the botanical review · bennettitales. leaf, stem, wood, and reproductive fragments are preserved...

CONTENTS i

Contents

Systematics, Ontogeny, and Phylogenetic Implications of Exceptional

Anatomically Preserved Cycadophyte Leaves from the Middle Jurassic

of Bearreraig Bay, Skye, Northwest Scotland

Beatrice L. Dower, Richard M. Bateman, and Dennis Wm. Stevenson . . . . . . . . . . 105

Two New Petrified Cycad Stems, Brunoa gen. nov. and Worsdellia

gen. nov., from the Cretaceous of Patagonia (Bajo de Santa Rosa,

Río Negro Province), Argentina

Analía E. Artabe, Alba B. Zamuner, and Dennis Wm. Stevenson . . . . . . . . . . . . . . 121

The Genus Cycas (Cycadaceae) in Vietnam

Ken D. Hill, Hiêp T. Nguyen, and Phan K. Loc . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134

Cycads of Colombia

Dennis Wm. Stevenson . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194

Range and Variation in the Genus Ceratozamia (Zamiaceae)

Loran M. Whitelock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235

Variation in the Mexican Cycad Dioon edule (Zamiaceae)

Loran M. Whitelock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240

Phylogeny of Encephalartos: Some Eastern Cape Species

P. Vorster, F. H. Van der Bank, M. Van der Bank, and M. Wink . . . . . . . . . . . . . . . 250

Molecular Systematic Studies in Cycads: Evidence from trnL Intron

and ITS2 rDNA Sequences

David J. Bogler and Javier Francisco-Ortega . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260

The World List of Cycads

Ken D. Hill, Dennis W. Stevenson, and Roy Osborne . . . . . . . . . . . . . . . . . . . . . . . 274

Spatial Distribution, Population Structure, and Fecundity of

Ceratozamia matudai Lundell (Zamiaceae) in El Triunfo

Biosphere Reserve, Chiapas, Mexico

Miguel Angel Pérez Farrera and Andrew P. Vovides . . . . . . . . . . . . . . . . . . . . . . . . 299

THE BOTANICAL REVIEW

VOL. 70 APRIL–JUNE 2004 NO. 2

Issued 00 August 2004

The Botanical Review 70(2): 105–311, April-June 2004

© 2004 The New York Botanical Garden

CYCADOPHYTES FROM SKYE 105



Copies of this issue [70(2)] may be purchased from the NYBG Press,

The New York Botanical Garden, Bronx, NY 10458-5126, U.S.A.;

[email protected]. Please inquire as to prices.

105

The Botanical Review 70(2): 105–120

Systematics, Ontogeny, and Phylogenetic Implications of

Exceptional Anatomically Preserved Cycadophyte Leaves from

the Middle Jurassic of Bearreraig Bay, Skye, Northwest Scotland

BEATRICE L. DOWER

Land Use Consultants

Glasgow, G12 8JJ, Scotland

RICHARD M. BATEMAN

Department of Botany

The Natural History Museum

London, SW7 5BD, England

AND

DENNIS WM. STEVENSON

New York Botanical Garden

Bronx, NY 10458, U.S.A.

I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106

III. Locality and Materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106

IV. Systematic Paleobotany . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107

V. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115

VI. Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118

VII. Literature Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118

I. Abstract

The Middle Jurassic (Aalenian-Bajocian) shallow marine deposits of Bearreraig Bay, Skye,

northwest Scotland, have yielded calcite-permineralized leaves of cycadophytes showing un-

usually well preserved anatomy. Morphological characters identify the leaves as Nilssonia cf.

tenuinervis Seward (Cycadales), Otozamites mortonii sp. nov. (Bennettitales), a putative juve-

nile leaf showing imbricate, recurved pinnae, and Otozamites sp. Permineralized Jurassic cyca-

dophytes occur in only four other localities worldwide; the better-known coeval adpression

flora of Yorkshire lacks anatomical preservation. Past studies of fossil cycadophyte species

have therefore emphasized morphology, whereas the Skye specimens reveal details of anatomy

greatly exceeding published descriptions of similar species. The arrangement of vascular

106 THE BOTANICAL REVIEW

tissues in the rachis of Otozamites resembles that described for Ptilophyllum cutchense Morris

(Bennettitales) from India. Stomata observed in the preserved cuticle of the Nilssonia leaf

superficially resemble those of the extant cycad Macrozamia Miquel. Given the 180 million

years separating these two genera, and the fragmentary preservation and equivocal phyloge-

netic position of Nilssonia, comparative interpretations remain tentative. Leaf characters have

been little used in phylogenetic analyses, reflecting exaggerated fears of anatomical and mor-

phological convergence; these characters therefore require particular attention when compar-

ing fossil cycadophytes with their living relatives.

II. Introduction

The Cycadales (early Permian to Present) and the Bennettitales (late Permian to late Creta-

ceous) are collectively known as the “cycadophytes,” as they show strikingly similar vegetative

morphology (e.g., Delevoryas, 1968, 1982; Pant, 1987; Stevenson, 1990; Norstog & Nicholls,

1997). They have strongly contrasting, distinct reproductive structures, however, the Bennettitales

being widely regarded as the relatively derived sister group to the angiosperm-gnetalean clade

(Doyle & Donoghue, 1986; Crane, 1988; Stewart & Rothwell, 1993; Taylor & Taylor, 1993).

The fossil record of cycadophyte leaves is dominated by adpressions that do not preserve inter-

nal anatomy, so that the few anatomically preserved Mesozoic floras provide especially impor-

tant insights. Well-known adpression floras include the Rhaetic flora of Scoresby Sound, east

Greenland (Harris, 1937), the Aalenian-Bajocian flora of Yorkshire (Harris, 1961, 1964, 1969),

the largely Kimmeridgian flora of the French Jura (Barale, 1981), and the Kimmeridgian flora

of Brora, Scotland (Seward, 1911; van Konijnenburg–van Cittert & van der Burgh, 1989).

Japan (Lower Jurassic: Kimura & Tsujii, 1982) and Mexico (Middle Jurassic: Person &

Delevoryas, 1982) have yielded floras geographically more distant from Skye. The only com-

parable three-dimensionally preserved Jurassic leaf flora occurs in the Rajmahal Hills of India

(Bose, 1953; Rao & Achuthan, 1967; Bose & Kasat, 1972a; Sukh-Dev & Zeba-Bano, 1975).

Among the adpression floras, those of Yorkshire, Oxfordshire, and Lincolnshire are closest to

Skye in both age and geography (Harris, 1964, 1969; Oldham, 1976).

Bearreraig Bay, on the east coast of Skye, northwest Scotland, has yielded an allochthonous,

shallow-marine assemblage of plant fragments showing relatively low species-level diversity

(Bateman & Morton, 1994; Bateman et al., 2000). About 15 organ species represent at least 11

whole-plant species from the Equisetales, Marattiales, Filicales, Coniferales, Cycadales, and

Bennettitales. Leaf, stem, wood, and reproductive fragments are preserved within calcite-rich

nodules, showing varying degrees of anatomical preservation.

This article focuses on the cycadophytes from Bearreraig. The material described consists

of a small number of substantial and remarkably well preserved leaf segments assigned to the

cycad Nilssonia cf. tenuinervis Seward and the bennettites Otozamites mortonii sp. nov. and

Otozamites sp.

III. Locality and Materials

The locality at Bearreraig Bay is situated on the east coast of the Isle of Skye, about 10 km

north of Portree on the Trotternish Peninsula. The cycad and bennettite fragments came from

several horizons in the section, extending from the top of the Dun Caan Shale Member to the

middle of the Holm Sandstone Member of the Bearreraig Sandstone Formation (Morton, 1984).

This represents about 10 my of deposition, spanning the well-documented Aalenian-Bajocian bound-

ary at the site. The flora was deposited 25–30 km offshore, in fully marine sediments accumulating

in the Middle Jurassic Hebrides Basin (Bateman et al., 2000). Decay and dissolution of abundant

PETRIFIED CYCAD STEMS FROM ARGENTINA 121






121


Two New Petrified Cycad Stems, Brunoa gen. nov. and Worsdellia

gen. nov., from the Cretaceous of Patagonia (Bajo de Santa Rosa,

Río Negro Province), Argentina

ANALÍA E. ARTABE,1 ALBA B. ZAMUNER,1 AND DENNIS WM. STEVENSON2

1División Paleobotánica

Facultad de Ciencias Naturales y Museo de La Plata

1900 La Plata, Argentina

2New York Botanical Garden,


I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121

III. Locality, Materials, and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122

IV. Systematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122

V. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130

VI. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132


I. Abstract

Polyxylic columnar stems covered by persistent leaf bases and found in sediments assign-

able to the Upper Cretaceous of Bajo de Santa Rosa, Río Negro Province, Argentina, are de-

scribed as two new generic entities in the Cycadales. Anatomical characters are the basis for

their being assigned to the Encephalartoideae of the Zamiaceae. Brunoa santarrosensis gen. et

sp. nov. is characterized by the presence of polyxyly, cone domes, mucilage cavities, and

uniseriate to triseriate araucaroid, scalariform, or bordered intervascular pitting. Worsdellia

bonettiae gen. et sp. nov. has polyxyly, anastomosing medullary vascular bundles, centripetal

xylem, mucilage canals, and concentric extraxylary bundles. Some characters (polyxyly, med-

ullary vascular bundles, and cone domes) were used to determine the systematic position, while

other characters (mucilage reservoirs and centripetal xylem) were used to establish the rela-

tionship between polyxylic and monoxylic forms.

II. Introduction

Cycadales are the most primitive order within gymnosperms with extant representatives.

The evolutionary history as known from fossils begins in the Upper Paleozoic (Mamay, 1969,

1976; Taylor, 1969; Zhu & Du, 1981) and reaches maximum distribution during the Mesozoic,

with decline beginning toward the end of the same period. Presently, Cycadales are a very well







134


The Genus Cycas (Cycadaceae) in Vietnam

KEN D. HILL

National Herbarium of New South Wales

Royal Botanic Gardens

Sydney 2000, Australia

HIÊP T. NGUYEN

Institute of Ecology and Biological Resources

Nghia Do, Cau Giay, Hanoi, Vietnam

AND

PHAN K. LOC

Department of Botany

University of Science, VNU

Thanh Xuan, Hanoi, Vietnam

I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135

III. Generic Concepts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135

IV. Species Concepts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136

V. Hybridism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136

VI. Conservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137

VII. Taxonomic Treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137

VIII. Species Known from China That May Be Expected to Occur in Vietnam . . . . . . . . 188

IX. Doubtful and Excluded Names . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190

X. Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191

XI. Literature Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191

I. Abstract

The genus Cycas is revised for Vietnam. Twenty-four species are enumerated, nine of them

described as new (C. aculeata, C. brachycantha, C. collina, C. condaoensis, C. pachypoda,

C. dolichophylla, C. fugax, C. hoabinhensis, and C. tropophylla). Descriptions of two Chinese

species known to occur close to the China-Vietnam border are also provided. A new combina-

tion is made for C. bifida (formerly C. rumphii var. bifida). The species are placed within an

infrageneric classification previously outlined. Distribution of all taxa is mapped, and a key to

species is provided. Illustrations are provided for new and poorly known taxa where adequate

CYCAS IN VIETNAM 135

material has been available. Previous reports of C. circinalis and C. rumphii from Vietnam are

discussed. Lectotypes are designated for C. balansae, C. chevalieri, and C. elongata, and a

neotype is designated for C. pectinata.

II. Introduction

The genus Cycas was first recorded from Vietnam by de Loureiro (1793), with his descrip-

tion of the new species Cycas inermis, based on collections he had made in Cochin China

(southern Vietnam) in 1787. Although the third species of Cycas to be described, C. inermis

has at no stage been properly understood. Since that date, eight additional taxa have been

described as new in the catalog of the flora of Vietnam. The first of these were C. tonkinensis

and C. bellefontii, described by Linden and Rodigas (1885, 1886). Both were described from

living plants in cultivation that had been collected in Tonkin (northern Vietnam), and no her-

barium material was preserved (see doubtful and excluded names below). Warburg described

C. balansae from near Hanoi in 1900, and Thiselton-Dyer described C. micholitzii from Annam

(central Vietnam–Laos) in 1905. Finally, Leandri described C. chevalieri from northern Viet-

nam and C. pectinata var. elongata from southern Vietnam in 1931. Taxa previously known

from other areas that have also been recorded from Vietnam are C. pectinata Buch.-Ham. and

C. siamensis Miq. The names C. circinalis L. and C. rumphii Miq. have at different times been

wrongly applied to Vietnamese taxa. Other names misapplied to plants from Vietnam have

been C. undulata and C. miquelii (see excluded names, below).

The comprehensive account of the genus by de Candolle (1868), recorded only Cycas inermis

from the region of Vietnam, largely on the basis of the notes published by de Loureiro. De

Candolle had also followed Miquel (1851) in misapplying the name C. inermis to specimens of

C. revoluta (see below). Pilger (1926) recorded only C. siamensis and C. micholitzii from

Vietnam. Schuster (1932) included C. tonkinensis in C. circinalis var. undulata, but also in-

cluded material of the C. rumphii complex from the Marianas, together with material from

Vietnam, in a confused concept. Schuster also recognized C. siamensis and C. micholitzii from

Vietnam, but then held C. inermis and the quite unrelated C. balansae as subspecies of

C. siamensis. Leandri (1931) had added C. immersa to the Vietnam catalog, and subsequently

Schuster correctly placed C. immersa in the synonymy of C. siamensis (in subsp. siamensis

sensu Schuster), although he included a number of unrelated species in the other subspecies he

erected within C. siamensis.

The regional account by Leandri (1931) listed 10 species occurring in Vietnam but misap-

plied the names Cycas circinalis, C. rumphii, and C. immersa. Ho and Duong (1960) recorded

only 7 species but again misapplied the three names above. Ho later (1991) added an eighth

species, C. inermis, again misapplying the above names and the latter name as well. Hiêp and

Vidal (1996) recorded 8 species, correctly placing C. immersa in the synonymy of C. siamensis

but otherwise followed the same misapplications (discussed below under relevant species).

More recent studies have gradually shown that the cycad flora of Vietnam is substantially

richer—in fact, probably the richest of the region (Hiêp & Loc, 1997, 1999).

III. Generic Concepts

The recently described genus Epicycas (de Laubenfels & Adema, 1998) is herein placed in

the synonymy of Cycas. When characters that are inconsistent are excluded, the new genus is

defined solely on the possession of a bulbous underground base. However, even this character

is neither wholly consistent within species nor restricted to the species placed in the new genus.

Moreover, of the species placed within the new genus, a number have what are clearly sister


Cycads of Colombia

DENNIS WM. STEVENSON



I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194

III. Cycadales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195

IV. Cycadaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196

V. Zamiaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197

VI. Phytogeography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230

A. Chocó and Montane Elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230

B. Río Magdalena Valley Element . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231

C. Amazonian Element . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231

VII. Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 232

VIII. Literature Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 232

I. Abstract

There are three genera of cycads in Colombia: Cycas, with two introduced and unnaturalized

species; the endemic genus Chigua, with two species; and Zamia, with 16 species, seven of

which are endemic. Keys to all species are given, as well as complete descriptions, synonymy,

types, exisiccatae, distributional data, and conservation status as used in the 1997 IUCN Red

List of Threatened Plants. Floristically, Zamiaceae is represented in Colombia by four ele-

ments: a Chocó, southern Córdoba, and northeastern Antioquia element, with the endemic

genus, Chigua, and six species of Zamia, Z. amplifolia, Z. disodon, Z. manicata, Z. roezlii,

Z. chigua, and Z. obliqua, with the first two endemic to Colombia; a montane element in the

northern Cordillera Occidental, with two endemic species, Z. montana and Z. wallisii; a Río

Magdalena Valley element, with Z. muricata, Z. poeppigiana, and the endemic Z. encephalar-

toides; and an element east of the Andes and principally Amazonian, with four other species,

Z. amazonum, Z. lecointei, Z. ulei, and the nearly endemic Z. hymenophyllidia.

II. Introduction

This treatment of the Cycads of Colombia is an English-language version of the Spanish-

language version that appeared in the Flora de Colombia (Stevenson, 2001). This treatment is

meant to complement those of Zamia for the Guianas (Stevenson, 1991), Panama (Stevenson,

1993), and Bolivia, Ecuador, and Peru (Stevenson, 2004) and to provide one of the bases for

the complete treatment of the new world cycads in Flora Neotropica. To date there has been no






194


RANGE AND VARIATION OF CERATOZAMIA 235






235


Range and Variation in the Genus Ceratozamia (Zamiaceae)

LORAN M. WHITELOCK

4524 Toland Way

Los Angeles, CA 90041, U.S.A.

I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235

III. Taxonomic History . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236

IV. Morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237

V. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 238

VI. Literature Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 238

I. Abstract

The genus Ceratozamia has an extensive distribution that starts in northeastern Mexico and

continues southward and southeastward into Guatemala, Belize, and Honduras. Over this ex-

tensive distributional range Ceratozamia is found in numerous disjunct populations. These

populations are never very widespread and are often restricted to a single mountain or canyon.

Because of the restricted range of these populations, and the lack of genetic exchange between

them, many of them have evolved into easily identifiable groups. At the present time there are

16 validly published species of Ceratozamia, with several more possible new species under

investigation.

II. Introduction

All 16 of the validly described species of Ceratozamia are from Mexico. This is not surpris-

ing, as Mexico is undeniably the center of diversity for this genus. The northernmost occur-

rence of Ceratozamia in Mexico is C. kuesteriana, from the state of Tamaulipas on Mexico’s

Gulf Coast, and the southernmost is C. matudae, from the Pacific slope of Chiapas. If we plot

the geographical distribution of Ceratozamia in Mexico (Fig. 1), we find that the northern

populations are generally restricted to the Sierra Madre Oriental and other mountain ranges on

the Gulf Coast. This distribution changes drastically just west of the Isthmus of Tehuantepec in

the states of Oaxaca and Veracruz. It is at this point that the distribution of Ceratozamia starts

its migration toward the Pacific Coast of Mexico and continues along this coast into the state of

Chiapas. East of Mexico the distribution of Ceratozamia continues into Guatemala, then north-

ward to Belize, and finally into central Honduras. At the present time Ceratozamia is not known

to occur west or south of Honduras.

The distribution of Ceratozamia as outlined above might pose questions as to why it is not

found in the Sierra Madre Occidental on Mexico’s west coast areas. These questions can be







240


Variation in the Mexican Cycad Dioon edule (Zamiaceae)

LORAN M. WHITELOCK

4524 Toland Way

Los Angeles, CA 90041, U.S.A.

I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240

III. Taxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240

IV. Distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241

V. Variation in Dioon edule . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241

VI. Forms of Dioon edule . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241

VII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 249


I. Abstract

The Mexican cycad Dioon edule with its two varieties, edule and angustifolium, range from

the states of Tamaulipas and Nuevo León in the north to the state of Veracruz in the south. The

variety angustifolium is restricted to the northern portions of the range, while the variety edule

is from the southernmost distribution in central Veracruz. Between the two varieties of Dioon

edule there are a number of disjunct colonies that exhibit variations that are undoubtedly the result

of an extended period of genetic isolation. These colonies display variation in the maximum size of

their stems, morphology and color of leaves and leaflets, distinctions in both male and female

cones, color of the sarcotesta, and size and shape of the sclerotesta. These differences are main-

tained even when specimens are grown in cultivation under identical conditions. Critical investi-

gations of these colonies may ultimately disclose the need for additional species descriptions.

II. Introduction

Dioon edule and its two varieties, edule and angustifolium, are restricted to the Sierra Madre

Oriental, with occasional colonies in hilly areas between the sierra and the Gulf of Mexico

(Fig. 28). Dioon edule and its varieties can be easily separated from all other species of Dioon

by the complete absence of spines on the leaflet margins. The only exception to this rule is that

marginal spines occur in Dioon edule on seedling or juvenile leaves. These spines are soon lost

as the plant matures.

III. Taxonomy

In the nineteenth century, descriptions of new species of Dioon were generally based only

on leaf and leaflet characteristics. Often new species descriptions were based on a single







250


Phylogeny of Encephalartos: Some Eastern Cape Species

P. VORSTER,1 F. H. VAN DER BANK,

2 M. VAN DER BANK,

2 AND M. WINK

3

1Botany Department

University of Stellenbosch

7602 Matieland, South Africa

2Department of Zoology

Rand Afrikaans University

2006 Auckland Park, South Africa

3Institut für Pharmazeutische Biologie

Universität Heidelberg

D-69120 Heidelberg, Germany

I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250

III. Aim . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251

IV. Material and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252

V. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252

VI. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252

VII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256


I. Abstract

A group of eight species of Encephalartos, comprising E. altensteinii, E. arenarius, E. horridus,

E. latifrons, E. lehmannii, E. longifolius, E. princeps, and E. trispinosus, from the Eastern Cape

Province of South Africa, was studied by analysis of iso-enzymes, ribosome DNA, and ITS 1 and

2 genes. The reason for this investigation was that the morphology of the vegetative and reproduc-

tive parts, though very distinctive in this geographical region, do not correlate, and it was hoped

that molecular data would elucidate evolutionary relationships. The three sets of molecular data

were found to agree to a remarkable degree. It was concluded that the vegetative morphology was

misleading but that the cone characteristics agree with molecular data and provide insight into the

interrelationships of these species. Thus, E. princeps was concluded to be relatively remotely re-

lated to the vegetatively similar E. lehmannii, and E. arenarius is not at all close to E. latifrons even

though the two species are easy to confuse when not in cone.

II. Introduction

The phylogeny of Encephalartos species has never been researched. While it is true that the

single scientific overview, albeit treating only the South African species (Dyer, 1965b), grouped







260


Molecular Systematic Studies in Cycads:

Evidence from trnL Intron and ITS2 rDNA Sequences

DAVID J. BOGLER AND JAVIER FRANCISCO–ORTEGA

Department of Biological Sciences

Florida International University

University Park

Miami, FL 33156, U.S.A.

(correspondence)

and

Fairchild Tropical Botanic Garden

Coral Gables, FL 33156, U.S.A.

I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261

III. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262

IV. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264

V. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266

A. Cycas Is Distantly Related to the Other Genera of Cycads . . . . . . . . . . . . . . . . . 267

B. Dioon Is Relatively Isolated and Contains Two Major Clades . . . . . . . . . . . . . . 268

C. Bowenia and Stangeria Are Not Closely Related . . . . . . . . . . . . . . . . . . . . . . . . . 268

D. Lepidozamia Is Closely Related to Encephalartos . . . . . . . . . . . . . . . . . . . . . . . . 269

E. Sequence Variation in Ceratozamia Is Very Low . . . . . . . . . . . . . . . . . . . . . . . . . 270

F. Microcycas and Zamia Are Closely Related . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270

G. Molecular Data Provide Useful Information about Species Relationships

in Zamia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270

VI. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271

VII. Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271


I. Abstract

The results of a pilot DNA sequencing study of cycads conducted at the new molecular

systematics laboratory at Fairchild Tropical Garden are presented and assessed with reference

to previous phylogenetic analyses and classification schemes based on morphology and anatomy.

Two DNA regions were sequenced and analyzed for variation, an intron in the trnL gene in the

chloroplast genome (trnL intron) and the internal transcribed spacer region between the 5.8S

and 26S ribosomal DNA subunits (ITS2). The trnL intron proved to be relatively conservative

among cycad genera, while the ITS2 region contained higher levels of variation. Parsimony

analysis of the sequences suggests a number of relationships, some of which were inferred by

previous morphological studies, some of which are new. The sequences of Cycas are the most

MOLECULAR SYSTEMATIC STUDIES IN CYCADS 261

divergent among cycads, suggesting the longest isolation. Dioon is relatively isolated from the

other genera and contains two major clades. Stangeria does not appear closely related to Bowenia

but does seem to have a weak affinity with Zamia and Microcycas. Lepidozamia is more closely

related to Encephalartos than to Macrozamia. Sequence variation among the species of

Ceratozamia is low. Microcycas and Zamia are closely related.

II. Introduction

Fairchild Tropical Botanic Garden has long been an important center for the study of cycad

biology. The extensive collections of cycads at Fairchild Tropical Garden and the associated

Montgomery Botanical Center are among the best in the world and have been utilized in a wide

variety of studies (Norstog, 1990; Norstog & Nicholls, 1997). Recently, a molecular systemat-

ics laboratory was jointly established between Florida International University and Fairchild

Tropical Botanic Center for the purpose of promoting studies of cycads, palms, and other

tropical plants. One of the first projects initiated in this new laboratory was a molecular system-

atics survey of cycads. Plans have been made for future, more extensive studies of molecular

variation in the New World cycads. In this article we report the results of a pilot study of

variation in trnL intron and ITS2 sequences in cycads.

Cycads are an ancient group of gymnosperms that were abundant and widely distributed during

the Mesozoic but are today much less common and largely confined to isolated tropical regions

(Norstog & Nicholls, 1997). The 11–12 genera of cycads currently recognized are thought to con-

stitute a monophyletic group classified as a single order, the Cycadales, which is divided into three

or four families (Johnson & Wilson, 1990; Stevenson, 1992). In these systems of classification,

Cycas is distinguished from the other genera by its leaflike, loosely arranged, multiovulate me-

gasporophylls, and it is placed in its own family, the Cycadaceae. Stangeria and Bowenia have

distinctive leaves and are grouped together in the family Stangeriaceae (Stevenson, 1992) or placed

in different families (Johnson & Wilson, 1990), but their precise affinities remain unsettled. The

rest of the genera are grouped into Zamiaceae. Efforts to resolve the phylogeny of cycad genera

more precisely using cladistic methods were made by Crane (1988), Stevenson (1990a), and

Schutzman and Dehgan (1993). Those analyses have stimulated discussion about character states

and evolutionary trends, but they differ in their results and conclusions. The formal classification

of cycads proposed by Stevenson (1992), based on cladistic analysis of morphological and ana-

tomical characters, serves as a useful point of reference and is shown in Fig. 1.

Molecular data have an advantage over morphological data in that they provide an almost

unlimited number of discrete characters with which to compare taxa and also usually present

fewer problems with homology assessment and character convergence (Hillis et al., 1996). One

of the first molecular systematic studies of cycads was made by Caputo et al. (1991), who

examined restriction fragment length polymorphisms (RFLPs) in the five genera of New World

cycads and Cycas, which was used as an outgroup. Parsimony analyses of these data indicated

that Dioon was the sister group to the other American genera, with Ceratozamia as the sister

group to a clade containing Microcycas, Zamia, and Chigua. As indicated by bootstrapping

support, these clades were strongly resolved, and the topology was congruent with the classifi-

cation based on morphological characters. The RFLP analysis was extended to include the Old

World genera (Caputo et al., 1993), but the results were at odds with classification based on

morphology (sensu Stevenson, 1990a), although removal of Macrozamia from the analysis

restored congruence. These studies demonstrated the potential utility of molecular markers for

resolving generic relationships in the cycads.

In the last ten years DNA sequence data have become easier to obtain and consequently

more widely used for reconstruction of plant phylogenies. In angiosperms the internal







274


The World List of Cycads

KEN D. HILL

Royal Botanic Gardens

Sydney 2000, Australia

DENNIS W. STEVENSON



AND

ROY OSBORNE

P. O. Box 244

Burpenary, Queensland 4505, Australia

I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 274

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 274

III. The World List . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 276

IV. Literature Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297

V. Appendix I: Useful Cycad References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297

I. Abstract

A list of the 305 currently recognized cycad species is given, along with citations of the

original place of publication and the location of type specimens when known. Included in the

list are currently recognized infraspecific taxa, brief geographical ranges, and a partial list of

synonyms for each taxon.

II. Introduction

The first “World List of Cycads” was published in Encephalartos (Journal of the Cycad

Society of South Africa) by Osborne and Hendricks (1985), with minor amendments in a supple-

mentary list in a subsequent issue of the same journal (Osborne & Hendricks, 1986). Several

updates have followed as changes in taxonomy and in outlook, especially in the genera Cycas,

Encephalartos, Macrozamia, and Zamia, made the previous lists obsolete, these being pre-

sented at the various International Conferences on Cycad Biology (Stevenson et al., 1990,

1995; Stevenson & Osborne, 1993a; Osborne et al., 1999) and elsewhere (Stevenson & Osborne,

POPULATION STRUCTURE OF CERATOZAMIA MATUDAI 299






299


Spatial Distribution, Population Structure, and Fecundity of

Ceratozamia matudai Lundell (Zamiaceae) in El Triunfo

Biosphere Reserve, Chiapas, Mexico

MIGUEL ANGEL PÉREZ FARRERA

Escuela de Biología

UNICACH

29000 Tuxtla Gutiérrez, Chiapas, Mexico

AND

ANDREW P. VOVIDES

Instituto de Ecología, A.C.

91000 Xalapa, Veracruz, Mexico

I. Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 299

II. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 300

A. Delimitation of Ceratozamia matudai . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 300

B. Conservation Status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301

III. Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301

A. Study Sites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301

B. Plots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301

IV. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303

A. Spatial Pattern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303

B. Population Structure and Density . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303

C. Growth Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 304

D. Fecundity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 305

V. Discussion and Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307

VI. Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 309


I. Abstract

We describe the spatial distribution, population structure, and fecundity of Ceratozamia

matudai in two populations in the El Triunfo Biosphere Reserve, in Chiapas, Mexico. Three

random plots of 20 × 20 m were laid out in a cypress forest habitat of the cycad and six plots in

a cloud forest habitat on Mount Ovando. The aggregated spatial pattern of C. matudai showed

a clumped local distribution on shallow soils on steep slopes. Individuals between the sites

showed differences in leaf production, trunk diameter, height, and growth pattern. A popula-

tion structure with an inverse “J” curve was obtained in both sites. Emergence of male and

the botanical review · bennettitales. leaf, stem, wood, and reproductive fragments are preserved...

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