foliar anatomy of beaucarnea lemaire (nolinaceae ss)

1 23

Plant Systematics and Evolution ISSN 0378-2697Volume 300Number 10 Plant Syst Evol (2014) 300:2249-2258DOI 10.1007/s00606-014-1048-2

Foliar anatomy of Beaucarnea Lemaire(Nolinaceae ss)

Mahinda Martínez, Luis Hernández-Sandoval & Lilia Carrillo

1 23

Your article is protected by copyright and

all rights are held exclusively by Springer-

Verlag Wien. This e-offprint is for personal

use only and shall not be self-archived

in electronic repositories. If you wish to

self-archive your article, please use the

accepted manuscript version for posting on

your own website. You may further deposit

the accepted manuscript version in any

repository, provided it is only made publicly

available 12 months after official publication

or later and provided acknowledgement is

given to the original source of publication

and a link is inserted to the published article

on Springer's website. The link must be

accompanied by the following text: "The final

publication is available at link.springer.com”.

ORIGINAL ARTICLE

Foliar anatomy of Beaucarnea Lemaire (Nolinaceae ss)

Mahinda Martınez • Luis Hernandez-Sandoval •

Lilia Carrillo

Received: 1 November 2013 / Accepted: 18 March 2014 / Published online: 9 April 2014

� Springer-Verlag Wien 2014

Abstract Beaucarnea (Nolinaceae) is a Mexican and

Guatemalan genus that inhabits dry tropical areas. Most of

the species are endangered under the Mexican legislation

because they have a high horticultural demand and are

threatened by habitat destruction. Species are difficult to

recognize, since their differences are a mixture of trunk,

inflorescence and fruit characters frequently absent in

herbarium specimens. The aim of this work is to describe

the foliar anatomy of the 11 species of Beaucarnea in

search of characters with taxonomic value to sustain the

generic subdivision, and to provide a key for specimens

determination based on leaf and growth form. We found

that four species (B. compacta, B. gracilis, B. purpusii and

B. stricta) have a grooved leaf outline in transverse section,

whereas the rest of the species are undulated. Other char-

acters, such as epicuticular waxes, stomatal distribution

and density, marginal teeth length and leaf apex provide

valuable characters for species determination.

Keywords Characters � Generic subdivision � Vegetative

determination

Introduction

Beaucarnea (Nolinaceae sensu Nakai 1943, Asparagaceae

Nolinoideae sensu APGIII (Chase et al. 2009) comprises

11 xerophytic species distributed from northern Mexico to

Central America (Hernandez et al. 2012). Only B. com-

pacta lacks an elongated stem, since the plant base grows

in diameter, but not in height (Fig. 1a). Most species are

arborescent with a swollen trunk bases, and the typically

xeromorphic leaves are crowded at the apex of a several

meter high stem (Fig. 1b–e). The vast majority of the

species are considered endangered under Mexican legisla-

tion (NOM-ECOL 059 de Mexico, SEMARNAT 2010;

Hernandez 1993).

No studies have been carried out as to the foliar anatomy

of all the described species of Beaucarnea, but in Nolin-

aceae (Beaucarnea, Calibanus, Dasylirion and Nolina),

leaves are isobilateral, with chlorenchyma reinforced with

fibers on both surfaces (Bogler 1998). The epidermis is

covered with a cuticle and epicuticular wax of the Con-

vallaria type. Stomata are sunken in papillated longitudinal

groves that close, especially when the plants dehydrate

(Bogler 1998). For Beaucarnea, Trelease (1911) suggested

that the genus could be subdivided into two sections: (1)

Beaucarnea (as Eubeaucarnea) for the species with

recurved leaves, smooth grooves and nearly smooth mar-

gins, which includes B. goldmanii, B. guatemalensis, B.

inermis, B. pliabilis and B. recurvata (see Fig. 1d, e) and

(2) sect. Papillatae (only B. gracilis and B. stricta, since he

considered B. purpusii a synonym of B. stricta) for the

plants with erect, papillose leaves (see Fig. 1b, c). Her-

nandez (1992) proposed that the characters correlate to the

different environments in which the species grow

(Table 1), and therefore this does not reflect generic sec-

tions. B. hiriartiae, for example, has intermediate

M. Martınez � L. Hernandez-Sandoval (&)

Licenciatura en Biologıa, Facultad de Ciencias Naturales,

Universidad Autonoma de Queretaro, Av. de las Ciencias s/n,

Juriquilla, 76230 Queretaro, Queretaro, Mexico

e-mail: [email protected]

L. Carrillo

Unidad de Recursos Naturales, Centro de Investigacion

Cientıfica de Yucatan, Calle 43 No. 130, Colonia Chuburna de

Hidalgo, 97200 Merida, Yucatan, Mexico

123

Plant Syst Evol (2014) 300:2249–2258

DOI 10.1007/s00606-014-1048-2

Author's personal copy

characters of both sections, since it has the papillated

grooves of sect. Papillatae, but the thin, recurved leaves of

sect. Beaucarnea.

Herbarium specimens of Beaucarnea recurvata from the

states of Veracruz and Oaxaca are often misidentified as B.

inermis from Tamaulipas and San Luis Potosı. The same

problem is frequent with B. gracilis, B. purpusii and B.

stricta from the Tehuacan Valley and neighboring areas.

Therefore, the purpose of this work was to describe the

foliar anatomy of the eleven species of Beaucarnea known

to date, contribute with taxonomic characters to evaluate

Trelease (1911) proposal, and provide a key that allows

specimens determination in the absence of flowers, fruit,

bark or adult specimens.

Materials and methods

At least two individuals of all the species collected in the

field or cultivated in gardens or greenhouses were exam-

ined, except for Beaucarnea guatemalensis from which we

only had herbarium material (see Table 1 for localities and

vouchers). Leaf bases up to where the sheathing area fin-

ishes, the middle portion and the leaf apex were fixed

separately. Material was fixed in Navashin’s solution (Jo-

hansen 1940), transferred to 70 % alcohol after 24 h, and

maintained there until processed. Calcium oxalate crystals

were partially eliminated by immersion in 25 % fluorohy-

dric acid for 5 days and then washed in tap water (Schnell

1967). Tissue was softened in 10 % ethylenediamine for

3 days at room temperature and rinsed in water. The

samples were then embedded in paraffin and sectioned with

a Leica rotary microtome at 12 microns (Ruzin1999). All

samples were cut transversally, except B. recurvata which

was also cut longitudinally to assess the presence of

Fig. 1 Plant and leaf forms of Beaucarnea: a B. compacta, erect

leaves, short stem covered by the old leaves, b B. gracilis, erect leaves

at the top of a several meter high stem, which are caducous, c B.

purpusii and B. stricta, erect leaves, stem covered by the old leaves,

d B. hiriartiae, B. goldmanii, B. guatemalensis and B. pliabilis in

which the leaves fold towards the middle of the blade, e B. inermis, B.

recurvata and B. sanctomariana, the leaves do not fold

Table 1 Species name, voucher information, distribution weather

and altitude

Species Locality and

collection number

Weather Altitude

(masl)

B. compacta L.

Hern. &

Zamudio

Guanajuato: San

Diego

Guamuchil, L.

Hernandez 4600

(QMEX)

Guanajuato:

Piedras Pintadas,

L. Hernandez

6354 (QMEX)

BSh (semi-

arid)

1,300–1,400

B. goldmanii

Rose

Chiapas: Uninajab

M.A. Perez

Farrera 3033

(QMEX)

Chiapas: Vivero

Faustino

Miranda

Aw (hot sub-

humid),

Cfa

(temperate

humid)

600–1,540

B. gracilis Lem. Puebla: Zapotitlan

de las Salinas, L.

Hernandez 6132

(QMEX) and L.

Hernandez 6289

(QMEX)

BSh (semi-

arid), Cwa

(temperate

sub-humid)

1,300–2,100

B. guatemalensis

Rose

Guatemala, Jalapa

L. Hernandez

1396-G

(MEXU)

Guatemala, Jalapa

L. Hernandez

2545 (MEXU)

Cwig

(temperate

sub-humid)

1,000–1,600

B. hiriartiae L.

Hern.

Guerrero: Canon

del Zopilote, L.

Hernandez 2463

(MEXU) and E.

Martınez s/n

(MEXU)

Cwa, Cfa

(both

temperate

sub-humid)

250–700

2250 M. Martınez et al.

123


phloem in the abaxial side vascular bundles. Slides were

stained with fast green safranin (Johansen 1940) and

mounted with permount. Pictures were taken in an Olym-

pus BX51 optical microscope with digital camera. Mea-

surements were obtained with Celera Scop (developed at

CICY) and Image J programs (http://www.rsbweb.nih.gov/

ij/, 2014). To determine if the central cells were alive, we

made free hand sections from greenhouse grown plants and

stained them with Evan’s blue (Peterson et al. 2008). For

the waxes, leaves were air-dried and observed in a Zeiss

Evo scanning electron microscope (SEM) at low vacuum.

For the crystals, leaves were free hand sectioned and

sputter coated, and for the stomata, leaves were critical

point dried and sputter coated. Both samples were analyzed

in a Zeiss Evo SEM at high vacuum. Numerical results

represent averages of two individuals and ten measure-

ments or counts per structure. Stomata density was calcu-

lated as number of stomata per square mm. Wax

nomenclature follows Barthlott and Frolich (1983) and

Barthlott et al. (1988). Mesophyll is described as suggested

by Radford et al. (1974), stomata according to Baranova

(1987), and crystals as Prychid and Ruddal (1999).

Results

Epidermis

Epicuticular waxes with crystalloids of the Convallaria

type (orientated) are present in B. compacta, B. gracilis, B.

hiriartiae, B. purpusii, B. recurvata, B. sanctomariana and

B. stricta (Fig. 2; Table 2). Crystalloids were more abun-

dant near and around the stoma, whereas the rest of the

surface had only a few wax crystalloids aggregated in

rosettes of unoriented plateletes. Beaucarnea goldmanii, B.

guatemalensis, B. inermis and B. pliabilis have only the

rosette crystalloids (Fig. 3). Leaves are amphistomatic with

tetracyclic arrangement in all species (Fig. 3). Stomata are

evident throughout both surfaces in B. goldmanii, B. hir-

iartiae, B. inermis, B. pliabilis and B. recurvata. In the

species with stomata sunken in crypts covered by cuticular

teeth (B. compacta, B. gracilis, B. purpusii, B. stricta), the

arrangement is only visible at the base of the leaf (Fig. 4)

because only the channels are evident on the rest of the

surface (Fig. 5). Stomata are aggregated in most of the

species (Table 2), except for B. goldmanii and B. pliabilis

in which they are solitary. Stomata density varies from a

low of 19 stomata/mm2 in B. goldmanii, to 110 in B.

sanctomariana (see Table 2). The thinnest cuticle is

Table 1 continued

Species Locality and

collection number

Weather Altitude

(masl)

B. inermis Rose San Luis Potosı:

San Geronimo,

H. Castillo 231

Cfa, Cw

(both

temperate

sub-humid)

30–350

B. pliabilis Rose Yucatan: Sigfredo

Escalante, R.

Orellana

2010.103

Yucatan: Sigfredo

Escalante, R.

Orellana

2010.001

Yucatan: Lilia

Carrillo, C.

Espadas-

Manrique

2013.001

BSh (semi-

arid)

5–30

B. purpusii Rose Puebla:

Xochitepec, L.

Hernandez 6134

(QMEX) and L.

Hernandez 6290

(QMEX)

BShw,

(semi-arid)

Aw, Amw0

(hot sub-

humid)

1,700–2,300

B. recurvata

Lem.

Oaxaca: Nizanda,

L. Hernandez

6294 (QMEX)

Veracruz: Lomas

de Roger, L.

Hernandez 6827

(QMEX)

Afw0 (hot

sub-humid)

150–1,000

B.

sanctomariana

L. Hern.

Oaxaca: Santa

Marıa

Chimapala,

M.A. Perez

Farrera s/n

(HEM)

Cfa

(temperate

sub-

humid),

Aw0 (hot

sub-humid)

200–250

B. stricta Lem. Oaxaca: La Ceiba,

L. Hernandez

6292 (QMEX)

Cwa, Cfa

(both

temperate

sub-humid)

500–1,200

Fig. 2 Epicuticular crystalloid waxes of the Convallaria type in B.

compacta, adaxial surface, (93560)

Foliar anatomy of Beaucarnea Lemaire 2251

123


http://www.rsbweb.nih.gov/ij/

http://www.rsbweb.nih.gov/ij/

present at the leaf base of B. stricta (0.3 lm), and the

thickest in B. goldmanii and B. gracilis (1.8 lm, see

Table 2). Beaucarnea compacta, B. gracilis, B. purpusii

and B. stricta have 4–8 rows of cuticular teeth on epider-

mal cells located near the furrow, covering the crypt almost

completely (Table 2; Fig. 6). The teeth in these species are

not actually on subsidiary cells. In B. goldmanii, B.

Table 2 Comparison of wax type, stomata, cuticle, leaf shape and crypt between the different species

Epicuticular

waxes

Stomata Stomata

density #/

mm2

Cuticle thickness at

the base of the leaf

Cuticle thickness at the

middle of the leaf (lm)

Leaf shape in

cross section

# of teeth at the

crypt and

location

B. compacta Convallaria Aggregated 19.6 0.9 lm 1.1 Grooved 4–5, epidermal

cells

B. goldmanii Absent Solitary 19 1.8 lm 0.9 Undulate 2, subsidiary

cells

projections

B. gracilis Convallaria Aggregated 72 1.8 lm 1.3 Grooved 5, epidermal

cells

B.

guatemalensis

Absent Aggregated 70 ND 1.5 Undulate 2, subsidiary

cells

projections

B. hiriartiae Convallaria Aggregated 78 1.1 lm 1.8 Undulate 2, subsidiary

cells

projections

B. inermis Absent Aggregated 40.8 0.5 lm 0.7 Undulate 2, subsidiary

cells

projections

B. pliabilis Absent Solitary 23.2 1.5 lm 1 Undulate 2, subsidiary

cells

projections

B. purpusii Convallaria Aggregated 30 0.7 lm 1.6 Grooved 7–8, epidermal

cells

B. recurvata Convallaria Aggregated 42.8 1.4 lm 1 Undulate 2, subsidiary

cells

projections

B.

sanctomariana

Convallaria Aggregated 110 0.5 lm 1.2 Undulate 2, subsidiary

cells

projections

B. stricta Convallaria Aggregated 40 0.3 lm 0.9 Grooved 4–5, epidermal

cells

Fig. 3 Epicuticular wax crystalloids aggregated in rosettes of unori-

ented platelets in B. goldmanii, tetracytic stomata, adaxial surface

(92,130)

Fig. 4 Epidermis of B. gracilis at the leaf base, adaxial surface (9294)


123


guatemalensis, B. hiriartiae, B. inermis, B. pliabilis, B.

recurvata and B. sanctomariana, the crypt is partially

covered by only two teeth that are cuticular projections

from the subsidiary cells (Fig. 7). Beaucarnea guatemal-

ensis and B. purpusii both have a papillose cuticle in the

area over the fibers (Figs. 8, 9), whereas B. compacta has

only a few such papillae in some individuals (Fig. 10). All

species have uniseriate epidermis. Epidermal cells are

isodiametric, densely cytoplasmic and densely nucleated

(Figs. 6, 7). The outer tangential walls of the epidermal

cells are very thick and saturated with cutin, the rest of the

walls are thin (Figs. 7, 12, 15).

Mesophyll

Leaves are isobilateral, and transverse outline can be either

grooved (Figs. 8, 10; see Table 2) in B. compacta,

B. gracilis, B. purpusii and B. stricta, or undulate (Fig. 11;

see Table 2) in B. goldmanii, B. guatemalensis, B. hiriar-

tiae, B. inermis, B. pliabilis, B. recurvata and B. sanc-

tomariana. Leaves have two lines of fibrovascular bundles

near the adaxial and abaxial surfaces of the leaf in B.

purpusii, B. goldmanii, B. pliabilis and B. sanctomariana

(Fig. 8). However, B. compacta, B. hiriartiae, B. gracilis,

B. guatemalensis, B. inermis and B. recurvata have fibro-

vascular bundles on the adaxial side, whereas the abaxial

side has mostly fiber bundles (Figs. 10, 11). Only culti-

vated specimens of B. gracilis have vascular bundles in the

Fig. 5 Epidermis of B. gracilis (grooved lamina) in the middle

portion of the leaf, adaxial surface (9114)

Fig. 6 Stomatic crypt of B. compacta (9400) with six cuticular teeth

on the epidermal cells. Stoma is at the bottom of the crypt

Fig. 7 Stomata of B hiriartiae (9200) with two subsidiary cell

projections. Abaxial side of the leaf

Fig. 8 Transversal view of the grooved leaf of B. purpusii (9100).

Adaxial side of the leaf facing up


123


middle of the mesophyll, which is thicker than the meso-

phyll of field individuals. B. compacta also has those

vascular bundles, even in field specimens (Fig. 10). Fibers

in girders in the adaxial and abaxial of the leaf are com-

pletely surrounding the vascular bundles (Fig. 12) in all

species. A parenchyma bundle sheath surrounds the fiber

girders almost completely, except for the area adjacent to

the cuticle. The parenchyma sheath, as well as the fiber

girders are conspicuous in the middle portion of the leaf

(Fig. 12), but are never so large at the base (Fig. 13,

immature, Fig. 14, mature). The parenchyma cells of the

sheath are larger than those of the chlorenchyma. The

mesophyll lacks channels or cavities. It is constituted by

three areas, two are formed by densely photosynthetic

chlorenchyma adjacent to the stomatal cavities alternating

with the fiber girders, and a central area formed by 2–15

rows of parenchyma cells (Figs. 8, 10, 11). The two or

three cell layers closest to the epidermis are photosynthetic.

The central cells lack chloroplasts and are larger than theFig. 9 Epidermis of B. guatemalensis with cuticular papillae (9192)

Fig. 10 Transversal view of the grooved leaf of B. compacta (940).


Fig. 11 Transversal view of the undulate leaf of B. hiriartiae (940).


Fig. 12 Vascular bundle with fibers and bundle sheath in the adaxial

side of the middle portion of B. compacta (9400)

Fig. 13 Vascular bundles without fibers in the basal portion of the

young leaf of B. inermis (9100)


123


chlorenchyma cells, and fiber bundles can be present,

especially at the base of the leaf. The central cells are alive

in all the layers and all the species.

Leaf margin

Leaf margins have fiber bundles (see Fig. 15) in all species.

They also have cuticular teeth, the smallest in B. compacta,

B. purpusii, B. guatemalensis and B. goldmanii (Fig. 16),

the largest in B. gracilis and B. hiriartiae (Fig. 17). All

teeth tips point towards the leaf apex. Teeth are caducous

and might be absent from the outermost leaves in the

rosette. Teeth also tend to be larger towards the tip of the

leaf than towards the base.

Vascular bundles

The bundles at the base of the leaf are collateral (Figs. 13,

14), the largest bundles always towards the adaxial side,

and the smaller towards the abaxial, both with phloem.

Vascular bundles of the middle portion and apex of the leaf

are also collateral (Fig. 12), with adaxial and abaxial

sclerenchyma. Sclerenchyma associated with the xylem is

more abundant than that associated with the phloem. In the

adaxial side, tissue arrangement from the epidermis

inwards is (1) fibers, (2) protoxylem, (3) metaxylem, (4)

phloem and (5) fibers (Fig. 12). In the abaxial side, from

the epidermis inwards the order is (1) fibers, (2) phloem

and (3) metaxylem (Figs. 8, 10, 11). In none of our prep-

arations did we find protoxylem in the abaxial side.

Fig. 14 Vascular bundles with incomplete fiber girders in a trans-

versal view of the mature basal portion of B. goldmanii (940)

Fig. 15 Leaf margin of B. gracilis at the leaf apex, with marginal

fibers (9400)

Fig. 16 Small marginal teeth of B. goldmanii, the teeth point towards

the apex (9594)

Fig. 17 Large marginal teeth of B. gracilis, the teeth point towards

the apex (9524)


123


Crystals

Styloids are very abundant in all the species, and are dis-

tributed in the chlorenchyma and the bundle sheath, but not

in the central cells that surround the vascular bundle.

Styloids can be aggregated and up to 6 per cell (Fig. 18) or

solitary and aligned (Fig. 19). Raphides were also present

in the mesophyll of B. compacta and B. inermis (Fig. 20).

Discussion

Characters with taxonomic value

Species can be recognized by a combination of characters

such as leaf shape in transverse section (grooved or

undulated), stomata (aggregated or solitary), size of the

marginal teeth, presence or absence of Convallaria type

waxes, and apex shape in young leaves.

Frolich and Barthlott (1988, cited by Bogler 1998)

demonstrated that Convallaria type waxes are present in the

four genera of the Nolinaceae (Beaucarnea, Calibanus,

Dasilyrion and Nolina), but the rosette crystalloid wax

(Barthlott et al. 1998) that we found in all Beaucarnea

species were described in Fabaceae and related families,

such as Connaraceae, Malpighiaceae, and even Asteraceae,

but not for monocotyledons. Barthlott et al. (1998) sug-

gested that size and complexity of the individual wax

rosettes might be more or less taxon specific, but in Beau-

carnea the usefulness of the character might be at the

generic level, since we found the crystalloids in all the

species, whereas Convallaria type waxes are present in B.

compacta, B. gracilis, B. hiriartiae, B. purpusii, B. re-

curvata, B. sanctomariana and B. stricta. Wax form and

disposition is independent of leaf shape (grooved or undu-

lated), or stomatal distribution (solitary or aggregated).

The species in sect. Papillatae (Trelease 1911) have

erect, rigid leaves with grooves and stomatal crypts with

more than four teeth (see Table 1; Fig. 1a–c). Trelease

(1911) included B. gracilis and B. stricta in this section,

but B. compacta and B. purpusii also belong to the section.

Trelease’s sect. Beaucarnea, which includes B. goldmanii,

B. guatemalensis, B. inermis, B. pliabilis and B. recurvata

with recurved, smooth leaves, have what we describe as

undulated surfaces (see Table 1). Beaucarnea hiriartiae

and B. sanctomariana, described after Trelease’s treatment

belong to this section. Since the generic subdivision is

based only on morphological and anatomical characters

that might be responding to climatic conditions, an inde-

pendent, molecular marker is needed to confirm the

subdivision.

Fig. 18 Aggregated styloids in the leaf parenchyma of B. hiriartiae

(9429)

Fig. 19 Solitary aligned styloids in the leaf parenchyma of B.

goldmanii (9902)

Fig. 20 A group of raphides in the leaf parenchyma of B. compacta

(91,970)


123


Beaucarnea inermis and B. recurvata are difficult to

differentiate in herbarium specimens, but have anatomical

characters that aid in their determination. B. inermis does

not have Convallaria type waxes, the cuticle is thin at the

leaf base (0.5 lm) and thickens towards the middle

(0.7 lm), and the apex is triangular. B. recurvata has

Convallaria-type epicuticular waxes, the cuticle is thicker

at the base (1.4 lm) and thins towards the middle of the

leaf (1 lm), and the apex is flat. B. purpusii and B. stricta

are difficult to distinguish based on anatomical characters,

and they seem to differ from each other only by the leaf

apex, which is concave in B. purpusii and flat in B. stricta.

The characters that allow the differentiation of B.

goldmanii from B. guatemalensis, two very similar species

from nearby areas, are the cuticular papillae on the fibers of

B. guatemalensis. Fibers of B. goldmanii lack such cutic-

ular papillae. Another difference is that B. goldmanii has

solitary stomata, whereas they are aggregated in B. gua-

temalensis. The differences are important to note, because

plants determined as B. guatemalensis are allegedly being

imported from Guatemala and commercialized in Mexico,

since the species is not in the Mexican legislation (NOM-

057, SEMARNAT 2010), but which are actually B.

goldmanii.

Character constancy

We found that cultivation induces some changes in the

anatomy of the plants. For example, leaf mesophyll is

thicker and extravascular bundles develop in the central

portion of the mesophyll. Marginal teeth are useful to

discriminate between B. gracilis, B. purpusii, and B. stricta

in sect. Papillatae, and for B. hiriartiae, B. recurvata, and

B. sanctomariana in sect. Beaucarnea, but they have to be

measured in young leaves from the central portion of the

rosette, since they are caducous in older leaves.

We provide the following key to differentiate sections

and species based on the growth form and leaf characters.

1. Leaves with grooved surfaces (sect. Papillatae).

2. Plants without elongated stems, leaf apex rounded.

B. compacta

2. Plants arborescent, leaf apex concave or flat.

3. Stems naked, leaf marginal teeth 136 lm

long. B. gracilis

3. Stems covered with the old, recurved leaves,

leaf marginal teeth 56–78 lm long.

4. Apex concave. B. purpusii

4. Apex flat. B. stricta

1. Leaves with undulated surfaces (sect. Beaucarnea).

5. Cuticle over the fibers covered with cuticular

papillae. B. guatemalensis

5. Cuticle over the fibers smooth.

6. Stomata solitary

7. Margin teeth ca 60 lm long. B. goldmanii

7. Margin teeth ca 100 lm long. B. pliabilis

6. Stomata aggregated

8. Leaf apex triangular. B. inermis

8. Leaf apex flat.

9. Margin teeth over 120 lm. B.

hiriartiae

9. Margin teeth ca 100 lm.

10. Stomatal density over 100/mm2.

B. sanctomariana

10. Stomatal density \50/mm2. B.

recurvata

Relationship to climate

All the species of Beaucarnea have leaves with an anatomy

characteristic for arid zones. They present cuticle, epicu-

ticular waxes, compact mesophyll, sunken stomata, and

dense fibers in girders. It is not possible to establish a clear

relationship in which the more xeromorphic species, with

grooved leaves and several cuticular teeth occupy the drier,

B-type climates (those in which evaporation exceeds pre-

cipitation, see Table 1). All the species grow in steep

slopes with shallow soils, as well as different altitudes.

Thus, plants must be responding to microclimatic condi-

tions, for which we lack information.

Acknowledgments Funding was provided by SINAREFI-SAGA-

RPA through the project ORN-PTA-10-6. Oliva Ramırez Segura

helped to process the histological samples, and Ana Lucıa Tovar

Alvarez the MEB preparations. Miguel Angel Perez Farrara collected

the samples of B. sanctomariana, and Celene Espadas aided in field

work of B. pliabilis. Maricela Gomez and Teresa Terrazas provided

valuable comments on earlier manuscript drafts. D. Bogler and J.

Mauseth carefully reviewed our manuscript. We are grateful to all of

them.

References

Baranova MA (1987) Historical development of the present classi-

fication of morphological types of stomates. Bot Rev 53:53–79

Barthlott W, Frolich D (1983) Mikromorphologie und Orientierungs-

muster epicuticularer Wachs-Kristalloide: Ein neues systematis-

ches Merkmal bei Monokotylen. Pl Syst Evol 142:171–185

Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I,

Wilkhelm H (1998) Classification and terminology of plant

epicuticular waxes. Bot J Linn Soc 126:237–260


123


Bogler D (1998) Nolinaceae. In: Kubitzki K (ed) The families and

genera of vascular plants. Springer, Berlin, pp 392–396

Chase MW, Reveal JL, Fay MF (2009) A subfamilial classification

for the expanded asparagalean families Amaryllidaceae, Aspar-

agaceae and Xanthorrhoeaceae. Bot J Linn Soc 161:132–136

Hernandez L (1992) Una especie nueva de Beaucarnea. Acta Bot

Mexicana 18:25–29

Hernandez L (1993) Beaucarnea >un genero amenazado? Cact Sucul

Mexicanas 38:11–14

Hernandez L et al (2012) Manejo y conservacion de las especies con

valor comercial de pata de elefante (Beaucarnea). Universidad

Autonoma de Queretaro, Queretaro

ImageJ (2014) http://rsbweb.nih.gov/ij/. Accessed 6 Feb 2014

Johansen DA (1940) Plant microtechnique. McGraw-Hill Book

Company, New York, London

Nakai (1943) Chosakuronbun Mokuroku [Ord. Fam. Trib. Nov.],

p 226

Peterson LR, Peterson CA, Melville LH (2008) Teaching plant

anatomy. NRC Press, Ottawa

Prychid C, Ruddal PJ (1999) Calcium oxalate crystals in monocot-

yledons: a review of their structure and systematics. Ann Bot

84:725–739

Ruzin SE (1999) Plant microtechnique and microscopy. Oxford

University Press, Oxford, New York, p 322

Schnell R (1967) Etudes sur l’anatomie et la morphologie des

Podostemecees. Candollea 22:157–272

SEMARNAT (2010) NORMA Oficial Mexicana NOM-059-SEMAR-

NAT-2010, Proteccion ambiental-Especies nativas de Mexico de

flora y fauna silvestres-Categorıas de riesgo y especificaciones

para su inclusion, exclusion o cambio-Lista de especies en

riesgo. Diario Oficial 30 de diciembre de 2010

Trelease W (1911) The desert group Nolineae. Proc Am Philos Soc

50:404–443


123


http://rsbweb.nih.gov/ij/

foliar anatomy of beaucarnea lemaire (nolinaceae ss)

Documents