla & Ferguson
analyzed taxa are supported by extensive literature (Cowan (1988) also described the exine of pollen grains of Holocalyx
1979; Ferguson & Skvarla 1981; Skvarla & Ferguson 1988; as sparsely scrobiculate/fossulate (scrobiculate=punctate
Ferguson & Schrire 1994; Ferguson et al. 1994). Concerning in Punt et al. 2007), whereas Ferguson et al. (1994)
the apertural type, Skvarla & Ferguson (1988) described characterized the pollen grains of this species as foveolate
Harleyodendron and Holocalyx as showing a lolongate and slightly perforate. The specimens included in this
study presented exine ornamentation with perforations
endoaperture. However, Ferguson & Skvarla (1991) reported
of different sizes. Regarding the exine of Uribea, our results
that there was confusion regarding the endoapertures
coincide with those published by Ferguson et al. (1994).
and clarified that the pollen grains of Harleyodendron
The pollen grains of these species can be differentiated
and Holocalyx present lalongate endoapertures. Our from each other under LM in terms of size, shape, and
results also reported a lalongate endoaperture, which is sexine/nexine ratio. Harleyodendron has small to medium
sometimes difficult to visualize since the constriction of the pollen grains, shapes ranging from prolate-spheroidal to
ectoaperture usually is positioned upon the endoaperture. subprolate, and a finely microreticulate exine, Holocalyx
Some differences were observed between the results has small pollen grains, shapes ranging from subprolate
found here and data from the literature. Regarding the to prolate, and exine ranging from finely microreticulate
apertural membrane, Skvarla & Ferguson (1988) described to reticulate, and Uribea shows medium pollen grains with
a finely granulate apertural membrane in Holocalyx, while prolate-spheroidal shape, microreticulate exine, and sexine
a psilate apertural membrane is reported in this research. thicker than nexine.

Acta Botanica Brasilica, 2023, 37: e20220208 5

 Débora Cavalcante de Oliveira, Luis Carlos Casas Restrepo, Márcio Ferreira dos Santos,
Luciano Paganucci de Queiroz and Francisco de Assis Ribeiro dos Santos

Under SEM analysis, the difference in pollen morphology Regarding Harleyodendron unifoliolatum, Cowan (1979)
among these species is remarkable when their exine stated that this species may be pollinated by small insects
ornamentation is compared. While in Holocalyx was found that are attracted to its whitish, fragrant flowers, or that
a less complex exine ornamentation without supratectal they are self-fertile. However, this species presents a unique
structures, being perforate, the other genera showed a and unusual floral morphology among the papilionoid
more specialized exine which were classified as perforate- legumes, as they are radially symmetrical with the five fleshy
microechinate in Harleyodendron and as having an irregular petals becoming reflexed backward its open flowers, and the
relief and granular projections on the perforate tectum with ten big and rigid anthers are kept coherent by intermixed
slightly rugulate areas in Uribea. long hairs making a dome an apical opening like a pore
Morphological characteristics such as shape, apertures, (Fig. 1A). The anthers dehisce through two longitudinal
and perforate exine with heterogeneous perforations somewhat introrse slits making pollen available within the
exhibited by Holocalyx coincide with those that are commonly dome. Unfortunately, there is no empirical data that could
found in Leguminosae since the family and most genera of suggest what flower visitors could act as pollinators of this
the Papilionoideae subfamily present monad, tricolporate, interesting plant. Pollen grains with echinate exine have
and finely reticulate pollen grains (Erdtman 1952; Guinet been linked to pollination by animals (Wodehouse 1935;
1981; Ferguson & Skvarla 1981). Hesse 2000; Tanaka et al. 2004), an idea that is shared by
The exine ornamentation here observed in Holocalyx
Ferguson & Skvarla (1982), who report that species in the
has also been reported by Skvarla & Ferguson (1988) for
genera Ambrosia L. and Artemisia L. (Asteraceae) generally
Exostyles glabra Vogel and for some species of Zollernia, for
have psilate pollen grains and are wind-pollinated, while
which Ferguson & Schrire (1994) also reported the same
other genera with ornate pollen grains (commonly echinate)
exine ornamentation. As well as Holocalyx, these taxa are
are pollinated by insects.
included in the Exostyleae clade (Mansano et al. 2002;
Jones & Jones (2001) reported that butterflies and
Cardoso et al. 2012, 2013).
The exine ornamentation with the presence of moths pollinate species that usually have reticulate, striate,
microspines observed in Harleyodendron unifoliolatum as and echinate pollen grains. Butterfly-pollinated flowers
well as the exine with granular projections on the perforate usually display showy colors such as red, yellow, blue, and
tectum shown in Uribea tamarindoides are uncommon exine orange, are erect, and exhibit a landing platform, nectaries
ornamentations among the species of Leguminosae (Skvarla hid in spurs or narrow tubes, and simple nectar guides. On
& Ferguson 1988; Ferguson et al. 1994). Nonetheless, these the other hand, moth-pollinated flowers are white, light
traits have been reported in other species of the Exostyleae pink or light yellow, zygomorphic, pendulous or horizontal
clade such as Exostyles venusta Schott and Lecointea amazonica without a landing platform, with nectaries very hidden in


Ducke (Skvarla & Ferguson 1988; Ferguson & Schrire 1994), long tubes or spurs, and without nectar guides (Jones &
and other genera of the Papilionoideae subfamily such as Jones 2001; Rech et al. 2014).
Macrotyloma (Wight & Arn.) Verdc. (Ferguson 1981). As Harleyodendron unifoliolatum has flowers with large
The variation in exine ornamentation among related and rigid anthers and perforate-microechinate pollen
genera of the clade Exostyleae have raised the question grains, it could be assumed that this species is pollinated
about whether all genera of the clade show variation in by large bees. Nonetheless, because of the distinct floral
exine ornamentation and which is included in this clade morphology, as well as the exine ornamentation, and the
share the same type of ornamentation. lack of information about the pollinator, further research
focused on this species is needed to elucidate the pollination
Implications of pollen morphology on pollination of H. unifoliolatum.
Among the species included in this study, Holocalyx Finally, information regarding the pollination of Uribea
balansae is pollinated by bees and other small insects tamarindoides was not found. Its flowers are zygomorphic,
(Carvalho 2003), its flowers are small (2–3 x 0.5–0.9 mm), purple or light purple with five petals, the adaxial being
greenish, actinomorphic, with five petals, ten stamens differentiated into a banner and ten stamens (Dugand
(Mansano & Viana-Filho 2010) and their pollen grains are 1962). Although there is no information about the U.
perforate. These characteristics were associated with the tamarindoides pollinator, it can be suggested that this
pollination by small insects by Ferguson (1984). This author species is pollinated by bees, taking into account that the
reported Templetonia egena Benth. and Camoensia brevicalyx specialized bilateral flowers of Papilionoideae facilitate
Benth. (Papilionoideae), whose pollen grains show a finely bee-flower interaction, as they have a standard petal, which
perforate exine and are pollinated by insects. Additionally, is larger and more external, serving as an attraction, two
several plant species with microreticulate pollen grains have wings that act as a landing area for visiting insects and
been reported as pollinated by different species of bees a keel that surrounds the androecium and gynoecium
(Braga et al. 2012; Bastos et al. 2020; 2021; Dias et al. 2022). (Lewis et al. 2005).

6 Acta Botanica Brasilica, 2023, 37: e20220208

 Pollen morphology of the early branching papilionoid legume
genera Harleyodendron, Holocalyx and Uribea

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