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Leaf anatomy in Allagoptera (Arecaceae)

Article in Botanical Journal of the Linnean Society · May 2016

DOI: 10.1111/boj.12439

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Botanical Journal of the Linnean Society, 2016. With 6 figures

Leaf anatomy in Allagoptera (Arecaceae)

ANDRE
SILVA PINEDO*, RENATA CORREA
^ MARTINS, REGINA CELIA

DE OLIVEIRA
and SUELI MARIA GOMES
Programa de P
os-Graduacßão em Botânica, Departamento de Botânica, Universidade de Brasília,
C.P. 04.457, Asa Norte, Brasília, Distrito Federal 70919-970, Brasil

Received 18 October 2015; revised 15 April 2016; accepted for publication 19 April 2016

The small genus Allagoptera (Arecaceae) includes six South American species. Their leaves have several
anatomical characters that remain unexplored. We provide a detailed description of the leaf anatomy of
Allagoptera, using 128 characters, and an identification key. Given the gradual size variation in the mesophyll
cells in some species, a new classification of ‘gradual dorsiventral mesophyll’ is proposed here. We report for the
first time ‘subsidiary ledges’ in the stomatal complex of Arecaceae. We propose using ‘bulliform cell’ for the
swelling cells along the midvein in Arecaceae. © 2016 The Linnean Society of London, Botanical Journal of the
Linnean Society, 2016

ADDITIONAL KEYWORDS: mesophyll – monocotyledons – Palmae – stomatal characters –

taxonomy – vascular system.

INTRODUCTION
Dransfield et al. (2005) re-established A. caudescens
Since the classical work of Tomlinson (1961), several (Mart.) Kuntze, which previously belonged to Polyandro-
studies of palm anatomy have been published (Glass- cocos Barb.Rodr. (Rodrigues, 1901), and Martins et al.
man, 1972; Barfod, 1988; Seubert, 1996a, b, 1997, (2015) described A. robusta R.C.Martins & Filg., bring-
1998a, b; Mathew & Bhat, 1997; Rudall et al., 2003; ing to six the number of known Allagoptera species.
Dransfield et al., 2008; Horn et al., 2009). The new- Moraes (1996) included brief anatomical descrip-
est comprehensive treatment of palm anatomy is tions illustrated with schematic drawings, but did
that of Tomlinson, Horn & Fisher (2011). Despite the not show paradermal sections, leaf margins or the
studies of root and leaf anatomy of Arecoideae (Seu- main vascular bundles. Therefore, despite the magni-
bert, 1998a, b; Alvarado & J
auregui, 2011), this sub- tude of that work, there were still some gaps in the
family remains insufficiently studied (Tomlinson knowledge on this genus. A recent study of A. are-
et al., 2011). Attaleinae, one of the main arecoid sub- naria has added many anatomical and histochemical
tribes, is characterized by a thick lamina, with meso- details without, however, applying them to the tax-
phyll and a hypodermis that is well developed and onomy of the genus (Defaveri et al., 2015). Other
an epidermis with a thickened outer wall, particu- anatomical works on Allagoptera have focused on
larly on the adaxial surface. stamen development (Uhl & Moore, 1980) and root
The monophyletic genus Allagoptera Nees anatomy (Seubert, 1998a, b).
(Arecoideae, Attaleinae; Dransfield et al., 2008) has Biometric data could not distinguish A. campestris
been little studied anatomically. Its taxonomy and from A. robusta in the Distrito Federal, Brazil (Mar-
some anatomical, morphological, palynological and tins, 2012), and further studies of the external mor-
cytological data were presented by Moraes (1996), who phology of three cerrado species (A. campestris,
recognized four species: A. arenaria (Gomes) Kuntze; A. leucocalyx and A. robusta) could not separate
A. brevicalyx M.Moraes; A. campestris (Mart.) Kuntze; them (Martins et al., 2015).
and A. leucocalyx (Drude) Kuntze. Subsequently, Although some studies have addressed the taxo-
nomic relationships of Allagoptera with other palm
*Corresponding author. E-mail: [email protected] genera (Asmussen & Chase, 2001; Hahn, 2002;

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016 1
2 A. S. PINEDO ET AL.

Gunn, 2004), we still lack an analysis of the relation- using acid dissociation (Krauss & Arduin, 1997).
ships between Allagoptera species. In her taxonomic Classical plant anatomy procedures were used to
review, Moraes (1996) observed the existence of two make slides (Johansen, 1940). At least four samples
species groups: one included A. campestris, A. leuco- were used per individual. The sections were analysed
calyx and A. arenaria; and the other only A. brevica- using a Zeiss optical microscope and the images were
lyx. Her study, however, did not include the recently obtained with a Leica photomicroscope associated
added species A. caudescens and A. robusta. There- with the computer, using the LAS EZ image capture
fore, the relationship between Allagoptera species system.
still has gaps to be filled. In this study, we aimed to
apply leaf anatomical features to advance the taxo-
nomic understanding of Allagoptera. TERMINOLOGY AND DATA ANALYSES

‘Leaf segment’ was adopted to designate the parts of

each palm leaf (Horn et al., 2009; Martins, 2012),
instead of ‘leaflet’ (Nowak, Dengler & Posluszny,
MATERIAL AND METHODS
2008; Noblick, 2013) and ‘pinna’ (Horn et al., 2009;
COLLECTION OF MATERIAL Defaveri et al., 2015; Martins et al., 2015). The char-
The material of A. brevicalyx was borrowed from two acters were compiled from the leaf anatomical litera-
herbaria with permission to remove leaf samples for ture on Arecaceae (Glassman, 1972; Barfod, 1988;
anatomical studies. The other five species were col- Moraes, 1996; Horn et al., 2009; Mill
an & Kahn,
lected in the field following the methods described by 2010; Alvarado & J
auregui, 2011; Tomlinson et al.,
Martins & Filgueiras (2010). All vouchers are listed 2011; Batagin-Piotto et al., 2012; Noraini et al.,
in Table 1. The herbarium acronyms are according 2012; Noblick, 2013; Martins et al., 2015). For the
to Thiers (2008–onward). Samples were removed quantitative analyses of the epidermis, hypodermis
from the middle third of a leaf segment, located in and mesophyll thickness, we used a mean of four
the median leaf region. The herbarium material was measurements of two leaf segments of three individ-
rehydrated in 50% (v/v) aqueous glycerine in a stove uals per species.
at c. 60 °C for 48 h, dehydrated in an ethanolic gra- The term ‘bulliform cells’ (Appezzato-da-Gl
oria &
dient and conserved in 70% ethanol. We analysed at Carmello-Guerreiro, 2009), used for grasses, was
least four individuals per species. adopted here instead of ‘expansion tissue’ (Silva &
Potiguara, 2008; San
ın & Galeano, 2011; Martins,
2012), ‘expansion cells’ (Mill

an & Kahn, 2010; Alvar-
ANATOMICAL STUDY ado & J
auregui, 2011; Tomlinson et al., 2011) or
Cross-sections were made with a table microtome ‘expansion cell tissue’ (Glassman, 1972; Noblick,
(Ranvier type). Paradermal sections were made 2013). ‘Bulliform cells’ designates only the

Table 1. Vouchers for the Allagoptera species analysed for their leaf anatomy

Species Voucher Locality

Allagoptera arenaria Pinedo 8, 9, 10 (UB) Biological Reserve of Jurubatiba – RJ, 22°140 S, 41°350 W
(Gomes) Kuntze (restinga)
Allagoptera brevicalyx Guedes et al. 19334 (ALCB) Conservation area UNIDUNAS – BA, 12°140 S, 37°510 W
M.Moraes* (restinga)
Loureiro et al. 755 (ALCB) S~
ao Jo~ ao Forest – BA, 12°320 S, 38°170 W (restinga)
Guedes 1213 (ALCB) Dunes of Salvador’s airport – BA, 12°550 S, 38°190 W (restinga)
Matos & Vidal 797 (HUEFS) S~
ao Jo~ ao Forest – BA, 12°320 S, 38°170 W (restinga)
Allagoptera campestris Pinedo 2, 4 (UB) Bras
ılia’s Botanical Garden – DF, 15°520 S, 47°500 W
(Mart.) Kuntze (Campo sujo, cerrado)
Allagoptera caudescens Pinedo 6, 7 (UB) Ecological Reserve Pocßo das Antas – RJ 22°350 S, 42°200 W
(Mart.) Kuntze (Atlantic Forest)
Allagoptera leucocalyx Pinedo & Silvestre 11, 12 (UB) Quebra Coco stream, Cavalcante – GO 13°360 S,
(Drude) Kuntze 47°280 W (Cerrad~ ao, cerrado)
Allagoptera robusta Pinedo & Martins 1, 3 (UB) Park Way Mansions Sector – DF, 15°530 S, 47°550 W
R.C.Martins & Filg. (Cerrad~ ao, cerrado)

*Species analysed exclusively from herbarium material, with the permission of the curator. The herbarium acronyms in
the vouchers follow Thiers (2008–onward).

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
 ALLAGOPTERA LEAF ANATOMY 3

differentiated cells near the midvein, and ‘bulliform sheath, rounded to ovate, locked, semilocked or free
cell complex’ refers to the whole group made up of in the adaxial and abaxial sides; phloem in two to
these cells. six groups of conductive regions in the first-order
The classification of T€
urpe (1967) for the vascular vascular bundles; segment margin angled or
bundles of first, second and third order was followed rounded, thicker or thinner than lamina; marginal
and the term ‘fourth order’ was added to designate fibre groups present or absent (A. caudescens);
those with a smaller calibre. The terminology of intramarginal ledge present or absent; vascular
T€urpe (1967) was used to distinguish the vascular pattern variable between species.
bundles as locked, semi-locked or free, depending on
whether the union of the vascular bundle and
subepidermal sclerenchyma tissue was complete, KEY TO ALLAGOPTERA USING ANATOMICAL CHARACTERS

incomplete or absent. 1 Lamina plane or smooth abaxially, mesophyll

homogeneous, fibre groups in a continuous strip

2 Adaxial epidermis of the same thickness as the

RESULTS
abaxial, common epidermal cells of varying size,
ANATOMICAL DESCRIPTION stomata in a single row, main vascular bundle
Allagoptera Nees (Figs 1–6) bicollateral. . .. . .. . .. . ...A. campestris
Lamina plane to strongly undulate abaxially, 20 Adaxial epidermis thinner than the abaxial, com-
hypostomatic; cuticle and external periclinal wall mon epidermal cells of uniform size, stomata in
complex thicker, thinner or as thick as the epider- 2–3 rows, main vascular bundle collateral or
mal cell interior; epidermis uniseriate, both sides bicollateral. . .. . .. . .. . .. . .. . .A. robusta
with the same thickness or thicker abaxially or
adaxially; common cells with straight contour; tri- 10 Lamina undulate or slightly depressed abaxially,
chomes absent; papillae only on the bulliform cells mesophyll classical or gradual dorsiventral, fibre
except in A. leucocalyx; adaxial epidermis 6–15 lm groups isolated or in an almost continuous strip
in thickness; common cells with variable shapes
and similar sizes, of the same height or higher 3 Leaf lamina undulate abaxially, stomata in two
than the anticlinal walls, in linear arrangement, rows
with junctions that are zig-zag or more and less
straight, or randomly arranged; abaxial epidermis 4 Lamina concave adaxially, adaxial hypodermis
4–15 lm thick; common cells rectangular or quad- equal to or thinner than the abaxial hypoder-
rangular and similar or variable in size, of the mis, vascular bundles of four size orders, mid-
same height or higher than the anticlinal walls, vein with several vascular bundles, marginal
irregular junctions; stomata tetracytic, in regular fibre groups absent. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .
rows in the intercostal region; guard cells reniform, . . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .
in depressions; subsidiary cells with ledges; bulli- . . .. . .. . .A. caudescens
form cell complex only on the abaxial surface, two 40 Lamina plane adaxially, adaxial hypodermis
or three cell layers thick, with or without inter- equal to or thicker than the abaxial hypoder-
spersed fibre groups; subepidermal fibre only at the mis, vascular bundles of three size orders, mid-
adaxial side, number variable, adjacent or inside vein with one vascular collateral bundle,
the hypodermis, in continuous bands or dispersed marginal fibre groups present. . .. . .. . .
groups; hypodermis thicker than epidermis, adaxial . . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . .. . ... A. brevicalyx
cells slightly bigger than the abaxial cells but smal-
ler in A. caudescens; adaxial hypodermis conspicu- 30 Leaf lamina slightly depressed abaxially, stom-
ous, one or two layers, 11–21 lm thick, cell shape ata in one or three rows
uniform or variable; abaxial hypodermis conspicu-
ous, one layer, 8–22 lm thick, cell shape uniform; 5 Epidermis > 8 lm thick, adaxial hypodermis
mesophyll classical dorsiventral, gradual dorsiven- > 14 lm thick, common epidermal cells of vari-
tral or homogeneous, five to ten cell layers, 112– able sizes, mesophyll classical dorsiventral,
337 lm thick; secretory glands present; raphids main vascular bundle collateral, fibre groups
absent; palisade parenchyma absent or present, frequent and in an almost continuous
with cells two to three times taller than wide, layer. . .. . .. . .. . .. . .. . .. . .. . .. . .. . ..A. arenaria
spongy parenchyma of five or six cell layers; vascu- 50 Epidermis < 8 lm thick, adaxial hypodermis
lar bundles generally up to fourth order (up to < 14 lm thick, common epidermal cells of
third only in A. brevicalyx), with sclerenchymatous uniform size, mesophyll gradual dorsiventral,

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
4 A. S. PINEDO ET AL.

Figure 1. Leaf anatomy of Allagoptera arenaria (restinga). A–F, cross-sections; G–I, paradermal sections. A, lamina
overview: gradual dorsiventral mesophyll. B, main vascular bundle of the leaf segment, highlighting the bulliform cells
(stars). C, leaf segment border with marginal fibre groups (triangle). D, leaf segment adaxial side. E, leaf segment abax-
ial side with stomatal complex (arrows). F, pattern of vascular bundles. G, adaxial epidermis. H, abaxial epidermis with
stomata arrangement. I, stomatal complex. Scale bars: A–C, F, H: 100 lm; G, I: 50 lm; D–E: 25 lm.

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
 ALLAGOPTERA LEAF ANATOMY 5

Figure 2. Leaf anatomy of Allagoptera brevicalyx (restinga). A–F, cross-sections; G–I, paradermal sections. A, lamina
overview: classical dorsiventral mesophyll. B, main vascular bundle of the leaf segment, highlighting the bulliform cells
(stars). C, leaf segment border with marginal fibre groups (triangle). D, leaf segment adaxial side. E, leaf segment abax-
ial side with stomatal complex (arrow). F, pattern of vascular bundles. G, adaxial epidermis. H, abaxial epidermis with
stomata arrangement. I, stomatal complex. Scale bars: A–C, F, H: 100 lm; G, I: 50 lm; D, E: 25 lm.

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
6 A. S. PINEDO ET AL.

Figure 3. Leaf anatomy of Allagoptera campestris (cerrado). A–F, cross sections; G–I, paradermal sections. A, lamina
overview: homogeneous mesophyll. B, main vascular bundle of the leaf segment, highlighting the bulliform cells (stars).
C, leaf segment border with marginal fibre groups (triangle). D, leaf segment adaxial side. E, leaf segment abaxial side
with stomatal complex and subsidiary ledges (arrows). F, pattern of vascular bundles. G, adaxial epidermis. H, abaxial
epidermis with stomata arrangement. I, stomatal complex. Scale bars: A–C, F, H: 100 lm; G, I: 50 lm; D–E: 25 lm.

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
 ALLAGOPTERA LEAF ANATOMY 7

Figure 4. Leaf anatomy of Allagoptera caudescens (Atlantic Forest). A–F, cross-sections; G–I, paradermal sections. A,
lamina overview (classical dorsiventral mesophyll). B, main vascular bundle of the leaf segment, highlighting the bulli-
form cells (stars). C, leaf segment border with a secretory gland (asterisk). D, leaf segment adaxial side. E, leaf segment
abaxial side with stomatal complex (arrow). F, pattern of vascular bundles. G, adaxial epidermis. H, abaxial epidermis
with stomata arrangement. I, stomatal complex. Scale bars: A–C, F, H: 100 lm; G, I: 50 lm; D–E: 25 lm.

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
8 A. S. PINEDO ET AL.

Figure 5. Leaf anatomy of Allagoptera leucocalyx (cerrado). A–F, cross-sections; G–I, paradermal sections. A, lamina
overview: gradual dorsiventral mesophyll. B, main vascular bundle of the leaf segment, highlighting the bulliform cells
(stars). C, leaf segment border with marginal fibre groups (triangle) and a secretory gland (asterisk). D, leaf segment
adaxial side. E, leaf segment abaxial side with stomatal complex (arrow). F, pattern of vascular bundles. G, adaxial epi-
dermis. H, abaxial epidermis with stomata arrangement. I, stomatal complex. Scale bars: A–C, F, H: 100 lm; G, I:
50 lm; D–E: 20 lm.

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
 ALLAGOPTERA LEAF ANATOMY 9

Figure 6. Leaf anatomy of Allagoptera robusta (cerrado). A–F, crosssections; G–I, paradermal sections. A, lamina over-
view: homogeneous mesophyll. B, main vascular bundle of the leaf segment, highlighting the bulliform cells (stars). C,
leaf segment border with marginal fibre groups (triangle). D, leaf segment adaxial side. E, leaf segment abaxial side
with stomatal complex and subsidiary ledges (arrows). F, pattern of vascular bundles. G, adaxial epidermis. H, abaxial
epidermis with stomata arrangement. I, stomatal complex. Scale bars: A–C, F, H: 100 lm; G, I: 50 lm; D–E: 20 lm.

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
10 A. S. PINEDO ET AL.

main vascular bundle bicollateral, fibre groups cells of the same height as the anticlinal walls; cuti-
rare and in isolated groups. . .. . .. . .. . .. . . cle and external periclinal wall complex thicker
. . .. . .. . .. . .. . .. . .. . .. . ..A. leucocalyx adaxially and thinner abaxially than the epidermal
cell interior; papillae on the bulliform cells. Adaxial
epidermis 13 lm thick; common cells rectangular or
Allagoptera arenaria (Gomes) Kuntze (Fig. 1) quadrangular in shape, one to two times wider than
Lamina plane to slightly undulate abaxially tall (Fig. 2G). Abaxial epidermis 11 lm thick; com-
(Fig. 1A); epidermis thicker abaxially than adaxi- mon cells of uniform size, in a zig-zag pattern
ally; common cells of the same height as the anticli- (Fig. 2I). Stomata in no more than five rows
nal walls; cuticle and external periclinal wall (Fig. 2H); stomatal ledges present. Subsidiary cells
complex as thick as the epidermal cell interior; wider at the apex; subsidiary cell ledges short. Bulli-
papillae on the bulliform cells. Adaxial epidermis form cell complex in no more than two cell layers,
9 lm thick; common cells rectangular or quadrangu- two or three times wider than tall, without inter-
lar, two to three times wider than tall (Fig. 1G). spersed fibre groups, one group on each side of the
Abaxial epidermis 13 lm thick; common cells of main vascular bundle (Fig. 2B). First layer bulliform
variable sizes, in a zig-zag pattern (Fig. 1I). Sto- cells of 10–15 unequally sized cells. Fibre groups
mata in no more than five rows (Fig. 1H); stomatal rare, in a discontinuous layer, five to ten fibres per
ledges present. Subsidiary cells wider at the apex; group (Fig. 2A). Subepidermal fibres similar to those
subsidiary cell ledges short. Bulliform cell complex of the vascular bundle sheaths. Hypodermis conspic-
up to three cell layers, two to three times wider uous, two layers adaxially; adaxial hypodermis
than tall, without interspersed fibre groups, one 18 lm thick, cells with variable shapes, one to two
group on each side of the main vascular bundle times wider than tall (Fig. 2D); abaxial hypodermis
(Fig. 1B). First layer bulliform cells of 15–20 equally 12 lm thick, cells about as wide as tall (Fig. 2E).
sized cells. Fibre groups abundant, in a continuous Mesophyll classical dorsiventral, seven cell layers,
layer, more than ten fibres per group (Fig. 1A). 190 lm thick, well lignified (Fig. 2A); palisade par-
Subepidermal fibres distinct from those of the vas- enchyma two cell layers; spongy parenchyma with no
cular bundle sheaths. Hypodermis two layers adaxi- more than five cell layers. Midvein with one vascular
ally; adaxial hypodermis 18 lm thick, cells with bundle collateral, elliptical, semilocked or free adaxi-
variable shapes, one to two times wider than tall ally and abaxially, slightly lignified; protoxylem on
(Fig. 1D); abaxial hypodermis conspicuous, 14 lm the adaxial side; metaxylem vessels no more than
thick, cells 1.0–1.5 times wider than tall (Fig. 1E). three. First- and second-order vascular bundles
Mesophyll classical dorsiventral to gradual dorsiven- locked adaxially and abaxially. Third-order vascular
tral, eight or more cell layers, 289 lm thick, well bundles free adaxially and locked abaxially. Fourth-
lignified (Fig. 1A); palisade and spongy parenchyma order vascular bundles absent (Fig. 2A). Commissure
indistinct (specimens with gradual dorsiventral mes- vascular bundles equidistant from both lamina sur-
ophyll) or present (specimens with classical dor- faces. Leaf segment margin rounded, of the same
siventral mesophyll). Midvein with one vascular thickness as the lamina, strongly lignified; marginal
bundle collateral or bicollateral, pyriform, locked or fibre groups exclusively rounded, one or more; intra-
semilocked adaxially and abaxially, slightly ligni- marginal ledge absent (Fig. 2C).
fied; protoxylem on the adaxial side; metaxylem ves-
sels four to six. First-order vascular bundles Allagoptera campestris (Mart.) Kuntze (Fig. 3)
semilocked adaxially and abaxially. Second-order Lamina plane abaxially (Fig. 3A); epidermis of about
vascular bundles semilocked adaxially and semi- the same thickness on both sides; cuticle and exter-
locked or free abaxially. Third-order vascular bun- nal periclinal wall complex much thinner than the
dles free adaxially and locked or semilocked epidermal cell interior; papillae on the bulliform
abaxially. Fourth-order vascular bundles free adaxi- cells. Adaxial epidermis 8 lm thick; common cells
ally and locked abaxially (Fig. 1A). Commissure vas- with pentagonal shape, two to three times wider
cular bundles equidistant from both lamina than tall, much shorter than anticlinal walls
surfaces. Leaf segment margin angled, thicker than (Fig. 3G). Abaxial epidermis 7 lm thick; common
lamina, well lignified; marginal fibre groups ovate cells of variable sizes, in a straight pattern, of the
or rounded, one or more; intramarginal ledge pre- same height as the anticlinal walls (Fig. 3I). Stomata
sent, relatively highly elevated (Fig. 1C). in no more than three rows (Fig. 3H); stomatal
ledges absent. Subsidiary cells wider at the middle;
Allagoptera brevicalyx M.Moraes (Fig. 2) subsidiary cell ledges short. Bulliform cell complex
Lamina undulate abaxially (Fig. 2A); epidermis no more than two cell layers thick, one to two times
slightly thicker adaxially than abaxially; common wider than tall, with interspersed fibre groups, one

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
 ALLAGOPTERA LEAF ANATOMY 11

group on each side and a little group below the main layers. Midvein with several vascular bundles, pyri-
vascular bundle (Fig. 3B). First layer bulliform cells form, locked adaxially and free abaxially, strongly
of 10–15 unequally sized cells. Fibre groups abun- lignified; protoxylem on the adaxial side and middle
dant, in a continuous layer, more than ten fibres per of the lamina; metaxylem vessels more than seven.
group (Fig. 3A). Subepidermal fibres similar to those First-order vascular bundles semilocked adaxially
of the vascular bundle sheaths. Hypodermis one and free abaxially. Second-order vascular bundles
layer adaxially; adaxial hypodermis 15 lm thick, free adaxially and semilocked abaxially. Third- and
cells uniform, more than two times wider than tall fourth-order vascular bundles free adaxially and
(Fig. 3D); abaxial hypodermis conspicuous, 10 lm locked abaxially (Fig. 4A). Commissure vascular bun-
thick, cells slightly taller than wide (Fig. 3E). Meso- dles equidistant from both lamina surfaces. Leaf seg-
phyll homogeneous, six cell layers, 184 lm thick, ment margin angled, thinner than lamina, slightly
strongly lignified (Fig. 3A). Midvein with one vascu- lignified; marginal fibre groups absent; intra-
lar bundle bicollateral, pyriform, locked adaxially marginal ledge absent (Fig. 4C).
and semilocked abaxially, lignified; protoxylem on
the adaxial side and middle of the lamina; metaxy- Allagoptera leucocalyx (Drude) Kuntze (Fig. 5)
lem vessels fewer than three. First-order vascular Lamina plane abaxially (Fig. 5A); epidermis slightly
bundles locked adaxially and locked or semilocked thicker abaxially than adaxially; cuticle external
abaxially. Second- and third-order vascular bundles periclinal wall complex thinner than the epidermal
locked adaxially and abaxially. Fourth-order vascular cell interior; papillae absent. Adaxial epidermis
bundles locked or free adaxially and locked abaxially 7 lm thick; common cells with pentagonal shape,
(Fig. 3A). Commissure vascular bundles adaxially in one or two times wider than tall, shorter than the
the lamina. Leaf segment margin angled, thicker anticlinal walls (Fig. 5G). Abaxial epidermis 6 lm
than lamina, strongly lignified; marginal fibre group thick; common cells of uniform sizes, in a straight
single, ovate or triangular; intramarginal ledge pattern, of the same height as the anticlinal walls
present, relatively high elevated (Fig. 3C). (Fig. 5I). Stomata in no more than three rows
(Fig. 5H); stomatal ledges present. Subsidiary cells
Allagoptera caudescens (Mart.) Kuntze (Fig. 4) wider at the middle; subsidiary cell ledges short.
Lamina strongly undulate abaxially (Fig. 4A); epi- Bulliform cell complex in no more than two cell lay-
dermis slightly thicker abaxially than adaxially; cuti- ers, two to three times wider than tall, without
cle and external periclinal wall complex about as interspersed fibre groups, one group on each side of
thick adaxially and thinner abaxially than the epi- the main vascular bundle (Fig. 5B). First layer bul-
dermal cell interior; papillae on the bulliform cells. liform cells of 10–15 equally sized cells. Fibre
Adaxial epidermis 7.4 lm thick; common cells with groups rare, in a discontinuous layer, fewer than
pentagonal shape, more than three times wider than five fibres per group (Fig. 5A). Subepidermal fibres
tall, of the same height as the anticlinal walls distinct from those of the vascular bundle sheaths.
(Fig. 4G). Abaxial epidermis 8 lm thick; common Hypodermis one layer adaxially; adaxial hypodermis
cells of variable sizes, in a zig-zag pattern, shorter 13 lm thickness, cells uniform, one or two times
than anticlinal walls (Fig. 4I). Stomata in no more wider than tall (Fig. 5D); abaxial hypodermis con-
than five rows (Fig. 4H); stomatal ledges absent. spicuous, 14 lm thick, cells 1.0–1.5 times wider
Subsidiary cells wider at the middle; subsidiary cell than tall (Fig. 5E). Mesophyll gradual dorsiventral,
ledges very short. Bulliform cell complex in no more five cell layers, 126 lm thick, lignified (Fig. 5A).
than three cell layers, more than three times wider Midvein with two vascular bundles, bicollateral,
than tall, with interspersed fibre groups, one single angled, locked adaxially and locked or semilocked
and continuous group below the main vascular bun- abaxially, strongly lignified; protoxylem on the
dle (Fig. 4B). First layer bulliform cells of 20 equally adaxial side and middle of the lamina; metaxylem
sized cells. Fibre groups frequent, in a discontinuous vessels four to six. First-order vascular bundles
layer, five to ten fibres per group (Fig. 4A). Subepi- locked adaxially and abaxially. Second-order vascu-
dermal fibres distinct from those of the vascular bun- lar bundles locked or semilocked adaxially and
dle sheaths. Hypodermis one layer adaxially; adaxial locked abaxially. Third- and fourth-order vascular
hypodermis 14 lm thick, cells in variable shapes, bundles free adaxially and semilocked abaxially
slightly taller than wide (Fig. 4D); abaxial hypoder- (Fig. 5A). Commissure vascular bundles equidistant
mis not conspicuous, 19 lm thick, cells slightly taller from both lamina surfaces. Leaf segment margin
than wide (Fig. 4E). Mesophyll classical dorsiventral, angled, as thick as the lamina, strongly lignified;
more than eight cell layers, 186 lm thick, slightly marginal fibre group single, ovate or rounded;
lignified (Fig. 4A); palisade parenchyma two cell lay- intramarginal ledge present, relatively low elevated
ers; spongy parenchyma with no more than six cell (Fig. 5C).

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
12 A. S. PINEDO ET AL.

Allagoptera robusta R.C.Martins & Filg. (Fig. 6) The absence of corrugations on the adaxial leaf
Lamina plane abaxially (Fig. 6A); epidermis thicker surface in all species and the great thickness of the
abaxially than adaxially; cuticle and external pericli- cuticle and external periclinal wall complex is proba-
nal wall complex as thick as the epidermal cell inte- bly an adaptation to intense light conditions in the
rior; papillae on the bulliform cells. Adaxial habitat (Fahn, 1982). Two groups of species, one with
epidermis 8 lm thick; common cells with an irregu- undulate or slightly depressed and the other with a
lar shape, two to three times wider than tall, much plane abaxial surface, can be distinguished.
shorter than the anticlinal walls (Fig. 6G). Abaxial Both restinga species (A. arenaria and A. brevica-
epidermis 11 lm thick; common cells of uniform size, lyx) had their stomata sunken in depressions, which is
in a zig-zag pattern, of the same height as the anti- a common adaptation to water stress. Allagoptera are-
clinal walls (Fig. 6I). Stomata in no more than five naria is common in the restinga, where it experiences
rows (Fig. 6H); stomatal ledges absent. Subsidiary water stress (Magnago, Martins & Pereira, 2011).
cells wider at the apex; subsidiary cell ledges long. The thickness of the epidermis varies greatly
Bulliform cell complex in no more than three cell lay- between the species. The epidermal thickness is
ers, one or two times wider than tall, with inter- directly related to the exposure of the plant to sun
spersed fibre groups, a group on each side and a (Santiago et al., 2001) and species with the adaxial
little group below the main vascular bundle epidermis of the same thickness or thinner than the
(Fig. 6B). First layer bulliform cells of 10–15 abaxial ones usually develop in shady environments.
unequally sized cells. Fibre groups abundant, in a Our results corroborate this idea, especially consider-
continuous layer, more than ten fibres per group ing that Moraes (1996) pointed out that A. arenaria
(Fig. 6A). Subepidermal fibres similar to those of the and A. brevicalyx grow in full sun, whereas A. leuco-
vascular bundle sheaths. Hypodermis one layer calyx is an understorey species.
adaxially; adaxial hypodermis 16 lm thick, cells with Thinner cuticle and external periclinal wall com-
uniform shape, more than two times wider than tall plex, as found in A. campestris, is usually found in
(Fig. 6D); abaxial hypodermis conspicuous, 14 lm species growing in mesophytic conditions (Fahn,
thick, cells 1.0–1.5 times wider than tall (Fig. 6E). 1982), in agreement with the observation that this
Mesophyll homogeneous, six cell layers, 292 lm species prefers shady environments in the cerrado
thick, very lignified (Fig. 6A). Midvein with two or (Martins, 2012). On the other hand, A. arenaria and
three vascular bundles, collateral or bicollateral, A. brevicalyx grow in full sun (Moraes, 1996), which is
elliptical, locked adaxially and semilocked or free accompanied with having the external cuticle pericli-
abaxially, lignified; protoxylem on the adaxial side nal wall complex thicker than the epidermal cell inte-
and middle of the lamina; metaxylem vessels four to rior. Thick outer walls in adaxial epidermal cells were
six. First-order vascular bundles semilocked adaxi- observed in all Allagoptera species (Moraes, 1996).
ally and abaxially. Second-order vascular bundles Stomata in palms do not necessarily occur in contin-
locked or semilocked adaxially and abaxially. Third- uous regular longitudinal rows (Tomlinson et al.,
order vascular bundles locked adaxially and semi- 2011). In Allagoptera, the distribution of stomatal
locked abaxially. Fourth-order vascular bundles free rows varied between the species. Anomocytic stomata,
adaxially and locked abaxially (Fig. 6A). Commissure as reported for A. campestris (Martins et al., 2015),
vascular bundles equidistant from both lamina sur- were not observed here. We only found tetracytic
faces. Leaf segment margin angled, as thick as lam- stomata with two terminal subsidiary cells and two
ina, strongly lignified; marginal fibre group single, other narrow and sunken lateral cells (e.g. Fig. 1E). In
ovate or rounded; intramarginal ledge present, rela- paradermal sections, the terminal cells are polygonal,
tively low elevated (Fig. 6C). instead of tetragonal, and the lateral ones are not con-
spicuous. The combination of transversal and parader-
mal sections is essential for the identification of the
sunken subsidiary cells. Stomatal ledges of cuticular
DISCUSSION
projections are common on the guard cell toward the
Anatomical leaf characters clearly distinguish the six ostiole (Appezzato-da-Gl
oria & Carmello-Guerreiro,
Allagoptera species in ways similar to what has been 2009) and have been found in cocosoid palms (Tomlin-
found in some other palm genera, including Oenocar- son, 1961) and also here in Allagoptera.
pus Mart. and others (Silva & Potiguara, 2008; Tom- The presence of ledges on the subsidiary cells, here
linson et al., 2011). We were able to define 128 leaf called subsidiary ledges, was observed in our study.
anatomical characters, a high number, and compara- These are projections of the subsidiary cells that
ble to what has been found in leaf transversal and embrace the guard cells and are raised, making an
paradermal sections in some Poaceae (T€ urpe, 1967; edge around the guard cells (Figs 3E, 6E). This phe-
Oliveira et al., 2015; Reis et al., 2015). nomenon appears to have not yet been described in

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
 ALLAGOPTERA LEAF ANATOMY 13

the literature, although they may have been shown abaxial hypodermis of this same species, however, is
in some anatomical illustrations (Appezzato-da- the thickest among all.
Gl
oria & Carmello-Guerreiro, 2009; Oliveira & The mesophyll is isobilateral or dorsiventral in
Machado, 2009). In Arecaceae, these structures have Attaleinae (Tomlinson et al., 2011) and dorsiventral
been observed in Chamaerops L. and Trachycarpus in Allagoptera (Moraes, 1996). Our results agree
H.Wendl. (Tomlinson et al., 2011) and in Oenocarpus with these observations for A. brevicalyx (which
(Silva & Potiguara, 2008). Subsidiary ledges seem to grows in restinga) and A. caudescens (which grows
be more common than stomatal ledges in Arecaceae, in the Atlantic forest), in which the palisade and
and appear to be an anatomical peculiarity of some spongy layers are quite evident. No distinction in the
species in the family, and possibly a synapomorphy palisade and spongy layers was observed in A. cam-
for certain groups. pestris and A. robusta (cerrado species). They have a
Having the guard cells sunken in depressions is a homogeneous mesophyll, with cells with similar
feature that creates a humid microenvironment that heights. Homogeneous mesophyll composed of pal-
reduces the leaf transpiration rate (Esau & Morretes, isade cells with different sizes is found in A. arenaria
1974). Both stomatal and subsidiary ledges seem to (restinga) (Defaveri et al., 2015). We also noted this
expand this humid microenvironment and reduce cell size variation in this species and in A. leucocalyx
leaf transpiration even more, providing water sav- (cerrado), but we did not observe homogeneous meso-
ings for the plant. phyll. The gradual reduction in cell height produces
We propose to use the term ‘bulliform cells’ for Are- dorsiventrality in the lamina. This variation occurs
caceae, as the cells are similar to those found in Poa- gradually from the adaxial to the abaxial surface,
ceae and have the same function with the difference making it impossible to distinguish a typical spongy
that bulliform cells generally occur adaxially in grass parenchyma. Consequently, we propose a new classi-
leaf lamina (T€ urpe, 1967; Oliveira et al., 2015; Reis fication for the mesophyll: (a) ‘classical dorsiventral
et al., 2015). The bulliform cells in palms are present mesophyll’, in which the palisade and spongy par-
only on the abaxial surface. Variations between spe- enchyma are clearly differentiated from each other
cies in number of cell layers and the occurrence of (A. brevicalyx and A. caudescens); and (b) ‘gradual
fibre groups mixed with the bulliform cells were signif- dorsiventral mesophyll’, in which the cells are gradu-
icant for species separation in Allagoptera. Bulliform ally reduced in size (A. arenaria and A. leucocalyx).
cells may be homologous in Poaceae and Arecaceae; The bundles have an abaxial position in the leaf
ontogenetic studies should clarify this. lamina, agreeing with the results presented by Mor-
In Allagoptera, the hypodermis is well developed aes (1996). Allagoptera belongs to Arecoideae,
and thicker than the epidermis, both adaxially and defined by Thomas & Boura (2015) as the ‘one vessel’
abaxially, similar to the situation in Syagrus Mart. subfamily, based on the number of metaxylem ves-
and Cocos L. (Tomlinson, 1961; Tomlinson et al., sels in vascular bundles of the stem, and it would
2011). The hypodermal cells are uniseriate on both often be correlated with a tropical rain forest habitat.
sides, except in A. arenaria and A. brevicalyx which The vasculature is continuous in the plants. Conse-
have two adaxial layers, which is in contrast to Mor- quently, the number of metaxylem vessels in the
aes (1996) who described three or four adaxial layers leaves should not be very different from that of the
and one or two abaxial layers for the genus. stems. Therefore, some Allagoptera species are
Cuticle and external periclinal wall complex, epider- exceptions in the ‘one vessel’ subfamily proposed by
mis and hypodermis together distinguish two groups, Thomas & Boura (2015) for Arecoideae.
one with a thin coating (A. campestris, A. caudescens The vascular bundles are in contact with one or
and A. leucocalyx) and another with a thick coating both epidermal surfaces in Attaleinae (Tomlinson
(A. arenaria, A. brevicalyx and A. robusta). Allagop- et al., 2011), and this connection occurs by means of
tera brevicalyx had both a well-developed epidermis fibre fascicles in Allagoptera species (Moraes, 1996).
and hypodermis, whereas in A. robusta, the hypoder- Here we show that the first- and second-order bun-
mal cells almost substituted the epidermal layer, dles are connected to both epidermal surfaces (except
being almost absent. When compared with the hypo- in A. caudescens, an Atlantic Forest species), the
dermal cells, the epidermal cells are almost always third-order bundles are attached to one or both leaf
thinner in palms (Tomlinson et al., 2011). sides and the fourth-order bundles are united only to
Allagoptera caudescens is native to mesophytic for- the abaxial surface. The classification of the leaf bun-
ests and grows under lower light and water stress dles regarding its epidermal connection in species of
than the other species analysed (DeWalt, Maliakal & Poaceae (T€ urpe, 1967) can be used for Allagoptera
Denslow, 2003; McElhinny et al., 2005). Thus, the and probably for all Arecaceae. In this way, the vas-
thin adaxial hypodermis in this species could be cular bundle can be locked, semilocked or free adaxi-
related to relaxed environmental pressures. The ally and abaxially in these plants.

© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016
14 A. S. PINEDO ET AL.

A distinct pattern of distribution of the vascular English text. Thanks to the herbarium curators for
bundles was observed in the leaf segments. There is allowing us to take small samples of the herbarium
a repetition of the sequence of the first-, second-, specimens for anatomical study. Also, thanks to
third- and fourth-order bundles that is unique to CAPES for a grant to the first author.
each species, constituting a leaf vascular pattern.
The fibres are abundant, with distinct organization
in the adaxial hypodermis, as pointed out by Tomlin-
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