C O N T E N TS List of Contributors . vii Preface . ix 1. Evolution and Systematics Robert S. Wallace and Arthur C. Gibson . 12. Shoot Anatomy and Morphology Teresa Terrazas Salgado and James D. Mauseth . 23 3. Root Structure and Function Joseph G. Dubrovsky and Gretchen B. North . 414. Environmental Biology Park S. Nobel and Edward G. Bobich . 57 5. Reproductive Biology Eulogio Pimienta-Barrios and Rafael F. del Castillo . 756. Population and Community Ecology Alfonso Valiente-Banuet and Héctor Godínez-Alvarez . 917. Consumption of Platyopuntias by Wild Vertebrates Eric Mellink and Mónica E. Riojas-López . 1098. Biodiversity and Conservation Thomas H. Boyle and Edward F. Anderson . 1259. Mesoamerican Domestication and Diﬀusion Alejandro Casas and Giuseppe Barbera . 14310. Cactus Pear Fruit Production Paolo Inglese, Filadelﬁo Basile, and Mario Schirra . 16311. Fruits of Vine and Columnar Cacti Avinoam Nerd, Noemi Tel-Zur, and Yosef Mizrahi . 18512. Forage, Fodder, and Animal Nutrition Ali Nefzaoui and Hichem Ben Salem . 199
13. Nopalitos, Mucilage, Fiber, and Cochineal Carmen Sáenz-Hernández, Joel Corrales-Garcia, and Gildardo Aquino-Pérez . 21114. Insect Pests and Diseases Helmuth G. Zimmermann and Giovanni Granata . 23515. Breeding and Biotechnology Brad Chapman, Candelario Mondragon Jacobo, Ronald A. Bunch, and Andrew H. Paterson . 255 Index . 273
C O N T R I BU TO R SEdward F. Anderson (Deceased), Desert Botanical Joel Corrales-Garca, Departamento de IngenieríaGarden, Phoenix, Arizona Agroindustrial, Universidad Autónoma de Chapingo, MexicoGildardo Aquino-Prez, Insituto de RecursosGenéticos y Productividad, Montecillo, Mexico Rafael F. del Castillo, Centro Interdisciplinario de Investigacíon para el Desarrollo Integral RegionalGiuseppe Barbera, Istituto di Coltivazioni Arboree, Unidad Oaxaca, MexicoUniversità degli Studi di Palermo, Italy Joseph G. Dubrovsky, Departamento de BiologíaFiladelfio Basile, Dipartimento Scienze Economico- Molecular de Plantas, Instituto de Biotecnología,Agrarie ed Estimativ, Universita degli Studi di Catania, Universidad Nacional Autónoma de México, CuernavacaItaly Arthur C. Gibson, Department of OrganismicHichem Ben Salem, Institut National de la Biology, Ecology and Evolution, University ofRecherche Agronomique de Tunisie, Laboratoire California, Los Angelesde Nutrition Animale, Ariana, Tunisia Hctor Godnez-Alvarez, Departamento deEdward G. Bobich, Department of Organismic Ecología Funcional y Aplicada, Instituto de Ecología,Biology, Ecology and Evolution, University of Universidad Nacional Autónoma de México, MexicoCalifornia, Los Angeles CityThomas H. Boyle, Department of Plant and Soil Giovanni Granata, Dipartimento di Scienze eSciences, University of Massachusetts, Amherst Technologie Fitosanitartie, Università degli Studi di Catania, ItalyRonald A. Bunch, D’Arrigo Bros. Co., Salinas,California Paolo Inglese, Istituto di Coltivazioni Arboree, Palermo, ItalyAlejandro Casas, Departamento de Ecología de losRecursos Naturales, Instituto de Ecología, Universidad James D. Mauseth, Department of IntegrativeNacional Autónoma de México, Morelia Biology, University of Texas at AustinBrad Chapman, Plant Genome Mapping Laboratory, Eric Mellink, Centro de Investigación CientiﬁcaUniversity of Georgia, Athens y de Educación Superior de Ensenada, Mexico vii
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 Africaviii Contributors
P R E FAC EThe Cactaceae, a family of approximately 1,600 species, is and their uses. Twelve authors are from Mexico, eleven fromnative to the New World but is cultivated worldwide. In re- the United States, ﬁve from Italy, three from Israel, twosponse 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 onmorphology, spine properties, and often spectacular ﬂowers the Cactaceae. Nearly half of the authors, especially thosehave caused hobbyists to collect and cultivate large numbers dealing with agronomic aspects, are involved with theof 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 thethrive in arid and semiarid environments, where they are widespread interest in cacti but also should facilitate furtheroften 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 inland 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 thetions 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). BioticThis 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
(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 Erickx Preface
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 andThe Cactaceae is one of the most popular, easily recogniz- showy ﬂowers. Nearly every introductory college biologyable, 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 cactiWorld 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 (Crassulacean1988), and the epiphytic genus Rhipsalis has dispersed nat- acid metabolism) and succulence (Gibson and Nobelurally, 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
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 use2 Wallace and Gibson
whatever data are available at the time to formulate an ini- Talinum and Portulaca (Fig. 1.2; Appleqvist and Wallacetial 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 theresolution. Yet there are still some unresolved issues con- family Portulacaceae, as well as the evolutionarily distinctcerning 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 rFDNA aﬃnities to Caryophyllales, should be classiﬁedwithin the order (Angiosperm Phylogeny Group 1998). Cactaceae, a Monophyletic FamilyAmong these are the insectivorous sundews (Droseraceae) Even casual students of cacti can recognize the repetitiveand pitcher plants of Nepenthaceae. It is unclear at this vegetative design within this plant family (Gibson andtime 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 onas allies in one or more separate orders. Regardless of that modiﬁed axillary buds, termed areoles, but lacking broadoutcome, placement of family Cactaceae is unaﬀected for green leaves. The colorful ﬂower of the typical cactus hasthe 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, ofCaryophyllales have been much more diﬃcult to deter- course, exceptional forms: (1) spineless plants (e.g., certainmine. Investigators have been interested in determining to epiphytes such as Disocactus and Epiphyllum and small cactiwhich 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, Opuntiaand developmental evidence favored the Aizoaceae (Turner chaﬀeyi, and Peniocereus striatus); (3) primitive cacti that1973; 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 havecent analyses claimed that the Cactaceae has most recent relatively small ﬂowers with fewer parts (e.g., small-ﬂoweredancestry 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., Pereskiabecame called suborder Portulacineae Thorne (Cronquist sacharosa). None of these exceptions is troubling, because alland Thorne 1994), which included Cactaceae, Portula- are well-accepted members of the family and understood ascaceae, 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 ofmonophyletic 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 inversionter 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 in1994). Using a 1,100 bp sequence of open reading frame in Nicotiana tabacum; Downie and Palmer 1993) that involvescpDNA, the largest gene in the chloroplast genome, the genes atpE, atpB, and rbcL. This cpDNA inversion hasDownie et al. (1997) concluded again that Pereskia (Cacta- been found in all cacti sampled, so this is an excellentceae) belongs in the portulacaceous cohort. With internal molecular synapomorphy for deﬁning Cactaceae (Wallacetranscribed 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 independentlyPortulacaceae, and the Cactaceae was identiﬁed as the sis- in another caryophyllalean lineage, the Chenopodiaceaeter taxon of a clade that includes species of Talinum. In a (Downie and Palmer 1993). Nonetheless, because cactimore 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., traceableshown that the Cactaceae is indeed nested within the back to a single ancestral population in which the inversionPortulacaceae sensu lato and is most closely related to appeared and then became genetically ﬁxed. What remains Evolution and Systematics 3
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 tuberosusFigure 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).
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 withary 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 haveAll 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 stagesis distinguished by structural criteria, for which there are linking the leafy, nonsucculent, aerole-bearing shoots ofrelatively 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, suchreproductive 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 ofhave been assigned to this subfamily: Pereskia (16 spp.; cpDNA structural arrangements of the chloroplast genomeLeuenberger 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 plastidvegetative morphology and anatomy but share some ple- genome (Wallace 1995). All Cactoideae examined to datesiomorphic (primitive) reproductive features (Buxbaum have a diﬀerent deletion at the 5 end of the accD region1953). 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 commonMaihuenia 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 phylogeniesits 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 hasretrorse 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 aredruse, i.e., an aggregate crystal of calcium oxalate (Bailey themselves divergent because they have not been found to1964; Gibson and Nobel 1986); (3) pollen grains are poly- share restriction site changes, although many occurporate 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 thatular envelope, often described as being an aril; and (5) spe- Pereskia and Maihuenia are as divergent from one anothercial 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 asBailey 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 leavesthe family. not known to occur elsewhere in Cactaceae (Gibson Subfamily Cactoideae is less easily delimited by syn- 1977b; Leuenberger 1997). Wood features of Maihuenia areapomorphies. In fact, probably only one general form ap- also diagnostic to a specialist (Gibson 1977b), although allplies to all genera: namely, the stem is succulent and pos- the cell types found in Maihuenia, including the special Evolution and Systematics 5
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
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 priorisis, the researcher must include at least one species that has choice of taxa to best represent the primitive species has beenthe presumed primitive features of the group being studied. a ﬁeld of great speculation and, until now, selecting theFor Cactaceae as a whole, this has been easy because the leaf- primitive taxon has been a subjective process. Often, speciesbearing 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 frequentphylogenetic analyses. For Opuntioideae also, the choice is and are usually incompletely described. Evolution and Systematics 7
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
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 PortulacaFigure 1.3. Strict consensus tree of 22,400 equally parsimonious trees from analysis of the rbcL gene for the family Cactaceae. A total of1,434 bp of sequence was used for comparisons. Some important nodes in this tree are still unresolved.
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 components10 Wallace and Gibson
within it that are recognized taxonomically at the subtribe are more distant than was previously thought. Cochemiealevel (Pachycereinae and Stenocereinae of Gibson and appears to be basal to Mammillaria, which may promptHorak 1978; Gibson 1982; Cota and Wallace 1997). Nu- systematists to recognize it as a segregate genus. Molecularmerous Pachycereeae and Leptocereeae may be character- systematic studies to evaluate the extensive infragenericized as having primarily bat pollination, although insect classiﬁcation of Mammillaria also will determine whetherand 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 theplaces 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 radiationin similar habitats of South America. in Mexico and surrounding regions of this monophyletic tribe. Cacteae and Notocacteae Tribe Notocacteae is the South American counterpartSystematic studies of the tribe Cacteae have begun to elu- to Cacteae. This evolutionary branch includes a broadcidate the complex intergeneric relationships in this, the array of low-growing barrel cacti native to various areas ofmost 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, allwith ribs to be derived from columnar cacti with ribs, and strictly South American lineages and likely derived fromthe barrel cacti of Echinocactus and Ferocactus have often ancestral populations arising farther north and west. Onlybeen 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 aretheir 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 twoand monophyly. For example, as currently circumscribed, “barrel cactus” tribes (Cacteae and Notocacteae) arose fromthe genera Ferocactus and Echinocactus are paraphyletic or a common ancestor during the early diversiﬁcation of thepolyphyletic, and these species require further study to re- Cactoideae. If these tribes are determined to be sistersolve the relationships as elucidated by morphological and groups, the barrel cacti will then serve as a good examplemolecular characters. One particularly surprising discovery for independent morphological evolution along diﬀerentoriginating from molecular studies is that the highly spe- paths on diﬀerent continents that resulted in dissimilarcialized 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 theThis 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 Desertdata 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 Techniquescandida 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 arelationship between hummingbird-pollinated Cochemiea monotypic genus or placed into another genus. Withinand Mammillaria also has been conﬁrmed, although they subtribe Stenocereinae of the Pachycereeae occurs a mas- Evolution and Systematics 11
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 are12 Wallace and Gibson
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 ofuniform, 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 formsonym, 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 alution of the geophytic habit in Pterocactus, in which most vital role in the evolution of the diversity of these cacti andplant biomass is subterranean and the aboveground parts have also contributed to nomenclatural chaos (Bensonare annual shoots. 1982). In fact, the Opuntioideae accounts for more than Evolution and Systematics 13
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
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. spinosissimaFigure 1.5. Strict consensus tree of 32,700 equally parsimonious trees from analysis of rpl16 intron sequences inthe subfamily Opuntioideae (Dickey and Wallace 2000). The analysis strongly supports recognizing many ofthe segregate genera formerly proposed for opuntioids.