5. C O N T E N TS
List of Contributors . vii
Preface . ix
1. Evolution and Systematics
Robert S. Wallace and Arthur C. Gibson . 1
2. Shoot Anatomy and Morphology
Teresa Terrazas Salgado and James D. Mauseth . 23
3. Root Structure and Function
Joseph G. Dubrovsky and Gretchen B. North . 41
4. Environmental Biology
Park S. Nobel and Edward G. Bobich . 57
5. Reproductive Biology
Eulogio Pimienta-Barrios and Rafael F. del Castillo . 75
6. Population and Community Ecology
Alfonso Valiente-Banuet and Héctor Godínez-Alvarez . 91
7. Consumption of Platyopuntias by Wild Vertebrates
Eric Mellink and Mónica E. Riojas-López . 109
8. Biodiversity and Conservation
Thomas H. Boyle and Edward F. Anderson . 125
9. Mesoamerican Domestication and Diffusion
Alejandro Casas and Giuseppe Barbera . 143
10. Cactus Pear Fruit Production
Paolo Inglese, Filadelfio Basile, and Mario Schirra . 163
11. Fruits of Vine and Columnar Cacti
Avinoam Nerd, Noemi Tel-Zur, and Yosef Mizrahi . 185
12. Forage, Fodder, and Animal Nutrition
Ali Nefzaoui and Hichem Ben Salem . 199
6. 13. Nopalitos, Mucilage, Fiber, and Cochineal
Carmen Sáenz-Hernández, Joel Corrales-Garcia,
and Gildardo Aquino-Pérez . 211
14. Insect Pests and Diseases
Helmuth G. Zimmermann and Giovanni Granata . 235
15. Breeding and Biotechnology
Brad Chapman, Candelario Mondragon Jacobo,
Ronald A. Bunch, and Andrew H. Paterson . 255
Index . 273
7. C O N T R I BU TO R S
Edward F. Anderson (Deceased), Desert Botanical Joel Corrales-Garca, Departamento de Ingeniería
Garden, Phoenix, Arizona Agroindustrial, Universidad Autónoma de Chapingo,
Mexico
Gildardo Aquino-Prez, Insituto de Recursos
Genéticos y Productividad, Montecillo, Mexico Rafael F. del Castillo, Centro Interdisciplinario
de Investigacíon para el Desarrollo Integral Regional
Giuseppe Barbera, Istituto di Coltivazioni Arboree, Unidad Oaxaca, Mexico
Università degli Studi di Palermo, Italy
Joseph G. Dubrovsky, Departamento de Biología
Filadelfio Basile, Dipartimento Scienze Economico- Molecular de Plantas, Instituto de Biotecnología,
Agrarie ed Estimativ, Universita degli Studi di Catania, Universidad Nacional Autónoma de México, Cuernavaca
Italy
Arthur C. Gibson, Department of Organismic
Hichem Ben Salem, Institut National de la Biology, Ecology and Evolution, University of
Recherche Agronomique de Tunisie, Laboratoire California, Los Angeles
de Nutrition Animale, Ariana, Tunisia
Hctor Godnez-Alvarez, Departamento de
Edward G. Bobich, Department of Organismic Ecología Funcional y Aplicada, Instituto de Ecología,
Biology, Ecology and Evolution, University of Universidad Nacional Autónoma de México, Mexico
California, Los Angeles City
Thomas H. Boyle, Department of Plant and Soil Giovanni Granata, Dipartimento di Scienze e
Sciences, University of Massachusetts, Amherst Technologie Fitosanitartie, Università degli Studi di
Catania, Italy
Ronald A. Bunch, D’Arrigo Bros. Co., Salinas,
California Paolo Inglese, Istituto di Coltivazioni Arboree,
Palermo, Italy
Alejandro Casas, Departamento de Ecología de los
Recursos Naturales, Instituto de Ecología, Universidad James D. Mauseth, Department of Integrative
Nacional Autónoma de México, Morelia Biology, University of Texas at Austin
Brad Chapman, Plant Genome Mapping Laboratory, Eric Mellink, Centro de Investigación Cientifica
University of Georgia, Athens y de Educación Superior de Ensenada, Mexico
vii
8. Yosef Mizrahi, Department of Life Sciences and Mnica E. Riojas-Lpez, Departamento de
Institutes for Applied Research, Ben-Gurion University Ecología, Centro Universitario de Ciencias Biológicas
of the Negev, Israel y Agropecuarias, Universidad de Guadalajara, Mexico
Candelario Mondragon Jacobo, Programa de Carmen Senz-Hernndez, Departamento de
Nopal y Frutales, Instituto Nacional de Investigaciones Agroindustria y Enología, Facultad de Ciencias Agrarias
Forestales y Agropecuarias, Queretaro, Mexico y Forestales, Universidad de Chile, Santiago
Ali Nefzaoui, Institut National de la Recherche Mario Schirra, Instituto per la Fisologia della
Agronomique de Tunisie, Laboratoire de Nutrition Maturazione e della Conservazione del Frutto delle
Animale, Ariana, Tunisia Specie Arboree Mediterranee, Oristano, Italy
Avinoam Nerd, Institutes for Applied Research, Noemi Tel-Zur, Department of Life Sciences,
Ben-Gurion University of the Negev, Israel Ben-Gurion University of the Negev, Israel
Park S. Nobel, Department of Organismic Biology, Teresa Terrazas Salgado, Programa de Botánica,
Ecology and Evolution, University of California, Los Colegio de Postgraduados, Montecillo, Mexico
Angeles
Alfonso Valiente-Banuet, Departamento de
Gretchen B. North, Department of Biology, Ecología Funcional y Aplicada, Instituto de Ecología,
Occidental College, Los Angeles, California Universidad Nacional Autónoma de México, Mexico
City
Andrew H. Paterson, Plant Genome Mapping
Laboratory, University of Georgia, Athens Robert S. Wallace, Department of Botany, Iowa
State University, Ames
Eulogio Pimienta-Barrios, Departamento de
Ecología, Centro Universitario de Ciencias Biológicas Helmuth G. Zimmermann, Plant Protection
y Ambientales, Universidad de Guadalajara, Mexico Research Institute, Agricultural Research Council,
Pretoria, South Africa
viii Contributors
9. P R E FAC E
The Cactaceae, a family of approximately 1,600 species, is and their uses. Twelve authors are from Mexico, eleven from
native to the New World but is cultivated worldwide. In re- the United States, five from Italy, three from Israel, two
sponse to extreme habitats, cacti have evolved special phys- from Tunisia, and one each from Chile and South Africa.
iological traits as well as distinctive appearances. The stem Most of the authors share my interests in basic research on
morphology, spine properties, and often spectacular flowers the Cactaceae. Nearly half of the authors, especially those
have caused hobbyists to collect and cultivate large numbers dealing with agronomic aspects, are involved with the
of cacti. Both cactus form and function relate to nocturnal CactusNet sponsored by the Food and Agricultural Orga-
stomatal opening and Crassulacean acid metabolism, which nization of the United Nations. Approximately 1,300 refer-
lead to efficient use of limited soil water. Thus, cacti can ences are cited in the chapters, which not only indicate the
thrive in arid and semiarid environments, where they are widespread interest in cacti but also should facilitate further
often important resources for both wildlife and humans. investigations. The intended audience ranges from ecolo-
Indeed, cacti have been consumed by humans for more gists and environmentalists to agriculturalists and con-
than 9,000 years. Currently, Opuntia ficus-indica is culti- sumers to cactus hobbyists and enthusiasts.
vated in over 20 countries for its fruit, and an even greater The point of departure is the evolution of the family in
land area is devoted to its cultivation for forage and fodder. the broad sense, paying particular attention to new mo-
The fruits of other cactus species, known as pitahayas and lecular and genetic approaches (Chapter 1). People recog-
pitayas, and various other cactus products are appearing in nize cacti by their shoot morphology, which reflects vari-
an increasing number of markets worldwide. ous cellular characteristics (Chapter 2). The uptake of
Due to the high water-use efficiency and other adapta- water and nutrients from the soil by roots that sustains the
tions of cacti, biological and agronomic interest in them has shoots has unique features as well (Chapter 3). Survival de-
soared. From 1998 to 2000, more than 600 researchers pub- pends on adaptation to abiotic environmental conditions,
lished over 1,100 articles on cacti, including papers in pro- which cacti have done in special ways (Chapter 4). In ad-
ceedings of national and international meetings. Yet a cur- dition to enduring harsh conditions, cacti must reproduce,
rent, synthetic, widely ranging reference is not available. for which many strategies have evolved (Chapter 5). Biotic
This book, which consists of a series of authoritative, up-to- factors are also crucial for the success of cacti in natural en-
date, review chapters written by established experts as well vironments (Chapter 6). Because of their ecological suc-
as new contributors, emphasizes both the biology of cacti cess, cacti are important food resources for wild vertebrates
ix
10. (Chapter 7). The many unique characteristics of the De la Barrera assisted with the many Spanish citations.
Cactaceae have attracted collectors and raised concerns Marian McKenna Olivas competently did line editing, and
about issues of biodiversity and conservation (Chapter 8) Alicia Materi meticulously typed the developmental and
as well as led to their ancient usage and subsequent wide line editing changes. Financial support for these steps was
diffusion by humans (Chapter 9). The most widespread provided by Sol Leshin, a man of integrity and generosity
use occurs for fruits of platyopuntias, known as cactus with a profound interest in plants and their uses dating
pears (Chapter 10). Also, fruits of vine-like and columnar back to his M.S. in soil science in 1938. Numerous sugges-
cacti are increasingly popular in many countries (Chapter tions on improving the arrangement and scientific content
11). An even greater land area worldwide than is used for were the result of a graduate course taught from the book
cactus fruits is devoted to raising platyopuntias for forage and attended by Edward Bobich, Erick De la Barrera, C. J.
and fodder (Chapter 12). Besides such uses, cacti are also Fotheringham, Catherine Kleier, and Alexandra Reich.
important as a vegetable, as a dietary supplement, and as The dedication and important suggestions of these people
the host for the red-dye-producing cochineal (Chapter 13). helped meld the contributions of a diverse group of au-
Such uses, which are constrained by pests and diseases thors into the final product, for which I am extremely
(Chapter 14), are currently expanding via breeding and grateful.
biotechnology (Chapter 15). Park S. Nobel
Special thanks are due to those who helped in the re- February 10, 2001
alization of this book. Edward Bobich helped prepare the
line drawings and halftones for reproduction, and Erick
x Preface
11. CHAPTER
›1‹
EVO LU T I O N A N D S Y S T E M AT I C S
Robert S. Wallace and Arthur C. Gibson
Introduction
Phylogenetic Placement of Cactaceae
Cactaceae, a Family of Order Caryophyllales
Classification of Cactaceae within Suborder Portulacineae
Cactaceae, a Monophyletic Family
Defining Subfamilies of Cactaceae
Transitions from Structural Analyses to Molecular Systematics
Molecular Systematics of Cactoideae
Identifying the Oldest Taxa
Epiphytic Cacti
Columnar Cactus Lineages
Cacteae and Notocacteae
Solving Classification Problems Using Molecular Techniques
Phylogenetic Studies of Subfamily Opuntioideae
New Insights into Cactus Evolution
Structural Properties
Revised Biogeographic Models Based on Molecular Studies
Concluding Remarks
Literature Cited
1973; Barthlott 1983). These usually spiny organisms (Fig.
Introduction 1.1) are loved by plant fanciers for their diverse forms and
The Cactaceae is one of the most popular, easily recogniz- showy flowers. Nearly every introductory college biology
able, and morphologically distinct families of plants, and or ecology textbook contains at least one cactus photo-
it includes approximately 1,600 species (Gibson and Nobel graph, used to illustrate plant adaptation to dry habitats.
1986; Barthlott and Hunt 1993). Cacti occur in the New Important commercial products are derived from cacti
World from western and southern Canada (Speirs 1982) (Nobel 1994, 1998). Cacti have also helped evolutionary bi-
to southern Patagonia in Chile and Argentina (Kiesling ologists and ecologists understand CAM (Crassulacean
1988), and the epiphytic genus Rhipsalis has dispersed nat- acid metabolism) and succulence (Gibson and Nobel
urally, undoubtedly by birds, to tropical Africa and Mada- 1986; Nobel 1988, 1991).Funeahere:
gr r
i1
e
.
gascar and across to Sri Lanka and southern India (Thorne In some plant families, it is merely a matter of con-
1
12. Figure 1.1. The vegetative plant of Coryphantha bumamma (Ehrenberg) Brittton and Rose (tribe Cacteae), a low-growing spherical cactus from
Guerrero, Mexico.
venience to have correct names for plant species. In the order share derived characters, i.e., synapomorphies, that
Cactaceae, however, there is not only a huge demand for do not occur in any other angiospermous order. One struc-
correct names and precise classification into genera, but tural synapomorphy, and the first recognized feature for re-
also a critical need for a phylogenetic classification because lating these families, is that the seed contains a strongly
there are many subjects, some of which are covered in this curved, peripheral embryo around a central nutritive
book, that depend on having an accurate evolutionary re- perisperm, not endosperm. From that observation arose
construction of cactus history. the ordinal name Centrospermae (Eichler 1878). A chem-
ical synapomorphy is the occurrence of betalains, a class of
Phylogenetic Placement of Cactaceae nitrogenous pigments derived from tyrosine (Mabry 1964;
Clements et al. 1994). The Cactaceae and closely related
Cactaceae, a Family of Order Caryophyllales
families form a proteinaceous plastid inclusion (designat-
Family Cactaceae is assigned to order Caryophyllales, ed as type P3cf ) during the ontogeny of sieve-tube mem-
which includes, among others, ice plants (Aizoaceae), bers (Behnke 1976a,b, 1994). Congruence of the three
portulacas (Portulacaceae), carnations (Caryophyllaceae), mentioned unlinked and unique synapomorphic charac-
bougainvilleas (Nyctaginaceae), pokeweeds (Phytolac- ters in these same families, not in others, formed a solid
caceae), amaranths (Amaranthaceae), and saltbushes case for recognizing this monophyletic clade.
(Chenopodiaceae). The taxonomic history of classifying Order Caryophyllales, which was established by ana-
Cactaceae within this order has been adequately reviewed lyzing certain types of structural and chemical data, was
(Cronquist and Thorne 1994), and there is universal ac- tested with a new data set using chloroplast DNA (cpDNA)
ceptance that cacti are core members of Caryophyllales. restriction site mutations, and was confirmed by the loss
Phylogenetic placement within the Caryophyllales is of the rpl2 intron in the common ancestor of the order
undisputed, because cacti and other families within the (Downie and Palmer 1994). Indeed, investigators use
2 Wallace and Gibson
13. whatever data are available at the time to formulate an ini- Talinum and Portulaca (Fig. 1.2; Appleqvist and Wallace
tial hypothesis, and later test the model using an indis- 2001). In future systematic studies of the family, these se-
putable data set of a totally different nature that provides quence data will play an important role in redefining the
resolution. Yet there are still some unresolved issues con- family Portulacaceae, as well as the evolutionarily distinct
cerning the composition of Caryophyllales and whether groups it now contains, and how the evolutionary com-
other families, shown by molecular studies to share closest ponents of this diverse clade need to be circumscribed. :ehrn2.1 egi
ra u
e e rF
DNA affinities to Caryophyllales, should be classified
within the order (Angiosperm Phylogeny Group 1998). Cactaceae, a Monophyletic Family
Among these are the insectivorous sundews (Droseraceae) Even casual students of cacti can recognize the repetitive
and pitcher plants of Nepenthaceae. It is unclear at this vegetative design within this plant family (Gibson and
time whether molecular data will require these nontradi- Nobel 1986). Typically, a cactus possesses a perennial pho-
tional members to be classified within the order or instead tosynthetic succulent stem, bearing leaf spines produced on
as allies in one or more separate orders. Regardless of that modified axillary buds, termed areoles, but lacking broad
outcome, placement of family Cactaceae is unaffected for green leaves. The colorful flower of the typical cactus has
the time being. many separate perianth parts, numerous stamens, and an in-
ferior ovary with many ovules and parietal placentation. The
Classification of Cactaceae within Suborder Portulacineae fruit is a many-seeded berry, often juicy but in some taxa be-
Phylogenetic relationships of the Cactaceae within the coming dry or splitting open at maturity. There are, of
Caryophyllales have been much more difficult to deter- course, exceptional forms: (1) spineless plants (e.g., certain
mine. Investigators have been interested in determining to epiphytes such as Disocactus and Epiphyllum and small cacti
which of the betalain-containing families Cactaceae is phy- such as Lophophora and Ariocarpus); (2) geophytes with an-
logenetically most closely related. Traditional comparative nual above-ground shoots (e.g., Pterocactus kuntzei, Opuntia
and developmental evidence favored the Aizoaceae (Turner chaffeyi, and Peniocereus striatus); (3) primitive cacti that
1973; Rodman et al. 1984) or Phytolaccaceae (Buxbaum have relatively broad, dorsiventrally flattened leaves (e.g.,
1953; Cronquist 1981), emphasizing floral features. More re- Pereskia spp. and Pereskiopsis porteri); (4) plants that have
cent analyses claimed that the Cactaceae has most recent relatively small flowers with fewer parts (e.g., small-flowered
ancestry with the Portulacaceae (Thorne 1983; Gibson and species of Rhipsalis, Pseudorhipsalis, and Uebelmannia spp.);
Nobel 1986; Hershkovitz 1991; Gibson 1994), within what and (5) superior ovaries with axile placentation (e.g., Pereskia
became called suborder Portulacineae Thorne (Cronquist sacharosa). None of these exceptions is troubling, because all
and Thorne 1994), which included Cactaceae, Portula- are well-accepted members of the family and understood as
caceae, Didiereaceae, and Basellaceae. representing either primitive or highly reduced, apomorphic
New data sets from gene sequence experiments tested (derived) states of cactus features.
the model and strongly supported Portulacineae as a The morphological distinctiveness and monophyly of
monophyletic taxon that includes Cactaceae (Manhart and family Cactaceae have been further supported conclusive-
Rettig 1994). Cactaceae and certain Portulacaceae are sis- ly with molecular data. There has occurred a 6 kb inversion
ter taxa sharing a 500 base-pair (bp) deletion in the in the large single copy region of the plastid genome (rel-
Rubisco gene rbcL (Rettig et al. 1992; Downie and Palmer ative to the consensus land plant gene order seen in
1994). Using a 1,100 bp sequence of open reading frame in Nicotiana tabacum; Downie and Palmer 1993) that involves
cpDNA, the largest gene in the chloroplast genome, the genes atpE, atpB, and rbcL. This cpDNA inversion has
Downie et al. (1997) concluded again that Pereskia (Cacta- been found in all cacti sampled, so this is an excellent
ceae) belongs in the portulacaceous cohort. With internal molecular synapomorphy for defining Cactaceae (Wallace
transcribed spacer sequences of cpDNA, Hershkovitz and 1995; Wallace and Forquer 1995; Wallace and Cota 1996;
Zimmer (1997) obtained results that placed the primitive Cota and Wallace 1996, 1997). Remarkably, an identical in-
leaf-bearing cacti phylogenetically nested within the version of the same cpDNA region occurs independently
Portulacaceae, and the Cactaceae was identified as the sis- in another caryophyllalean lineage, the Chenopodiaceae
ter taxon of a clade that includes species of Talinum. In a (Downie and Palmer 1993). Nonetheless, because cacti
more intensive cpDNA analysis of the portulacaceous co- consistently exhibit this 6 kb inversion, molecular system-
hort, using gene sequence data of ndhF, a recent study has atists infer that Cactaceae are monophyletic, i.e., traceable
shown that the Cactaceae is indeed nested within the back to a single ancestral population in which the inversion
Portulacaceae sensu lato and is most closely related to appeared and then became genetically fixed. What remains
Evolution and Systematics 3
14. Amaranthus palmeri
AMARANTHACEAE
A. quitensis
Mollugo verticillata MOLLUGINACEAE
Allionia violacea
Mirabilis jalapa NYCTAGINACEAE
Bougainvillea sp.
Phytolacca acinosa PHYTOLACCACEAE
Aptenia cordifolia
AIZOACEAE
Tetragonia tetragonioides
Talinum paniculatum
T. angustissimum
T. caffrum
T. triangulare
Talinella pachypoda
Anacampseros retusa
Grahamia bracteata
Talinopsis frutescens
Portulaca grandiflora
P. mundula
P. molokiniensis
P. oleracea
Maihuenia poeppigii
Pereskia aculeata CACTACEAE
Quiabentia verticillata
Montia perfoliata
Claytonia virginica
Montia diffusa
M. parvifolia
Lewisia pygmaea
Calandrinia volubilis
C. ciliata var. menziesii
C. compressa
Montiopsis umbellata
M. berteroana
M. cumingii
Cistanthe grandiflora
C. mucronulata
C. guadalupensis
Calyptridium umbellatum
Talinum mengesii
Alluaudia humbertii
DIDIEREACEAE
Didierea trollii
Calyptrotheca somalensis
Ceraria fruticulosa
Portulacaria afra
Basella alba
BASELLACEAE
Ullucus tuberosus
Figure 1.2. Strict consensus tree of equally parsimonious trees from analysis of the ndhF gene sequence for the portulacaceous alliance,
which includes Cactaceae, Portulacaceae, Didiereaceae, and Basellaceae (after Appleqvist and Wallace 2000).
15. unresolved is whether investigators eventually will recog- sesses a minute, often microscopic, upper leaf (Oberblatt)
nize more than one family of the cacti for this evolution- subtending each areole (Boke 1944). This contrasts with
ary branch. Opuntioideae, in which the leaf is usually small, terete,
succulent, and easily discernible to the unaided eye. In
Defining Subfamilies of Cactaceae most species of the subfamily, stems of Cactoideae have
All recent familial classifications of Cactaceae have recog- ribs (tubercles and areoles are arranged in a vertical series),
nized three major clades, most commonly classified as sub- but this cannot qualify as a synapomorphy and would ig-
families: Pereskioideae, Opuntioideae, and Cactoideae nore the presence of stem ribs of certain Opuntioideae, es-
(Hunt and Taylor 1986, 1990; Gibson and Nobel 1986; pecially corynopuntias (Grusonia). Nonetheless, among ex-
Barthlott 1988; Barthlott and Hunt 1993). Each subfamily tant cacti, there are no apparent morphological stages
is distinguished by structural criteria, for which there are linking the leafy, nonsucculent, aerole-bearing shoots of
relatively clear discontinuities among these three clades. Pereskia to any of the suggested primitive ribbed forms of
Subfamily Pereskioideae has been defined essentially as Cactoideae. Other features that clearly differentiate be-
the pool of extant cacti with the primitive vegetative and tween leafy pereskias and plesiomorphic Cactoideae, such
reproductive features (Buxbaum 1950; Boke 1954; Bailey as an outer stem cortex consisting of multiseriate hypo-
1960; Gibson 1976; Gibson and Nobel 1986). As tradi- dermis, are also found in Opuntioideae.
tionally defined, this subfamily has no known structural New evidence to evaluate the commonly used subfa-
synapomorphy (Barthlott and Hunt 1993). Two genera milial classification of Cactaceae comes from analyses of
have been assigned to this subfamily: Pereskia (16 spp.; cpDNA structural arrangements of the chloroplast genome
Leuenberger 1986) and the Patagonian Maihuenia (2 spp.; adjacent to the region of the rbcL gene and comparative se-
Gibson 1977b; Leuenberger 1997). The broad-leaved quencing of a number of plastid coding and noncoding se-
shrubs and trees of Pereskia and small-leaved, mound- quences. Opuntioideae are clearly demarcated molecular-
forming plants of Maihuenia have totally different external ly by the deletion of the gene accD (ORF 512) in the plastid
vegetative morphology and anatomy but share some ple- genome (Wallace 1995). All Cactoideae examined to date
siomorphic (primitive) reproductive features (Buxbaum have a different deletion at the 5' end of the accD region
1953). Vegetative morphology of Maihuenia grades into and have lost the intron to the plastid gene rpoC1, a dele-
low-growth forms of Opuntioideae. In fact, both species of tion of approximately 740 bp, which supports a common
Maihuenia were originally described as species of Opuntia ancestry for all members of this subfamily (Wallace 1995;
(Leuenberger 1997). Wallace and Cota 1996). The clades defined by these struc-
Subfamily Opuntioideae is the most easily defined by tural rearrangements are further supported by phylogenies
its structural synapomorphies: (1) areoles have glochids, determined from comparative sequencing.
i.e., very short and fine deciduous leaf spines that have Unfortunately, a unique genetic synapomorphy has
retrorse barbs and are easily dislodged; (2) every cell com- not yet been discovered for subfamily Pereskioideae, as pre-
prising the outer cortical layer of the stem possesses a large viously circumscribed, but Pereskia and Maihuenia are
druse, i.e., an aggregate crystal of calcium oxalate (Bailey themselves divergent because they have not been found to
1964; Gibson and Nobel 1986); (3) pollen grains are poly- share restriction site changes, although many occur
porate and possess peculiar microscopic exine features uniquely as synapomorphies for each genus (Wallace 1995).
(Leuenberger 1976); (4) the seed is surrounded by a funic- In fact, nucleotide sequencing data now demonstrate that
ular envelope, often described as being an aril; and (5) spe- Pereskia and Maihuenia are as divergent from one another
cial tracheids occurring in secondary xylem (wide-band as either is from Opuntioideae and Cactoideae.
tracheids of Mauseth 1993a, 1995; vascular tracheids of Wallace (2002) used nucleotide sequence data as
Bailey 1964, 1966 and Gibson 1977a, 1978) possess only justification to propose recognizing a fourth subfamily,
annular secondary thickenings (Gibson and Nobel 1986). Maihuenioideae. When recognized as a separate subfami-
Other distinguishing features could be listed but are not ly, Maihuenioideae have distinctive structural synapomor-
true synapomorphies, i.e., derived character states within phies, including curious anatomical features within leaves
the family. not known to occur elsewhere in Cactaceae (Gibson
Subfamily Cactoideae is less easily delimited by syn- 1977b; Leuenberger 1997). Wood features of Maihuenia are
apomorphies. In fact, probably only one general form ap- also diagnostic to a specialist (Gibson 1977b), although all
plies to all genera: namely, the stem is succulent and pos- the cell types found in Maihuenia, including the special
Evolution and Systematics 5
16. spindle-shaped tracheids with helical secondary thicken- Needed is a technique that is independent of structure,
ings, are also observed within other members of Cac- where cases of parallelism and convergence can be clearly
toideae that have small growth forms (Gibson 1973; Gibson recognized so that each species can be inserted into its
and Nobel 1986; Mauseth 1995; Mauseth et al. 1995; proper phylogenetic lineage. Application of molecular
Mauseth and Plemons 1995). systematic techniques to address these issues provides a
The proposal by Wallace to recognize subfamily fresh look at old problems. The goal of modern plant sys-
Maihuenioideae was discussed openly for five years in de- tematics is to obtain, for each family, an entirely new and
liberations and correspondence with Cactaceae specialists potentially unbiased data set in which to test all presumed
of the International Organization for Succulent Plant classifications.
Study (IOS). The Cactaceae Working Party of the IOS
concentrated its efforts on clarifying infrafamilial relation- Molecular Systematics of Cactoideae
ships among species and genera and stabilizing nomencla- As of January 1, 2000, sequences for several plastid DNA
ture for the cactus family, in order to make informed de- regions (rbcL, rpl16 intron, trnL-F intergenic spacer, ndhF)
cisions about revising its classification. This procedure, not for representative taxa within the Cactaceae have been
protected by the current international code of nomencla- completed at Iowa State University (R. S. Wallace and
ture, should become an accepted practice of the systemat- coworkers) and form the framework for phylogenetic com-
ic community, instead of using preliminary publications to parisons of the various evolutionarily related groups with-
justify scientific decisions. It may also become a standard in the family. Genomic DNA samples have been isolated
practice in the future to include molecular systematic stud- from photosynthetic stems (and leaves, when available)
ies or cladistic analyses of morphological or molecular data representing all key species groups, including currently rec-
as part of publishing a new plant species. In this regard, full ognized genera, infrageneric taxa, and morphologically
subfamilial diagnoses can be found for the Opuntioideae anomalous species for which assignment to a genus has
and Cactoideae in Barthlott and Hunt (1993), for the been problematic. From the relatively small sample studied,
Maihuenioideae in Wallace (2002, after Leuenberger 1997), many systematic tangles are becoming unraveled each
and for the Pereskioideae, based on the diagnosis of time new groups are carefully sampled and analyzed. Even
Pereskia in Leuenberger (1986). so, Cactaceae must be more thoroughly subsampled, and
the task of processing hundreds of species is time consum-
Transitions from Structural Analyses to ing. Fortunately, molecular studies are no longer as costly
Molecular Systematics as they were a decade ago, due to advances in sequencing
The 250-year history of cactus taxonomy and systematics, technology. As the various evolutionary groups within the
as in all plant families, was dominated by the use of struc- Cactaceae are sampled more intensively, more robust phy-
tural characters to assign species to genera. Unfortunately, logenies will emerge to provide a more certain assessment
examples of evolutionary convergence and parallelism in of relationships within and among the subfamilies, tribes,
cactus structure are commonly observed (Table 1.1). These and genera that constitute the family.
include reversals in character states and neoteny, i.e., re- Results from future studies of molecular variation
versals to juvenile features. Losses of distinguishing taxon- likely will be, as they have already been, very illuminating
specific features are certainly commonplace in this family, in Cactaceae. New data can also be somewhat disturbing
in which plant habit, stem morphology, stem anatomy, and in cases where it is learned how incorrect some previous
flower characters have been targets of natural selection taxonomic placements were. These earlier classifications
(Buxbaum 1950, 1953; Gibson 1973; Gibson and Nobel mislead cactus systematists in attempts at classifying the
1986; Barthlott and Hunt 1993; Cornejo and Simpson family and establishing scenarios for its evolutionary
1997). What now worries cactus systematists are the un- changes. Findings from molecular studies have shown how
recognized cases of parallel evolution still hidden among difficult it is to estimate affinities among cacti by using
the genera, where a feature has been relied on as being con- only external or internal structural features. In practice, a
servative but now is discovered not to be. Experts of a combination of molecular and morphological data will
group can sharply disagree on assigning a species to one serve to provide the best estimate of phylogeny within the
genus or another based on one individual emphasizing Cactaceae and will assist taxonomists in producing a
seed characters, one flowers, and another areoles or inter- classification that incorporates evolutionary relationships
nal anatomy. One of these characters—or none—may hold in its hierarchies, while establishing a usable and practical
the key to its real phylogeny, but which one?Tb.1eleahere:
ar
n classification.
6 Wallace and Gibson
17. TA B L E 1 . 1
Examples of parallel and convergent evolution of features within Cactaceae, using examples from North and South America
Taxon
Feature North America South America
Growth habit and wood anatomy
Creeping (procumbent) columnar Stenocereus eruca Echinopsis coquimbanus
Living rocks Ariocarpus fissuratus Neoporteria glabrescens
Lophophora williamsii Oreocereus madisorianus
Massive barrel Echinocactus ingens Eriosyce ceratistes
Cylindrical barrel Ferocactus wislizenii Denmoza rhodacantha
Astrophytum myriostigma Copiapoa cinerea
Two-ribbed epiphyte Disocactus biformis Rhipsalis rhombea
Resupinate epiphyte Selenicereus testudo Pseudorhipsalis amazonicus
Lateral cephalium Cephalocereus senilis Espostoa lanata
Epidermal papillae on green stem Peniocereus marianus Pterocactus kuntzei
Opuntia pilifera Tephrocactus auriculatus
Tubular red, hummingbird-
pollinated flowers
Shrubs Stenocereus alamosensis Cleistocactus strausii
Epiphytes Disocactus macdougallii Schlumbergera truncata
Hummingbird flowers with
red to brown pollen Echinocereus triglochidiatus Cleistocactus brookei
Mammillaria poselgeri Denmoza rhodacantha
Hawkmoth flowers, white, nocturnal
with long tube Epiphyllum phyllanthus Selenicereus wittii
Very small flowers Pseudorhipsalis spp. Rhipsalis spp.
More than one flower per areole Myrtillocactus cochal Pseudorhipsalis amazonicus
Dark, glandular areolar trichomes Stenocereus thurberi Pilosocereus aurisetum
Hydrochorous (floating) seeds with
large hilum cup Astrophytum capricorne Frailea phenodisca
Small seeds with large arillate strophiole Strombocactus disciformis Blossfeldia liliputana
Mescaline Lophophora williamsii Echinopsis pachenoi
Stenocereus eruca
Large calcium oxalate druses in
outer cortex of stem Opuntia basilaris Monvillea spegazzini
Aztekium ritteri
References: Buxbaum (1950, 1955); Gibson (1973, 1988a,b); Rowley (1976); Bregman (1988, 1992); Rose and Barthlott
(1994); Zappi (1994); Barthlott and Porembski (1996); Porembski (1996); Barthlott et al. (1997).
obvious with such leafy forms in the genera Pereskiopsis,
Identifying the Oldest Taxa Quiabentia, or Austrocylindropuntia. However, for subfam-
When doing any type of contemporary phylogenetic analy- ily Cactoideae and each of its tribes, making an a priori
sis, the researcher must include at least one species that has choice of taxa to best represent the primitive species has been
the presumed primitive features of the group being studied. a field of great speculation and, until now, selecting the
For Cactaceae as a whole, this has been easy because the leaf- primitive taxon has been a subjective process. Often, species
bearing species of Pereskia and Maihuenia are undisputed possessing primitive features are not the ones widely culti-
choices, and they are then assumed to have retained impor- vated or readily available; these groups typically inhabit in-
tant plesiomorphic morphological or sequence characters for accessible localities or sites where collection is not frequent
phylogenetic analyses. For Opuntioideae also, the choice is and are usually incompletely described.
Evolution and Systematics 7
18. Buxbaum (1950) proposed that the primitive cereoid molecular studies will continue to elucidate the positions
cactus would logically be one that had a woody form like a of the most primitive members of the Cactoideae and will
typical dicotyledon and relatively few ribs, e.g., in cer- add more systematic information to evaluate the position
tain species of Leptocereus. Later, the tribe Leptocereeae of Calymmanthium and its placement as the basal lineage
(Buxbaum 1958) was often used as a taxonomic category to of the subfamily.
include cereoids having primitive vegetative and repro-
ductive features. Out of that assemblage has emerged Epiphytic Cacti
Calymmanthium substerile Ritter from northern Peru, Nearly 130 epiphytic species of Cactaceae are found in the
which so far has served admirably as the outgroup for all neotropical forests and woodlands. Disocactus (including
phylogenetic analyses of cpDNA variation in subfamily Nopalxochia), Pseudorhipsalis, Epiphyllum, Rhipsalis, Hatiora,
Cactoideae (Fig. 1.3). In every molecular systematic study and Schlumbergera are genera mainly of holoepiphytes, i.e.,
conducted on subfamily Cactoideae, Calymmanthium was true epiphytes and epiliths that do not root in soil. Hylo-
found to be the most basal lineage in this group.Fur3.eeahere:
gnr
i1 cereus (including Wilmattea) and Selenicereus include nu-
Calymmanthium is a poorly known columnar mono- merous species that are facultative epiphytes or secondary
type. The few cultivated specimens exhibit juvenile shoots hemiepiphytes, initially rooting in soil, and later becoming
with basitonic branching, whereas, in nature, this species fully epiphytic.
can achieve a height of 8 m (Backeberg 1976). Its solitary Epiphytic cacti arose from ribbed, terrestrial columnar
flower develops in a bizarre way, in that the lower portion cacti. This was an obvious conclusion by early students and
is somewhat like a vegetative shoot with long, green scales, collectors of cacti, and no one has ever suggested the re-
whereas the upper portion is more like the typical cereoid verse, because epiphytes are too highly specialized to have
flower (Backeberg 1976). A liquid-preserved specimen of given rise to the larger terrestrial cacti. Several major shifts
C. substerile collected in the wild by Paul Hutchison in structure from terrestrial to epiphytic life have been
(3567, with J. K. Wright, January 1964; UCB jar 1000) is hypothesized:
stored at the University of California, Berkeley, herbarium.
This specimen has seven ribs, whereas juvenile shoots tend
1. Epiphytes easily form adventitious roots along
to have only three or four (Backeberg 1962, 1976). This
the stem and use these roots to anchor themselves
species has simple stem anatomy, with an unremarkable
to bark or rocks, as well as to absorb water and
epidermis, a uniseriate to biseriate collenchymatous hypo-
minerals. Many cacti have the ability to form adven-
dermis with relatively thin walls, and no mucilage cells in
titious roots from stem tissues, but holoepiphytes
either cortex or pith.
and hemiepiphytes do so while the stems are still
When compared with other columnar cacti using mo-
attached to the host plant.
lecular data, Calymmanthium lacks many of the synapo-
morphic nucleotide substitutions seen in the other tribal 2. Stems of many cactus holoepiphytes are broad
groups. Based on the plastid DNA sequences studied to and leaflike, possessing a high surface-to-volume
date, it does not ally with either tribe Leptocereeae or ratio (Sajeva and Mauseth 1991). The ribs of holo-
Browningieae, where it has been placed in previous taxo- epiphytes are thinner than ribs of terrestrial cacti,
nomic treatments, nor does it fall within the clade of the not providing enough bulk to support an upright
predominantly South American columnar cacti of tribes plant and requiring the plant to live in wetter habi-
Cereeae or Trichocereeae. Indeed, C. substerile may be tats because the stem does not store much water for
the only remaining representative of a cactus lineage that periods of drought. Holoepiphytes with very thin,
most closely represents the ancestral form of subfamily two-ribbed stems often do not possess a collen-
Cactoideae. chymatous hypodermis (e.g., in Schlumbergera,
There may be other, yet unstudied species that are also Disocactus, and Epiphyllum), whereas multiribbed
plesiomorphic, relative to the majority of cacti in the sub- columnar stems always form this support tissue
family, and would join C. substerile as “primitive outlier” (Gibson and Horak 1978).
taxa. Other cacti showing little morphological differentia- 3. Wood development is scanty, and the woody cylin-
tion from Calymmanthium are often considered “primi- der is very narrow, yielding a very thin and nonsuc-
tive” in the tribes to which they are associated (e.g., culent pith. Therefore, this wood is not used to sup-
Corryocactus [including Erdisia], Lepismium [including port the plant, and the pith is not designed to store
Pfeiffera and Lymanbensonia], and Leptocereus). Future water for dry seasons.
8 Wallace and Gibson
19. Ariocarpus
Mammillaria
CACTEAE
Echinocactus
Ferocactus
Armatocereus
LEPTOCEREEAE
Leptocereus
Bergerocactus
Carnegiea
Echinocereus
PACHYCEREEAE
Escontria
Polaskia
Stenocereus
Corryocactus
Arrojadoa
Gymnocalycium
Browningia
Cactoideae
Neoraimondia
Cereus
Cleistocactus
Espostoa BCT CLADE
Harrisia
Oreocereus
Trichocereus
Discocactus
Stetsonia
Uebelmannia
Calymmanthium
Copiapoa
NOTOCACTEAE
Notocactus
Lepismium
Rhipsalis
RHIPSALIDAE
Hatiora
Schlumbergera
Epiphyllum
Nopalxochia HYLOCEREEAE
Hylocereus
Maihuenioideae
Maihuenia
Opuntia phaeacantha
Tacinga
CACTACEAE
O. spinosior
Opuntioideae Pereskiopsis
Quiabentia
Pterocactus
O. subulata
Pereskioideae Pereskia aculata
P. grandifolia
Didiereaceae / Basellaceae Alluaudia
Basella
Portulacaceae
Portulaca
Figure 1.3. Strict consensus tree of 22,400 equally parsimonious trees from analysis of the rbcL gene for the family Cactaceae. A total of
1,434 bp of sequence was used for comparisons. Some important nodes in this tree are still unresolved.
20. 4. Spination on stems of cactus epiphytes, especially
on adult shoots, has been highly reduced or totally Columnar Cactus Lineages
eliminated. One might expect that these cacti lack Columnar cacti are presumably derived from a Calym-
spines because hanging plants are not easily eaten manthium-like ancestor that retained the upright, ribbed
by mammals, but the most likely explanation is that habit. Many columnar cacti are capable of supporting mas-
spines have been lost because they block sunlight sive stems with their combined rib, parenchymal, and vas-
from reaching the photosynthetic tissues of the stem cular structures (Cornejo and Simpson 1997). Molecular
(Gibson and Nobel 1986). evidence currently suggests that there are two primary
clades of columnar cacti that arose from the South
Cactus epiphytes are classified within two different American ancestral populations, each having inferred
tribes, the primarily South American Rhipsalideae and the common ancestries (Fig. 1.3). The first clade comprises
primarily North American Hylocereeae, implying that three former tribes that share a 300 bp deletion in Domain
within Cactoideae epiphytism evolved independently at IV of the plastid rpl16 intron, strongly suggesting a com-
least twice from terrestrial, ribbed columnar cacti, i.e., on mon ancestry based on this unique loss of DNA. Members
each of the continents (Gibson and Nobel 1986; Barthlott of the tribes Browningieae, Cereeae, and Trichocereeae all
1987). The speculation has been that Rhipsalideae evolved share this DNA deletion (R. S. Wallace, unpublished ob-
from ancestors like Corryocactus (Barthlott 1988) in west- servations). Acknowledging here the limited molecular
ern South America, passing through transitional forms re- phylogenetic resolution found within this group of cacti to
sembling Lepismium enroute to Rhipsalis, Schlumbergera, date, the cohort of genera found with this 300 bp deletion
and Hatiora, which inhabit the major center of diversity have been designated the “BCT” clade until more data are
for this tribe in Brazil. In North America, especially found to resolve the actual intertribal and intergeneric re-
Central America and the West Indies, shrubby species of lationships. The members of the BCT clade show tremen-
Hylocereeae, with arching stems and scandent growth dous diversity in growth habit, size, and habitat prefer-
habits, would have been the ancestors of climbing ences, and this clade is exemplary in its levels of floral
hemiepiphytes, e.g., Hylocereus and Selenicereus, as well as morphological variation and suites of pollination types, in-
the highly specialized two-ribbed, spineless holoepiphytes cluding insect, bat, hawkmoth, and hummingbird syn-
of that tribe. dromes. Interestingly, Buxbaum (1958) proposed that these
Molecular techniques have led to an important revela- groups are related to one another and constituted one
tion. The tribes with epiphytes likely represent two of the major radiation in South American cacti. Based on the
basal (i.e., the earliest divergent) lineages of subfamily scaly nature of the perianth in members of tribe Brown-
Cactoideae. Based on cladistic analysis of the chloroplast- ingieae, members of Cereeae and Trichocereeae are as-
encoded gene rbcL, hylocereoid epiphytes of Disocactus sumed to be more recently derived than those of Brown-
(subgenus Aporocactus), Epiphyllum, and Hylocereus, as well ingieae. This assumption needs to be checked with
as hemiepiphytes of Selenicereus, appear to have diverged as additional study and accompanying phylogenetic analysis.
a distinct lineage before, for example, Leptocereus and Phylogeny of the North American columnar cacti is
Acanthocereus (Wallace 1995; Cota and Wallace 1996), and somewhat better understood (Gibson and Horak 1978;
prior to the divergence of most columnar and barrel cactus Gibson 1982; Gibson et al. 1986). Molecular data current-
lineages. ly suggest that the two major lineages (tribes Leptocereeae
Early divergence of epiphytic groups from the colum- and Pachycereeae) arose from a Corryocactus-like transi-
nar and barrel forms suggests that there was a rapid evolu- tional form (derived from the original Calymmanthium-
tionary radiation that occurred within subfamily Cac- like ancestor in the northwestern Andes), and subse-
toideae. The hypothesized rapid radiation is likely the quently they radiated northward into North America
reason for the lack of resolution (common occurrence of within two geographic zones. In Central America and the
polytomy) among the major tribal lineages of subfamily Caribbean, Leptocereeae arose (Leptocereus, Acanthocereus,
Cactoideae. Until further studies of molecular variation are and Dendrocereus), achieving maximal diversity in the
complete—using additional DNA markers and more in- Greater Antilles, which formerly formed the backbone of
tensive sampling — the true branching order of the Cac- Central America (Gibson and Nobel 1986). The phyloge-
toideae phylogenetic tree will remain unresolved and in a netic sister taxon to the Leptocereeae is tribe Pachycereeae,
“polytomy” state. identified as having two distinct evolutionary components
10 Wallace and Gibson
21. within it that are recognized taxonomically at the subtribe are more distant than was previously thought. Cochemiea
level (Pachycereinae and Stenocereinae of Gibson and appears to be basal to Mammillaria, which may prompt
Horak 1978; Gibson 1982; Cota and Wallace 1997). Nu- systematists to recognize it as a segregate genus. Molecular
merous Pachycereeae and Leptocereeae may be character- systematic studies to evaluate the extensive infrageneric
ized as having primarily bat pollination, although insect classification of Mammillaria also will determine whether
and hummingbird pollination are found in some taxa. the morphological variants identified by traditional tax-
Certain arborescent Pachycereeae form extensive wood- onomists are supported by genetically based DNA varia-
lands in semiarid habitats throughout Mexico and other tion and therefore will provide valuable insights into the
places and provide an excellent example of ecological par- speciation processes of recently diverged cactus groups.
allelisms for the extensive woodlands of Cereus, Echinopsis Future studies of additional genera in the Cacteae will con-
(i.e., the Trichocerei), Browningia, and Armatocereus found tribute to a better understanding of phylogenetic radiation
in similar habitats of South America. in Mexico and surrounding regions of this monophyletic
tribe.
Cacteae and Notocacteae Tribe Notocacteae is the South American counterpart
Systematic studies of the tribe Cacteae have begun to elu- to Cacteae. This evolutionary branch includes a broad
cidate the complex intergeneric relationships in this, the array of low-growing barrel cacti native to various areas of
most speciose tribe of Cactoideae (Cota and Wallace 1997; South America, including Chilean deserts, lowland grass-
Butterworth and Wallace 1999; Butterworth et al. 2002). lands of Argentina, southern Brazil, Paraguay, Uruguay,
Preliminary results reinforce the traditional hypothesis, and related habitats. Although not as diverse as Cacteae,
e.g., that of Buxbaum (1950) or Barthlott (1988), that the Notocacteae exhibit similar diversity in stem morphology,
ancestor of Cacteae probably was ribbed, and that the most with short solitary or clumping barrel forms. The Noto-
highly derived taxa often have tubercular stem structures, cacteae include genera such as Blossfeldia, Copiapoa,
as seen in Coryphantha and Mammillaria. This observation Eriosyce (including Neochilenia, Neoporteria, and Pyrrho-
is not surprising per se, because one expects the barrel cacti cactus), Notocactus, Parodia, and perhaps Eulychnia, all
with ribs to be derived from columnar cacti with ribs, and strictly South American lineages and likely derived from
the barrel cacti of Echinocactus and Ferocactus have often ancestral populations arising farther north and west. Only
been depicted as the basal taxa of the Cacteae. However, a limited molecular study of the Notocacteae has been con-
number of interesting revelations about certain genera and ducted, so the intergeneric relationships of this tribe are
their relationships are emerging from the molecular data still not well understood.
that directly address questions of generic circumscription One central question to be resolved is whether the two
and monophyly. For example, as currently circumscribed, “barrel cactus” tribes (Cacteae and Notocacteae) arose from
the genera Ferocactus and Echinocactus are paraphyletic or a common ancestor during the early diversification of the
polyphyletic, and these species require further study to re- Cactoideae. If these tribes are determined to be sister
solve the relationships as elucidated by morphological and groups, the barrel cacti will then serve as a good example
molecular characters. One particularly surprising discovery for independent morphological evolution along different
originating from molecular studies is that the highly spe- paths on different continents that resulted in dissimilar
cialized plants of Aztekium, together with Geohintonia, morphological solutions to similar evolutionary and envi-
represent the most primitive living lineages of Cacteae. ronmental challenges. Furthermore, a phylogeny for the
This is an example where modern plants may manifest Notocacteae could also shed light on the pattern of mi-
highly specialized features, but they may still be considered gration seen in southeastern South America, as well as es-
basal lineages when phylogenetic analyses of appropriate tablish evolutionary links of the isolated Atacama Desert
data are conducted. species to those purportedly related genera on the eastern
Mammillaria, the largest genus of the Cactoideae with side of the Andes.
about 200 species, as currently treated, is monophyletic.
The peculiar species Oehmea beneckei and Mammilloydia Solving Classification Problems Using Molecular Techniques
candida are clearly nested within Mammillaria and should Data from cpDNA may also help cactus systematists to de-
not, therefore, be recognized as segregate genera. A close termine whether an oddball taxon should be treated as a
relationship between hummingbird-pollinated Cochemiea monotypic genus or placed into another genus. Within
and Mammillaria also has been confirmed, although they subtribe Stenocereinae of the Pachycereeae occurs a mas-
Evolution and Systematics 11
22. sive candelabriform columnar cactus that Gibson (1991) is very useful in determining evolutionarily related groups
found to be structurally very distinct and proposed recog- of taxa. Occurrence of the 300 bp deletion in the intron of
nition as a monotypic genus, Isolatocereus Backeberg. How- the plastid gene rpl16 is useful for including or excluding
ever, this segregate is most commonly treated within the taxa thought to be related to that clade. For example, the
genus Stenocereus, with which it shares synapomorphic sil- columnar cactus Stetsonia coryne from Argentina may have
ica bodies (Gibson and Horak 1978; Gibson et al. 1986). its closest affinities with members of Cereeae (Gibson and
Both cpDNA restriction site data (Cota and Wallace 1997) Nobel 1986), not Leptocereeae (Barthlott and Hunt 1993);
and gene sequence data strongly support recognizing I. du- members of the latter tribe do not share this 300 bp dele-
mortieri as a monotype, basal to the tightly nested species tion. Similarly, Neoraimondia, Armatocereus, and the Galá-
of Stenocereus (Fig. 1.4; Wallace 1995). Recognition of pagos Archipelago–endemic Jasminocereus thourarsii have
Isolatocereus is also supported by a cladistic analysis based on affinities with members of tribe Browningieae (Barthlott
structural features (Cornejo and Simpson 1997).Fur4eahere:
ge r
i1
.
n and Hunt 1993), not Leptocereeae (Gibson and Nobel
Another example of generic realignments that benefit 1986). Further study of these relationships will broaden the
from molecular systematic study is found in the genus information base from which more robust hypotheses
Harrisia (incl. Eriocereus and Roseocereus). This primarily about columnar cactus evolution and migration in South
South American and Caribbean genus has previously been America can be more reliably made.
classified in tribe Hylocereeae (Gibson and Nobel 1986;
Hunt and Taylor 1986) or in the Leptocereeae or Echi- Phylogenetic Studies of Subfamily Opuntioideae
nocereeae (Barthlott 1988; Hunt and Taylor 1990; Barthlott Until very recently, most cactus systematists and hobbyist
and Hunt 1993). Studies of its plastid sequences for the cactus growers had focused little attention on classification
gene rbcL, the trnL–F intergenic spacer, and the rpl16 in- of the 250 species of Opuntioideae, or approximately 15%
tron all indicate instead that this genus has its closest evo- of the family. This is regrettable because some opuntias are
lutionary affinities with members of the tribe Trichocereeae dominant perennials in drylands of the New World or have
in the BCT clade. Axillary hairs in the floral bracts are a become weedy invaders elsewhere and spread by grazing
morphological synapomorphy for placement of Harrisia habits of livestock (Nobel 1994, 1998). Important food
into this tribe. Furthermore, Harrisia shares the 300 bp sources are obtained from platyopuntias (Russell and Felker
deletion in Domain IV of the rpl16 intron observed in 1987). Understandably, gardeners generally elected not to
members of the BCT clade, which eliminates the possibil- cultivate opuntias, which have nasty, irritating glochids and
ity that Harrisia should be assigned to either the Lep- are not easily controlled plants, but now, growing small op-
tocereeae or Echinocereeae, which do not possess this untioids, especially taxa from western South America, has
unique deletion. Thus, Harrisia may be confidently placed become very popular among cactus enthusiasts.
within the Trichocereeae of the BCT clade. Due to the relatively small amount of systematic re-
Similar types of taxonomic placement problems can search emphasis placed on the Opuntioideae by past re-
also be resolved at the species level. A scandent, relatively searchers, a significant gap exists in our understanding of
thin-stemmed cactus originally described as Mediocactus the evolutionary relationships among these members of the
hahnianus from Rio Apa, Brazil, was transferred to the Cactaceae. Perhaps most important, an intensive phyloge-
genus Harrisia by Kimnach (1987) based on morphologi- netic analysis for this subfamily is required to evaluate the
cal similarities — particularly of the flower and stem — generic circumscription. Cactus researchers especially need
between this species and other members of Harrisia. A mo- to elucidate the early divergences of the opuntioid taxa to
lecular systematic study of the interspecific relationships in understand how many distinct lineages have resulted in
Harrisia (Wallace 1997) found that H. hahniana did not North and South America, as well as what the generic
fall within the well-supported Harrisia clade or with any “boundaries” are for genera and subgenera. For example,
species of Mediocactus or Hylocereus (tribe Hylocereeae) but the relationships of the low-growth forms, such as in the
allied strongly with members of the genera Trichocereus and genera Maihueniopsis and Tephrocactus, have been ex-
Echinopsis (also members of tribe Trichocereeae). Using the tremely hard to predict on the basis of superficial exami-
comparative sequence data from the rpl16 intron that cor- nation of external characters, and the evolutionary histo-
roborated similarities of floral morphology, Wallace trans- ry of structural transitions has been an area merely of
ferred H. hahnianus to the genus Echinopsis, now of the speculation.
BCT clade. A number of morphological transitions have been hy-
Presence or absence of a major structural rearrangement pothesized for the opuntioid lineages. Two in particular are
12 Wallace and Gibson
23. Leptocereus
Acanthocereus
Leptocereeae
Pachycereus
Lophocereus
Carnegiea
Neobuxbaumia
Bergerocactus
Pachycereinae
Nyctocereus
Columnar
ancestor
Peniocereus
Pachycereeae
Echinocereus
Stenocereinae
Morangaya
?
? Stenocereus
Escontria
Polaskia
Myrtillocactus
Isolatocereus
Corryocactus?
Figure 1.4. Hypothesized intergeneric relationships within some North American columnar cacti based on
analyses of rpl16 intron sequences. Tribe Pachycereeae appears to consist of two subtribes, Stenocereinae
and Pachycereinae (sensu Gibson and Horak 1978), but gene sequence analyses indicate that definitions of
both subtribes need to be expanded to include other species.
key: (1) a shift from persistent leaves to ephemeral foliage A factor that contributes considerably to the taxo-
leaves; and (2) changes in the shoot design from relatively nomic confusion within the subfamily is the high level of
uniform, cylindrical succulent stems to jointed stems with phenotypic plasticity shown within many opuntioid taxa.
either cylindrical or flattened segments, i.e., cladodes (syn- In species with shoot features, different vegetative forms
onym, phylloclades). Another presumed trend has been a have at times been given different scientific binomials,
shift in growth habit from upright woody plants (shrubs to adding to the nomenclatural problems of the group. Addi-
small trees) to shrubby or sprawling clumps, and even evo- tionally, both polyploidy and hybridization have played a
lution of the geophytic habit in Pterocactus, in which most vital role in the evolution of the diversity of these cacti and
plant biomass is subterranean and the aboveground parts have also contributed to nomenclatural chaos (Benson
are annual shoots. 1982). In fact, the Opuntioideae accounts for more than
Evolution and Systematics 13
24. 75% of the polyploidy observed in the Cactaceae (Benson Austrocylindropuntia) tend to grade into plants with
1982). flattened stems, as in Airampoa, which form the basal lin-
Although Opuntioideae present a considerable chal- eages of the platyopuntia clade. Forest emergents, such as
lenge to the cactus systematist, recent studies have provid- in Brasiliopuntia and Consolea of Brazil and the Caribbean,
ed much insight into opuntioid evolution. Of critical im- respectively, also show morphological transitions from
portance is sharply defining the generic concept for the terete stems of their trunks to flattened leaflike phyllo-
genus Opuntia. In some classifications, Opuntia represents clades (“pads”). These stem joints are seasonally deciduous
a wide array of small terete-stemmed trees, shrubs, plants in Brasiliopuntia. The true platyopuntias (genus Opuntia
with dwarf and clump-forming habits, chollas, club chol- in the type sense) have experienced complete loss of cylin-
las, platyopuntias (prickly pears), and the tree opuntias of drical stems, except in seedling stages. One notable excep-
Brazil and the Caribbean. In other classifications, these tion in the caatinga of eastern Brazil is Tacinga funalis, a
same plants may be reclassified into ten or more genera. scrambling, thin-stemmed subshrub that has reverted to
Some morphologically distinct plants, such as the geo- entirely terete stems, despite its clear affinities with flat-
phytic species of Pterocactus in Argentina or the persistent stemmed prickly pears, as determined by molecular data.
leaf-bearing species Pereskiopsis and Quiabentia of North The taxonomic dilemma is that the majority of the gen-
and South America, respectively, are more readily distin- era discussed here have typically been subsumed into a
guished as segregate genera. But even here, Pereskiopsis and “catch-all” genus, Opuntia. The molecular data have made
Quiabentia have been lumped into a single genus (Hunt it possible to determine evolutionarily related groups (e.g.,
and Taylor 1990). five major clades) and has provided sufficient evolutionary
Studies of seed morphology and other aspects of mi- information about these lineages to construct a robust phy-
cromorphology have provided evidence that a complete logeny. The intergeneric groups defined by the molecular
reevaluation of the generic circumscriptions in the sub- studies of Dickie and Wallace (2001) are essentially the same
family is warranted (Stuppy 2002). Molecular systematic generic groups that Stuppy (2002) proposed based on stud-
studies by Dickie (1998) and Dickie and Wallace (2001) ies of seed structures, in that both suggest that approxi-
were specifically designed to address these generic circum- mately 12 to 15 genera should be recognized as monophyletic
scription problems. From studies of plastid DNA variation units within the subfamily. Furthermore, the morphologi-
(rbcL, trnL–F intergenic spacer, rpl16 intron), the inferred cal discontinuities observed between these opuntioid genera
phylogeny indicated that there were five clades within the are, in reality, greater than those now recognized between
subfamily, related both geographically and morphologi- members of tribes in Cactoideae (e.g., the tribe Cacteae),
cally (Fig. 1.5), which follows the structural evidence de- whose generic distinctions have only rarely been questioned.
tailed by Stuppy (2002). A basal lineage for the subfamily Opuntioideae, therefore, offer a critical test for cactus
appears to include the species referable to the genera systematics. Many researchers, for convenience, would pre-
Austrocylindropuntia and Cumulopuntia, both native to the fer to have fewer and larger genera, but many smaller gen-
Peru-Bolivia-Chile Andean regions. Other clades are the era may have to be recognized to represent the true evolu-
narrowly distributed South American Pterocactus; a clade tionary lineages. Whether all or none of these smaller,
of Maihueniopsis-Tephrocactus (including Puna); and two demonstrably monophyletic groups are recognized at the
clades containing the more widely distributed opuntioids rank of genus, subtribes, or tribes by cactus systematists re-
found in both North and South America. The first of these mains to be seen. Discussions will eventually resolve these
more diverse clades is the “cylindroid” lineage, showing a questions and incorporate the available data and conclu-
south to north grade of specialization from leafy, cylindri- sions into a practical and generally accepted classification
cal-stemmed ancestral forms such as Pereskiopsis and for the Opuntioideae. Without a reliable phylogeny to
Quiabentia of North and South America, respectively, to form the basis of systematic comparisons, such discussions
more specialized, segmented-stemmed chollas of North and interpretations of morphological variation would be
America (Grusonia [including Marenopuntia, Micropuntia, very problematic, if possible at all.
and Corynopuntia] and Cylindropuntia).Fur51.eeahere:
gnr
i
For the flat-stemmed opuntioid taxa, a similar but New Insights into Cactus Evolution
more subtle south-to-north transition is seen, beginning
with the plesiomorphic genus Miqueliopuntia of the Structural Properties
Atacama Desert. Here terete-stemmed, clump-forming Having even the current, crude phylogenetic knowledge
opuntioids (in contrast to the solitary terete stems of from molecular systematic studies has provided new in-
14 Wallace and Gibson
25. Majority Rule
Maihuenia
Pereskia
Opuntia subulata
Austrocylindropuntia
O. pachypus
O. echinacea
Cumulopuntia
O. kuehnrichiana
Pterocactus kuntzei Pterocactus
Opuntia bradtiana Grusonia
O. clavata
Corynopuntia
O. stanlyi
O. marenae Marenopuntia
O. caribaea
Cylindropuntia
O. spinosior
Pereskiopsis porteri
Pereskiopsis
P. aquosa
Quiabentia pflanzii
Quiabentia
Q. verticillata
Opuntia weberi
O. nigrispina Tephrocactus
O. molinensis
O. clavarioides
Maihueniopsis
O. atacamensis
O. miquelii Miqueliopuntia
O. tilcarensis Airampoa
O. brasiliensis Brasiliopuntia
O. chaffeyi
O. guatemalensis
O. phaeacantha
Opuntia
O. polycantha
O. palmadora
O. inamonea
Tacinga funalis
Tacinga
T. braunii
Opuntia falcata
Consolea
O. spinosissima
Figure 1.5. Strict consensus tree of 32,700 equally parsimonious trees from analysis of rpl16 intron sequences in
the subfamily Opuntioideae (Dickey and Wallace 2000). The analysis strongly supports recognizing many of
the segregate genera formerly proposed for opuntioids.
