Flora 240 (2018) 48–57

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Flora
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Seed morphology of Ruellia L. (Acanthaceae) from the Southeastern T

Brazilian Atlantic rain forest: Taxonomic, phylogenetic, and ecological
aspects
⁎,1
Igor Henrique Freitas Azevedo , Denise Monte Braz
Departamento de Botânica, Instituto de Ciências Biológicas e da Saúde, Universidade Federal Rural do Rio de Janeiro, BR-465, km 7, Seropédica, RJ, CEP: 23890-000,
Brazil

A R T I C L E I N F O A B S T R A C T

Edited by Louis Ronse De Craene Considering the important, but sparse, data available concerning the seed morphology of Acanthaceae and its
Keywords: species-rich genus Ruellia, we analyzed the diaspores of five Ruellia species from the southeastern Brazilian
Dispersal Atlantic Rain Forest using stereomicroscopy, light microscopy, and scanning electron microscopy. The seeds
Hygroscopic trichomes were characterized as discoid, 1.2–5.2 mm in diameter, having a seed coat with hygroscopic-mucilaginous tri-
Mucilage chomes, these generally with annular secondary wall thickenings. R. blechum shows a unique seed morphology
Ruellieae for the genus, as was already likewise established for its pollen grains. Seed morphology allied to fruit mor-
Systematics phology could aid in characterizing the infrageneric clades of that genus, although future studies must include
larger numbers of taxa. The morphology observed, allied to relief, fluvial and climatic aspects of the study area,
highlight the roles of secondary hydrochory and epizoochory in seed dispersal within the genus, which is
supported by the presence of mucilaginous trichomes.

1. Introduction
Acanthaceae Juss. comprises 190 genera and over 4000 species
globally (McDade et al., 2008; Daniel and McDade, 2014; Stevens,
2017), with 40 genera and 448 species known from Brazil (BFG, 2015;
Profice et al., 2015). A capsular fruit with explosive dehiscence is an
important synapomorphy of the family (McDade et al., 2012). In
Acanthoideae, the largest subfamily of Acanthaceae, the capsular fruits
are characterized by the presence of hooked retinacula (Lindau, 1895;
Scotland and Vollensen, 2000; McDade et al., 2008) that aid in
launching the lenticular seeds during fruit explosion (Witztum and
Schulgasser, 1995).
Hygroscopic-mucilaginous trichomes on the seeds are consistent
among Ruellieae species within the Acanthoideae, and are considered a
synapomorphy of that tribe (Tripp et al., 2013). This group is re-
presented in Brazil by six genera and 112 species (BFG, 2015; Profice
et al., 2015), equivalent to almost 25% of the Acanthaceae species
found in that country.
Ruellia L. is the second largest genus of the family Acanthaceae, and
the largest in the tribe Ruellieae, with approximately 350 species
globally (Tripp et al., 2013) and 85 in Brazil (BFG, 2015; Profice et al.,
2015). Its species are herbs or shrubs (rarely vines) occurring in both
tropical and temperate regions of the Old World (OW) and New World
(NW), with weakly to strongly zygomorphic flowers and four stamens
with basally unappendaged and bithecous anthers (Tripp, 2007). The
only known morphological synapomorphy of the genus is its pollen,
termed “wabenpollen” by Lindau (1895), being characterized by a
coarsely reticulate exine as well as triporate and spheroidal pollen
grains (Tripp, 2007).
Ezcurra (1993) revised Ruellia for southern South America and in-
dicated seven informal taxonomic groups based on their inflorescences
and fruit morphologies. Tripp (2007) presented a global phylogeny of
the genus based on molecular data that established three large groups
and six small ones for the NW that has been improved and is currently
supported (Tripp and Manos, 2008; Tripp et al., 2009; Tripp, 2010;
Tripp and McDade, 2012, 2013). Despite the high diversity of Ruellia,
taxonomic and systematic studies of the genus in Brazil have been
limited to local floras and a single revision (Ezcurra, 1993), as well as
two unpublished regional revisions (Silva, 2011; Pessôa, 2012).
Morphological and molecular studies in the last two decades have
consolidated a consistent classification of Acanthaceae and delimitated
the largest infrafamiliar groups (McDade et al., 2000a,b; Scotland and
Vollensen, 2000; McDade et al., 2005, 2008; Tripp et al., 2013, among
others). Some studies including morphological traits of seeds have

⁎
Corresponding author.
E-mail address: igorhfazevedo@ufrrj.br (I.H.F. Azevedo).
1
Scholarship holder of the Programa de Apoio à Iniciação Científica (PROIC/PROPG-UFRRJ).

https://doi.org/10.1016/j.flora.2017.12.011
Received 6 October 2017; Received in revised form 20 December 2017; Accepted 22 December 2017
Available online 28 December 2017
0367-2530/ © 2017 Elsevier GmbH. All rights reserved.
I.H.F. Azevedo, D.M. Braz Flora 240 (2018) 48–57

Table 1 2.3. Morphological analysis

Ruellia species included in the present study, their voucher specimens, and infrageneric
classifications.
Laboratory work was conducted at the Botany Department of the
Species Voucher Infrageneric classification Biological Sciences and Health Institute at the Federal Rural University
specimens of Rio de Janeiro (ICBS/UFRRJ). The plants were collected with re-
Ezcurra (1993) Tripp (2007) productive structures, herborized and then incorporated into the RBR
Herbarium (at the same department). We collected seeds directly from
Ruellia blechum L. D. Braz 271 Not included (genus “Blechum” clade
Blechum) plants in the field and from exsiccatae, selecting those that were as
Ruellia brevifolia I. Azevedo 81 Group Physiruellia “Physiruellia” clade mature as possible. We also collected information about the plants'
(Pohl) C. and D. Braz habitats and noted additional morphological features in the field.
Ezcurra The morphological analyses were performed using observations,
Ruellia simplex C. I. Azevedo 80 Group Ruellia “Euruellia” clade
photography, and measurement of the seeds under a stereomicroscope,
Wright and D. Braz
Ruellia solitaria D. Braz 336 Group “Ruellia devosiana” light microscope (LM), and scanning electron microscope (SEM). A
Vell. Dipteracanthus cladea stereomicroscope was used to measure the lengths (L) and widths (W)
Ruellia sp. D. Braz 171 Not included Not included of the seeds (n = 10), and those measurements were subsequently used
a
to calculate arithmetic mean and standard error (x + s x ), standard de-
following Tripp et al. (unpublished results).
viation (s), the 95% confidence interval (C.I.), and coefficient of var-
iation (C.V.). We observed the isolated integuments of the seeds under a
revealed important taxonomic characters for some groups within the
LM with temporary slides. The SEM at the ICBS/UFRRJ (Hitachi
family (i.e. Graham, 1988; Lester and Ezcurra, 1991; Balkwill and
Tabletop Microscope, Model TM 1000; magnification x10,000) was
Campbell-Young, 1999), and studies with this approach have increased
used to visualize the entire seeds and details of their surfaces (without
recently (Daniel and McDade, 2014; Kiel and McDade, 2014; Al-Hakimi
the necessity of critical point drying or metallization). We examined the
et al., 2015, among others), including Ruellia (Greuter and Rankin
seeds for the presence of hygroscopic trichomes and mucilage secretion
Rodríguez, 2010; Tripp et al., 2013; Al-Hakimi and Latiff, 2015).
using water. The seed coat microstructure was described and classified
We analyzed the seed morphology of five Ruellia species from the
following Barthlott (1981) and Payne (1978).
Atlantic Rain Forest of Rio de Janeiro State, Brazil, to contribute to our
Descriptions of fruit shape and number of ovules follow Ezcurra
knowledge of the Acanthaceae as a whole, as well as the phylogeny and
(1993) and Tripp (2007), adapted when necessary.
ecology of the genus Ruellia.

2. Materials and methods
2.1. Sampling
The species studied are listed in Table 1. The taxon designated as
Ruellia sp. is a new species for the genus and is currently being de-
scribed by the authors and other collaborators.
2.2. Study area
The Acanthaceae specimens were collected in the Parque Natural
Municipal do Curió, located in the municipality of Paracambi, Rio de
Janeiro State, Brazil. The park consists of an approximately 1100 ha
fragment (Fraga et al., 2012) (22°34′ S to 22°36′ S x 43°42′ W to 43°41′
W) of Atlantic Rain Forest (Cysneiros et al., 2015) in a rugged landscape
(from 100 m to 690 m a.s.l.) that experiences a mild subtropical to hot
and humid tropical climate, with a mean annual temperature of 23.4 °C
(Fraga et al., 2012). The Park was designated a protected area largely
because of its many small rivers and some seasonal wetlands, as part of
the Guandu River basin (Cysneiros et al., 2015).
3. Results
3.1. Ruellia
Seeds discoid (laterally flattened), with orbicular to elliptical out-
lines, 1.2–5.2 mm long, asymmetric base with distinct hilum, apex
generally rounded, mucilaginous-hygroscopic and unicellular tri-
chomes present throughout the coat (total distribution) or restricted to
the seed margins (marginal distribution), and generally with annular
secondary wall thickenings.
On the seeds with total distribution of trichomes, each one of the
cells of the seed surface is differentiated into a trichome.
The morphological characters observed are summarized in Table 2,
and the measurements presented in Table 3.
3.1.1. Ruellia blechum (Fig. 1)
Seeds x = 1.76 × 1.52 mm, orbicular to elliptical in outline, base
truncate to cordate, apex rounded, surface sparsely verrucate
(Fig. 1A–C). Trichomes unicellular, lageniform, hygroscopic, mucilagi-
nous, restricted to the margins (Fig. 1D–E); warts sparse in the mid-
region (Fig. 1E–F). Cells of the mid-region elongated, 5–6-gonal out-
lines; anticlinal walls straight to curved, channeled; outer periclinal

Table 2
Morphological characters of the fruits and seeds of the Ruellia species studied.

R. blechum R. brevifolia R. simplex R. solitaria Ruellia sp.

Fruit Outline Short-obovoid Clavate Elliptical Clavate Long-obovoid

Number of ovules 12–16 8–12 16–24 12–16 6–8
Seed outline Orbicular to elliptical Elliptical to ovate Orbicular Elliptical to ovate Orbicular
Trichomes Shape Lageniform Attenuated Cylindrical Attenuated Cylindrical
Distribution Marginal Marginal Total Marginal Total
Seed outline Orbicular to elliptical Elliptical to ovate Orbicular Elliptical to ovate Orbicular
Seed coat texture Warty Striated Lanate Striated Lanate
Cells of the mid region Outline Elongated, 5–6-gonal Elongated, 4-gonal Isodiametric, 4–5-gonal Elongated, fusiform, 6- Isodiametric, 4–6-gonal
gonal
Anticlinal wall Straight to curved, Straight, raised Straight, raised Straight, raised Straight, raised
channeled
Outer periclinal wall Plane to concave Plane Trichome Plane to concave Trichome

49
I.H.F. Azevedo, D.M. Braz Flora 240 (2018) 48–57

Table 3
Diameter measurements of Ruellia seeds (n = 10).

Ruellia blechum Ruellia brevifolia Ruellia simplex Ruellia solitaria Ruellia sp.

Length (L) Variation range 1.53–1.89 4.05–5.22 2.06–2.47 2.36–3.81 3.35–4.35

1.76 ± 0.03 4.78 ± 0.08 2.27 ± 0.02 3.08 ± 0.08 3.79 ± 0.07
x + sx (mm)
C.I. 95% (mm) 1.71–1.81 4.61–4.95 2.23–2.32 2.91–3.25 3.65–3.93

Width (W) Variation range 1.22–1.62 3.27–4.02 1.97–2.37 1.65–2.93 3.12–3.97

1.52 ± 0.02 3.65 ± 0.05 2.12 ± 0.02 2.5 ± 0.08 3.55 ± 0.04
x + sx (mm)
C.I. 95% (mm) 1.47–1.56 3.55–3.75 2.08–2.17 2.34–2.66 3.45–3.64

L/W 1.16 1.31 1.07 1.23 1.07

x + s x - average and average standard deviation; C.I. – confidence interval.

Fig. 1. Seeds of Ruellia blechum as viewed under a

stereomicroscope (A–B), light microscope (C–D), and
by SEM (E–F). A. General aspect of the dry seed, with
hygroscopic trichomes restricted to the margins. B.
Seed in contact with water, hygroscopic activity of
the trichomes and mucilage. C. General aspect of the
seed, with hygroscopic trichomes restricted to the
margins, hygroscopic activity of the trichomes and
mucilage (lines radiating from the edges of the seed).
D. Lageniform trichomes on the margins. E.
Lageniform trichomes on the margins, which cannot
be characterized under SEM due to their dehydra-
tion. F. A wart on the mid-region of the seed. (Braz
271, RBR). Bars: A: 300 μm; B, C: 500 μm; D: 50 μm;
E: 100 μm; F: 20 μm.

50
I.H.F. Azevedo, D.M. Braz
walls planar to slightly concave (Fig. 1F).
3.1.2. Ruellia brevifolia (Fig. 2)
Seeds x = 4.78 × 3.65 mm, elliptical to ovate in outline, base
truncate, apex rounded, surface striate (Fig. 2A–B). Trichomes uni-
cellular, attenuated, hygroscopic, mucilaginous, restricted to the mar-
gins, with annular secondary wall thickenings (Fig. 2C–E). Cells of the
mid-region with elongated, 4-gonal outlines; anticlinal walls straight,
raised; outer periclinal walls planar (Fig. 2F).
3.1.3. Ruellia simplex (Fig. 3)
Seeds x = 2.27 × 2.12 mm, orbicular in outline, base truncate to
cordate, apex rounded, surface lanate (Fig. 3A–C). Trichomes uni-
cellular, cylindrical, hygroscopic, mucilaginous, present throughout the
51
Flora 240 (2018) 48–57
Fig. 2. Seeds of Ruellia brevifolia as viewed under a
stereomicroscope (A–B), light microscopy (C), and
by SEM (D–F). A. General aspect of the seed, with
hygroscopic trichomes (white) on the margins. B.
Seed in contact with water, and hygroscopic activity
of the trichomes. C. Hygroscopic trichomes with
secondary wall thickenings, clearly annular. D. Seed
margin, with clear distinctions between glabrous and
lanate regions. E. Hygroscopic trichomes densely
packed on the margins, with annular thickenings. F.
Cells of the mid-region, with 4-gonal outlines and
raised and straight anticlinal walls. (Azevedo 81 &
Braz, RBR). Bars: A, B: 1 mm; C: 100 μm; D: 80 μm; E:
20 μm; F: 100 μm.
coat, with annular secondary wall thickenings (Fig. 3C–E). Trichome
cells of the mid-region with isodiametric, 4–5-gonal outlines; anticlinal
walls straight, raised; outer periclinal walls differentiated into tri-
chome.
3.1.4. Ruellia solitaria (Fig. 4)
Seeds x = 3.08 × 2.5 mm, elliptical to ovate in outline, base cor-
date, apex rounded to obtuse, surface striated (Fig. 4A–B). Trichomes
unicellular, attenuated, hygroscopic, mucilaginous, with annular sec-
ondary wall thickenings (Fig. 4C–E), restricted to the margins. Cells of
the mid-region with elongated, fusiform, 5–6-gonal outlines; anticlinal
walls straight, raised; outer periclinal walls planar to slightly concave;
inner periclinal walls micropapillate (Fig. 4D).
I.H.F. Azevedo, D.M. Braz
3.1.5. Ruellia sp. (Fig. 5)
Seeds non-ciliate, x = 3.79 × 3.55 mm, orbicular in outline, base
cordate, apex rounded, surface lanate (Fig. 5A–C). Trichomes uni-
cellular, cylindrical, hygroscopic, mucilaginous, present throughout the
coat, with annular secondary wall thickenings (Fig. 5D–E). Trichome
cells of the mid-region (trichomes) with isodiametric, 4–6-gonal out-
lines, anticlinal walls straight, raised; outer periclinal walls differ-
entiated into trichome.
4. Discussion
4.1. Taxonomic and phylogenetic aspects
The seeds of Ruellia are described as flat, more or less orbicular in
52
Flora 240 (2018) 48–57
Fig. 3. Seeds of Ruellia simplex as viewed under a
stereomicroscope (A–B), light microscope (D), and
by SEM (C, E). A. General aspect of the dry seed. B.
Seed in contact with water, and hygroscopic activity
of the trichomes. C. General aspect of the seed and its
lanate surface. D. Hygroscopic trichomes with sec-
ondary wall thickenings, clearly annular. E.
Hygroscopic trichomes, with annular thickenings.
(Azevedo 80 and Braz, RBR). Bars: A: 500 μm; B:
1 mm; C: 500 μm; D: 50 μm; E: 20 μm.
outline, with a slight notch at the end of the chalazal region, and more
or less covered with hygroscopic mucilaginous trichomes with annular
or spiral thickenings of their walls (Ezcurra, 1993). These characters are
consistent with the observations of our study, except for the seeds of R.
blechum. We observed the hygroscopic mucilaginous trichomes in all
the species studied, considered by Tripp et al. (2013) as one of the four
morphological synapomorphies for the tribe Ruellieae. Secondary
thickenings of their walls were likewise observed in the species studied
(except for R. blechum), which were clearly and consistently annular
when observed under a LM (Fig. 2C, 3D, 4C and 5D). Al-Hakimi and
Latiff (2015), sampling five species of Ruellia from Yemen, observed
that the hygroscopic trichomes lacked secondary thickenings, which
currently appears to constitute the main difference between OW and
NW Ruellia seeds. Seed trichomes with secondary thickenings have been
I.H.F. Azevedo, D.M. Braz
observed in other genera within Ruellieae, however, in: Phaulopsis
Willd., Dyschoriste Nees, Hygrophila R. Br., among others (see Greuter
and Rankin Rodríguez, 2010; Al-Hakimi and Latiff, 2015), which in-
dicates the need for more investigations in that tribe and others in
Acanthaceae.
The studied species (Table 1) have been placed in four infrageneric
clades (“Physiruellia”, “Blechum”, “Euruellia” and “Ruellia devosiana”
clades) (Tripp 2007; Tripp et al., unpublished results), and Ruellia sp.
has not yet been included in any molecular phylogeny.
The group “Physiruellia” was delimited by Ezcurra (1993) based on
inflorescence patterns, and capsules clavate, these narrowly ob-
lanceolate in contour, hollow in the upper 2/3 of their total length,
solid and stipitate at the base and containing eight to 14 seeds. Tripp
(2007) characterized “Physiruellia” fruits as thin-walled clavate
53
Flora 240 (2018) 48–57
Fig. 4. Seeds of Ruellia solitaria as viewed under a
stereomicroscope (A–B), light microscope (C), and by
SEM (D–E). A. General aspect of the dry seed. B. Seed
in contact with water, and hygroscopic activity of the
trichomes on the margins (white). C. Hygroscopic
trichomes with secondary wall thickenings, clearly
annular. D. Seed margin, with clear distinctions be-
tween the glabrous and lanate regions. E.
Hygroscopic trichomes along the margins, with an-
nular thickenings of the walls. (Braz 336, RBR). Bars:
A, B: 1 mm; C: 50 μm; D: 100 μm; E: 20 μm.
capsules containing eight to 14 ovules, with seeds bearing hygroscopic
trichomes restricted to the margins. Ruellia brevifolia has been con-
sistently included in this group by both authors cited above, and its
clavate fruits with 8–12 ovules and seeds with marginal trichomes fit
well. Ruellia blechum is placed in the “Blechum” clade, which comprises
species previously established under the genus Blechum plus some
Ruellia species (Tripp, 2007). In addition to their distinct pollen grains
(Tripp, 2007), the species shows a unique seed morphology for the
genus: areas not covered by hygroscopic trichomes have sparse warts
(Fig. 1E–F); their hygroscopic trichomes not only lack secondary
thickenings, but also have a completely distinct lageniform shape
(“gourd-shaped”, Fig. 1D), as described and illustrated by Kippist
(1842); their fruits have “fracturing placentae” (Tripp et al., 2009)
(Fig. 6), although this is homoplasic in the genus (Tripp, 2007). Thus,
I.H.F. Azevedo, D.M. Braz
considering the presence of annular thickenings on the seed trichomes
as a synapomorphy of NW Ruellia, it seems to have happened a sec-
ondary loss of this character in R. blechum. Ezcurra’s (1993) group
Ruellia corresponds to Tripp’s (2007) “Euruellia” clade. Both classifi-
cations characterized the taxon based on the morphology of the in-
florescence and its elliptic capsules with 14–28 ovules. Tripp (2007)
also used the distribution of hygroscopic trichomes on the entire seed
surface to characterize “Euruellia”. This group includes Ruellia simplex,
with that typical fruit and seed morphology.
Ruellia solitaria was included in Ezcurra’s (1993) group Dipter-
acanthus, due to the morphology of its inflorescence and thick-walled
oblong fruits with their small, solid base and 6–12 seeds. That group
was not supported, however, in Tripp’s (2007) phylogeny, and only
recently (Tripp et al., unpublished results) R. solitaria has been included
54
Flora 240 (2018) 48–57
Fig. 5. Seeds of Ruellia sp. as viewed under a ste-
reomicroscope (A–B), a light microscope (D), and by
SEM (C, E). A. General aspect of the dry seed. B. Seed
in contact with water, and hygroscopic activity of the
trichomes. C. General aspect of the seed, its lanate
surface and hooked retinaculum at the base. D.
Hygroscopic trichomes with secondary wall thick-
enings, clearly annular. E. Hygroscopic trichomes
with secondary annular wall thickenings. (Braz 171,
RBR). Bars: A–C: 1 mm; D: 100 μm; E: 20 μm.
in a molecular phylogeny. Tripp et al. (unpublished results) has placed
this species in a small clade closely related to “Physiruellia” (see “R.
devosiana” clade in Tripp and McDade (2013)), together with R. affinis
Lindau, R. makoyana Closon and R. devosiana Jacob-Makoy ex
E.Morren. Considering its clavate fruits (considered here) with 12
ovules and seeds with marginal trichomes (Fig. 6), this species would
appear to belong to the “Physiruellia” clade, along with R. brevifolia; its
sessile and solitary flowers (as well as the other species of the “R. de-
vosiana” clade) contrast, however, with the typical compound and
multiflowered cymes of “Physiruellia”. The seeds of R. solitaria and R.
brevifolia can only, in fact, be differentiated in terms of the secondary
sculpturing of their seed coats: 4-gonal cells in the latter, and 5–6-gonal
in the former.
Another recently discovered and unclassified species is Ruellia sp. Its
I.H.F. Azevedo, D.M. Braz
Fig. 6. Phylogenetic arrangement of Ruellia, infrageneric groups, and the studied species with their fruits and seeds (cladogram constructed following results presented in Tripp (2007),
Tripp and McDade (2013) and Tripp et al. [unpublished results]). (Illustrated from plants in the field).
combination of compound cymes with pedicellate flowers and long-
obovoid fruits, with up to eight ovules and seeds with total distribution
of trichomes (Fig. 6), appears very similar to the species treated by
Tripp (2007) in the "R. inflata" clade (e.g., R. elegans Poir., R. exserta
Wassh. & J.R.I. Wood, and R. subsessilis Lindau). Therefore, although
that clade does not yet have a clear morphological characterization,
Ruellia sp. fits better in it than in any other group. Highlighting their
relative phylogenetic proximity (see the “Euruellia” and "R. inflata"
clades in Tripp and McDade (2013)), Ruellia sp. and R. simplex seeds are
highly similar, differing basically only in terms of their average sizes
(Fig. 6). Fruit morphology, on the other hand, can readily separate
them: long-obovoid capsules with up to eight ovules in Ruellia sp.,
versus long elliptical fruits with approximately 18 ovules in R. simplex.
According to the updated phylogeny and major clades of the genus
(Tripp, 2007; Tripp and McDade, 2013), New World Ruellia can be
divided into two major lineages: one includes the clades of “Blechum”,
“Physiruellia” and "R. devosiana" (thus including R. blechum, R. brevi-
folia, and R. solitaria – species with seed trichomes marginally dis-
tributed); the second lineage includes the clades of “Euruellia” and "R.
55
Flora 240 (2018) 48–57
inflata" (with R. simplex and Ruellia sp. – species with seed trichomes
totally distributed) (Fig. 6). The trichome distributions of the seeds
should therefore be studied in other groups of the genus, especially in
the highly diverse “Ebracteolati”, to shed light on any evolutionary
modifications of their patterns, which could reveal possible synapo-
morphies.
4.2. Ecological aspects
As dispersal units, seeds are incapable of controlling their water
losses through transpiration, but seed coat ornamentation increases
their surface areas from two to 20 times, which may be the main means
to control the internal temperature of the seeds (Barthlott, 1981). The
trichomes of Ruellia also secrete mucilage, as was analyzed by Schnepf
and Deichgräber (1983), a substance that is very efficient at water re-
tention and probably also aids in seed anchorage (see discussions below
concerning dispersal), thus both aiding seed protection and germination
(Witztum et al., 1969; Lester and Ezcurra, 1991; Western, 2012;
Stevens, 2017). Some authors also associate mucilage with possible
I.H.F. Azevedo, D.M. Braz
Fig. 7. Hypothetical associations between fruit and seed characters of Ruellia and their
possible advantages for the plants.
secondary epizoochory (Lester and Ezcurra, 1991; Ezcurra, 1993; Tripp
and McDade, 2014) or hydrochory (Greuter and Rankin Rodríguez,
2010).
An important characteristic of the entire subfamily Acanthoideae is
the presence of fruits with retinacula, which aid in autochoric dispersal
through explosive dehiscence of the fruits (Lindau, 1895). The strong
lateral flattening observed in the seeds of the Ruellia species studied
(and in this whole genus) support that type of dispersal, as it increases
their aerodynamics (Witztum and Schulgasser, 1995). The explosive
dehiscence of Ruellia fruits was demonstrated by Witztum and
Schulgasser (1995), and is responsible for short-distance dispersal.
Long-distance dispersal in Acanthaceae is quite enigmatic, however, as
was briefly discussed by McDade et al. (2012).
We observed evidence of secondary hydrochory in Ruellia that could
favor dispersal over longer distances. The species in the study area (and
other genera of Acanthaceae) often occur very close to streams. The
discoid shape of the seeds, allied to their hygroscopic trichomes and
mucilage secretion, endows them with buoyancy. Those morphological
features have previously been associated with water dispersal by Van
der Pijl (1969), Boesewinkel and Bouman (1995), and Greuter and
Rankin Rodríguez (2010). Hydrochory is strongly associated with en-
vironmental parameters (Van der Pijl, 1969; Fenner and Thompson,
2005; Western, 2012), and both the Curió Park and the Atlantic Rain
Forest experience high seasonal rainfalls, have rugged landscapes, and
abundant streams (Fraga et al., 2012) − scenarios under which hy-
drochory could have an important role in medium and long-distance
dispersal. The mucilaginous trichomes with annular thickenings could
serve to anchor the floating seeds to soil, rocks, and other surfaces,
including animals, as indicated by Gessner and Hammer (1962), Van
der Pijl (1969), Ezcurra (1993), Koch et al. (2008), among others.
Epizoochory can also benefit from the explosive dehiscence of the fruits
(Van der Pijl, 1969).
It is important to keep in mind that the dispersal of Ruellia (and
Acanthaceae) is not limited to a single mechanism in the Brazilian
Atlantic Rain Forest (or in any other type of natural vegetation) and the
different morphological characters promote advantages for the plants
under different environmental conditions. Van der Pijl (1969) called
this combination of different kinds of dispersal “polychory”. Fruit and
seed characters of Ruellia therefore appear to influence more than one
function (Fig. 7), which should be tested in further studies. The fruit
retinacula and explosive dehiscence can promote autochory and pos-
sibly epizoochory; the lateral flattening of the seed promotes its aero-
dynamics and buoyancy; the hygroscopic trichomes can facilitate seed
aerodynamics (as they are constricted when dry) and buoyancy, and the
association of mucilage and annular thickenings may facilitate an-
choring the seeds to solid substrates or animals; the mucilage itself
56
Flora 240 (2018) 48–57
helps to physically protect the seeds (against water loss, predation,
external enzymes) and promotes buoyancy and germination.
5. Conclusions
Seed and fruit morphologies were found to be important tools for
assigning Ruellia species to infrageneric clades, which highlights their
potential taxonomic importance of Acanthaceae. Further studies with
wider sampling could provide more criteria for delimiting groups and
promoting a better understanding of the evolution of seed character-
istics within the genus. There is still much to be discovered concerning
the dispersal mechanisms of Ruellia (and Acanthaceae) seeds over
medium and long-distances, but “polychory”, which includes auto-
chory, hydrochory, and/or epizoochory, seems highly probable.
Funding
This work was supported by the Programa de Apoio à Iniciação
Científica (PROIC/PROPG-UFRRJ) of the Universidade Federal Rural do
Rio de Janeiro, through a scholarship awarded to the first author, and by
the Associação Pró-Gestão das Águas da Bacia Hidrográfica do Rio Paraíba
do Sul (AGEVAP, Comitê Guandu) [n° 014/2013] through their fi-
nancial assistance to the study.
Acknowledgements
We would like to thank the Secretaria do Meio Ambiente e
Desenvolvimento Sustentável of Paracambi City for their support in the
study area; Dr. Gerson Araújo and José Antônio de Oliveira for their
assistance in the SEM analyses; Dr. Roy Funch for his essential and
excellent English revision; and the manuscript reviewers for their va-
luable contributions.
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