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Home , Austrocylindropuntia, Consolea, Consolea corallicola, Cylindropuntia, Cylindropuntia bigelovii, Cylindropuntia prolifera

474 Entomologist 84(4) December 2001

OPUNTIA CACTI OF NORTH AMERICA—AN OVERVIEW

JON P. REBMAN1 AND DONALD J. PINKAVA2 1San Diego Natural History Museum, P. O. Box 121390, San Diego, CA 92112-1390

2Department of Biology, State University, Tempe, AZ 85287-1601

ABSTRACT

The Cactaceae are a diversified group of New World with a wide array of evolutionary and ecological strategies that has given them the ability to adapt to many different habitats. The is both interesting and challenging because of its varied morphology, adaptations to the environment, and reproductive systems. Of the groups within the family, the are one of the most successful and widespread, but they exhibit many taxonomic difficulties and are, therefore, not well understood.

Key Words: Cactaceae, , diversity, adaptation, reproductive strategies

RESUMEN

Las cactáceas son un grupo de plantas muy diversificado con una impresionante colección de estrategias evolutivas y ecológicas que les ha dado la habilidad de adaptarse a muchos há- bitats diferentes en el nuevo mundo. Esta familia es interesante y desafiante debido a su va- riación morfológica, diversas adaptaciones al medio ambiente, y a sus sistemas de reproducción. Dentro de los grupos de la familia de las cactáceas, las opuntias son de los más exitosos y ampliamente distribuidas, pero presentan muchas dificultades taxonómicas y por lo tanto no son del todo entendidas.

The Cactaceae are an exciting and challenging (Gibson & Nobel 1986). However, there are no fos- group of plants because of their varied morphol- sil records known beyond the desert packrat ogy and succulence, their showy flowers, their (Neotoma sp.) middens of the Pleistocene (Mc- adaptations to the environment, and their repro- Carten 1981). ductive strategies. The family has ca. 1600 spe- cies in ca. 115 genera (Barthlott & Hunt 1993). TAXONOMY Cacti occur naturally from just south of the Arctic Circle in to the tip of Patagonia in South The discovery of in cacti helped tax- America. Native cacti are restricted to the New onomists understand the phylogenetic position of World, except for one , baccifera the Cactaceae. Betalains are reddish pigments (Miller) W. T. Stearn or mistletoe cactus of tropical found in a small, related group of families in the , which prehistorically migrated to Af- order (Carnations order). Other rica, Madagascar and Ceylon (Barthlott 1983). flowering plants have similarly colored pigments The sticky small of R. baccifera were pre- called anthocyanins, which are synthesized via a sumably carried across the Atlantic Ocean by different chemical pathway. Betalains get their birds. name from beets (the Beta in the Che- Cacti grow at altitudes from below sea level nopodiaceae), which are red in color due to the (e.g., at Death Valley, CA) to over 4,500 m in the presence of the , . Certain beta- Andes; and in climates having no measurable lains are responsible for the red to purple prickly- rainfall to more than 500 cm of annual precipita- pear pads, particularly when under stress as in tion. Cacti vary in size from that of a large marble macrocentra Engelmann. The Cactaceae to as tall as 20+ m and weighing several tons. were once classified near the carrot family (Api- There are three centers of cactus diversity: (1) aceae), but now the family is placed in a very dif- central , from where the North American ferent order, the Caryophyllales, along with the cacti have evolved, 2) the Andean region, and 3) only other betalain-producing angiosperm fami- . The dispersal of species radiating from lies, Achatocarpaceae, Aizoaceae, Amarantha- these three centers has overlapped very little, ex- ceae, Basellaceae, Chenopodiaceae, Didieriaceae, cept for human introductions. There is a sub- Nyctaginaceae, Phytolaccaceae, and Portula- center extending from northern , caceae (Cronquist 1988). northward through the Antilles and Barthlott (1988) presented a phylogeny of the to Florida. The origin of all cacti is probably in Cactaceae. There are three subfamilies of cacti— South America, perhaps 90-100 million years ago the phylogenetically Pereskioideae, the

Rebman & Pinkava: Opuntia cacti of North America 475

Opuntioideae (the subfamily we are specifically additional varieties and at least seven named interested in for this symposium), and the most interspecific hybrids in the alone. derived and speciose , comprising Two other genera of the , No- some 80% of all cacti. The greatest diversity of palea and , are found only in Florida in cacti is in South America. the United States. Nopalea (Fig. 4) has a flower The Opuntioideae differ from all other cacti in modified for hummingbird pollination. The flower having glochids (small, barbed, and deciduous is somewhat tubular in shape with red to orange spines) and seeds that are completely enwrapped that are almost completely closed, but with by a funicular stalk, which becomes hard and protruding and stigmas. The Nopalea bony. The largest genus in this subfamily is Opun- flower also has a nectar chamber covered by an tia, and in its very broad sense numbers perhaps extension of the style near its base. Just one spe- 200 species (Barthlott & Hunt 1993). cies (N. cochinellifera (L.) Salm-Dyck) is found in The opuntias (representatives of the subfamily the United States and has naturalized from culti- Opuntioideae) of the United States total 5 genera, vation in central Florida. The genus Consolea 61 species, 18-20 additional varieties and many (Fig. 5), has short, orange to red, slightly bilater- interspecific hybrids (Pinkava, ined.). The true ally symmetric flowers, with wide-opening petals chollas (, Fig. 1) have cylindric and a nectar chamber similar to that of Nopalea. stem segments and completely deciduous spine There is one species in the United States, the sheaths. Cylindropuntia has 20 species, six addi- nearly extinct native C. corallicola Small from the tional varieties and at least nine named interspe- , a species of special concern in this cific hybrids in the United States. The club-chollas symposium. (, Fig. 2) are low mat- or clump-formers with cylindric to spheric stem segments having ECOLOGY spines with only the tips being sheathed. In the United States, there are eight species and one Opuntias, and cacti in general, are widespread interspecific of club-chollas. The prickly- and have adapted to many diverse habitats. One pears (Opuntia sensu stricto, Fig. 3) have mostly hypothesis is that they occupy areas where there flattened stem segments and are completely with- is little competition from other plants, particu- out spine sheaths. There are 31 species, 12-14 larly when growing under extreme conditions. In

Fig. 1. Example of Cylindropuntia, C. spinosior (Engelmann) Knuth, the cane cholla.

476 Florida Entomologist 84(4) December 2001

Fig. 2. Example of Grusonia, G. kunzei (Rose) Pinkava, the Kunze club-cholla.

the United States, opuntias occur commonly in all Britton & Rose) often outgrow, even outlive, these four North American deserts: Chihuahuan, Sono- nurse plants. ran and Mojave hot deserts and the cold desert. In respect to the opuntias, prickly- MORPHOLOGY pears, for example, thrive in arid, shallow and well-drained soils, but also on over-grazed sites The morphology of cacti is often, at first, bi- and other disturbed areas, many attributable to zarre-looking, but close study reveals only an ex- human activities. In general, the greater the hab- aggeration of well-known features. All cacti have itat disturbance the less the plant competition, alternate leaves along the axis of a long-shoot/ but if too severe, of course, cacti also disappear. short-shoot growth pattern. As is true for virtu- Cacti also do well in dry, tropical deciduous for- ally all plants, there is an axillary bud at the up- ests where there is little shade much of the year per leaf base; however, in cacti this bud barely because of leaf-drop, even though the competing elongates and is called the short-shoot or areole. plants are close together. Epiphytic cacti, which In prickly-pears, the long-shoots are the pads are found mostly in the wet tropics, grow in open (stem segments also called cladodes) and the areas on branches of . Their roots are kept coverings (pericarpels). Each pad, in its first year relatively dry in the open air or in a scanty sub- only, produces areoles with subtending conic strate. All cacti require good drainage; long term leaves (Fig. 6). The short-shoot areole produces accumulation of water is detrimental to them. leaves modified into spines of two kinds—perma- But, cacti can do well and grow faster under hy- nent spines with their bases embedded in cork droponics, if well aerated. (those which can puncture your finger but remain Cacti utilize high PAR (Photosynthetically Ac- on the plant) and small, barbed, easily dislodged tive Radiation) (for details see Gibson & Nobel glochids (those which break off easily and stay 1986). They do poorly and etiolate rapidly in with your finger). Hormone concentrations during shade. However, shade is beneficial and often nec- the very early development of the spine determine essary during the critical stages of germination if it will be a regular spine, a glochid, or something and juvenile development, such as when growing intermediate between these structures which is in association with nurse plants. Some cacti, e.g., rare in nature (Mauseth & Halperin 1975). Spines the (Carnegiea gigantea (Engelmann) are produced from the short-shoot areole spirally

Rebman & Pinkava: Opuntia cacti of North America 477

Fig. 3. Example of Opuntia, O. basilaris Engelmann & Bigelow, the beavertail prickly-pear. from its margin to its apex. Spines elongate from veins from the surrounding stem that enter at the the base and are larger in diameter at the base, top and sides of the ovary, split and extend up- but cells within the spine die from the apex to the ward into the style and downward toward the base. The microscopic barbs of the glochid tip are of the ovary. This unique vasculature pro- created when an epidermal cell overrides the epi- vides evidence as to the derivation of the inferior dermal cell below it (Robinson 1974). The base of ovary of a cactus flower from a stem that pro- the glochid has an abscission layer (thin-walled trudes outward and engulfs the ovary. What is cells) that is easily broken by contact. Short- generally called a “fruit” is actually a fused com- shoots (areoles) also, on occasion, produce long- bination of long-shoot coverings (technically shoots including branches and flowers. called pericarpels) and the true botanical fruit, Tubercles (or podaria) are swellings below the the mature ovary. So, when we eat the fleshy conic leaves of the pad (long-shoot). The upper fruits of prickly-pears, called tunas, we are eating part of the conic leaf is the blade, which abscises primarily stem tissue (after removing the in a week or two at a notch. The leaf base, or pet- glochids and spines, of course). Because the peri- iole, and adjacent stem tissues are fused together carpel is composed of stem tissue, it, like a first- forming the tubercle. The tubercle may elongate year regular pad, produces conic leaves and are- and swell such as in species of pincushion cacti oles on its sides that, in turn, produce glochids (Mammillaria spp.). If the raised tubercles align and sometimes spines, or even flower buds. vertically around the stem they can coalesce with those directly above and below forming ribs, like ADAPTATIONS those of the saguaro. The flowers of cacti are quite variable, but Cacti have no escapability and therefore are there are some general features that are shared subject completely to their environs. Two major by the whole family. The ovary of the flower (the problems exist for cacti, particularly those in arid -bearing part of the pistil) is completely em- climates: temperature extremes and lack of avail- bedded within the stem—a modified pad or long- able water. However, several adaptations allow shoot. Non-cactus flowers are positioned on top of them to cope with these difficulties. the stem and vascular strands (veins) enter from Freezing temperatures in the United States the stem below. However, cactus flowers have limit distributions by destroying the growing api-

478 Florida Entomologist 84(4) December 2001

Fig. 4. Example of Nopalea, N. auberi (Pfeiffer) Salm-Dyck, the lengua de vaca. cal meristems (stem tips) of many cacti at the eral feet from the main plant body. Cacti also northern edges of their ranges and on northern quickly produce tiny “rain roots,” which efficiently north-facing slopes. This freezing effect may be absorb water after rains, but which quickly die moderated somewhat by stem tips having protec- when water is no longer available. The retention tion via pubescence and/or spines or by having de- of water within the cactus is enhanced by lower- pressed summits. ing transpiration rates via: 1) having leaves re- High temperature effects may be reduced by duced to spines which lowers surface area; 2) evasion from direct insolation by tilting toward having a heavy wax coating (cuticle) on surfaces, the sun such that only the smaller top surface impeding direct water loss to the atmosphere; 3) gets direct sun and not the sides, e.g., barrel cacti having daytime closure of stomata; and 4) being (Ferocactus species); or by an orientation of pads succulent wherein water adheres to complex car- of prickly-pears such that minimal surface area bohydrates called mucilage. Mucilage holds water (at edges of, not faces of pads) is exposed to direct very tightly, requiring energy to free the water. In sunlight during the hottest periods of the day. Wa- some cacti, ribs allow the stems to expand and ter is conserved by a reduction of leaf surfaces contract like the pleated part of an accordion both from broad blades to spines and the reduction of daily and seasonally, allowing for gains and losses stem surface area by having an efficient shape in of water. Cacti also conserve water by quickly relation to surface area/volume ratios, such as in sealing any breaks in the stem’s surface caused barrel and globular cacti. Also, there is shading of by animals, humans, or weather. Szarek (in Gib- surfaces by pubescence and/or spines and by the son and Nobel 1986) experimented with a teddy- formation of ribs and elongate tubercles. A spe- bear cholla ( (Engel- cialization of prickly-pears in Arizona is a meta- mann) Knuth) by severing it from its base, then bolic shutdown (aestivation, similar to hiber- tying it to a ring stand in the desert. It survived nation), which occurs during non-growing sea- three years without any contact with the soil. The sons so that only minimum metabolic mainte- scar tissue that formed where the plant was cut nance takes place (Nisbet & Patten 1974). quickly cut off the loss of water. Water absorption from rainfall is maximized in Crassulacean Metabolism (CAM) pro- most cacti by the presence of a shallow, wide- vides a method for photosynthesis to occur while spread root system, which often extends out sev- stomata are closed during the daytime. This tim-

Rebman & Pinkava: Opuntia cacti of North America 479

Fig. 5. Example of Consolea, C. falcata (Ekman & Werdermann) Knuth. ing of stomatal opening is common in cacti and DNA that can, in turn, mutate providing genetic other succulents but is the reverse of most other novelties and yet maintain the status quo in un- plants. In CAM, the stomata open at night, allow- changed genome copies; 4) interspecific hybrid- ing for the exchange of gases when temperatures ization allowing for the exchange of genes and transpiration rates are lower. Incoming CO2 between once genetically separated or partially is converted to stored malic acid in the cells dur- separated populations via hybrid fertility. ing nighttime. The next day, the malic acid is con- in the Cactaceae are usually perfect, verted back to CO2, which can then be used to containing both functional pistils and stamens. carry out photosynthesis and the making of car- Such flowers can either outcross with other indi- bohydrates using light energy. viduals or be self-fertile and pollinate themselves As a result of these adaptations, cacti thrive in (del Carmen Mandujano et al. 1996; McFarland et arid environments. They have adapted well to the al. 1989; Osborn et al. 1988; Ross 1981). However, extremes of their physical surroundings and have a very limited number of cacti have been reported the morphology and physiology to survive these to be dioecious, androdioecious, gynodioecious, or environmental adversities. trioecious (Fleming et al. 1994; Hoffman 1992; Parfitt 1985; Valiente-Banuet et al. 1997). The REPRODUCTIVE STRATEGIES OF OPUNTIOID CACTI opuntias have evolved some exceptions to synoecy (= hermaphroditism, having perfect flowers) as The opuntioid genera have evolved rapidly and well. Within the genus Opuntia, Parfitt (1985) successfully by taking advantage of a combina- documents O. stenopetala Engelmann as dioe- tion of several reproductive strategies: 1) sexual cious (with separate pistillate and staminate in- reproduction which promotes active gene ex- dividuals). More recently, change and helps to maintain genetic variability, was discovered to be cryptically dioecious (with including the development of dioecy and gynodio- functionally separate pistillate and staminate ecy that increases outcrossing and the genetic di- plants, but appearing morphologically bisexual) versity of populations; 2) cloning via vegetative (Negron-Ortiz 1998) and five taxa in the genus propagules such as detached stem segments and Cylindropuntia (including C. calmalliana (Coulter) fruits, and via sprouting from roots or non-sexual Knuth, C. molesta (Brandegee) Knuth, and seeds; 3) polyploidization allowing for additional C. wolfii (Benson) Baker) from southern Califor-

480 Florida Entomologist 84(4) December 2001

Fig. 6. Long-shoot pad of Opuntia aurea Baxter showing the spiral arrangement of short-shoots (areoles) at the bases of conic, long-shoot leaves. Photo by Martin Ganz.

nia and Baja appear to be gynodioe- tissue and has the ability to generate new organs cious (with perfect- and pistillate-flowered such as adventitious roots and stems, the fruits individuals) (Rebman 1998). can drop from the parent plant and develop into Asexual reproduction is a common occurrence clonal individuals. for many opuntias. The most prevalent type of Another type of asexual reproduction that has cloning in this group is vegetative propagation by been documented in Opuntia is adventive embry- stem or cladode detachment (Fig. 7). The terminal ony (Davis 1966). In this form of vegetative prop- stem segments of many species (e.g., Cylindro- agation, a diploid mother cell is translocated into puntia leptocaulis (DeCondolle) Knuth, Opuntia the embryo sac and without fertilization develops fragilis (Nuttal) Haworth, and O. pubescens into a clonal embryo that is produced inside of the Wendland) detach with ease from the parent seed. Thus, the individual that germinates from plant and readily take root creating clonal indi- the seed is actually a clone of the parent plant. viduals (Fig. 7). By this mechanism, some opun- The high frequency of vegetative propagation in tias can develop natural populations that appear opuntias can help to maintain particular genetic to be dense monocultures of clonal individuals. combinations, perpetuate hybrids, develop dense Some of these species frequently referred to as populations, and readily colonize new localities. “jumping cacti” (e.g., Cylindropuntia bigelovii, Cytogenetic analyses in the Cactaceae have C. fulgida (Engelmann) Knuth, and C. molesta) been a very useful taxonomic tool for distinguish- bear retrorsely-barbed spines on their easily dis- ing species and documenting natural hybrid pop- lodged stem segments and are dispersed by at- ulations (e.g., Baker & Pinkava 1987; Pinkava & tachment to some mobile vector such as animals. McLeod 1971; Pinkava & Parfitt 1982; Pinkava et In these taxa, the success of this type of dispersal al. 1973, 1985, 1998; Powell et al. 1991). The Cac- mechanism may be responsible for much of the taceae have a base number of x = 11 and polyp- species’ distributional patterns. loidy is the most common type of chromosomal The fleshy fruits of some opuntias, e.g., Cylin- variation, although aneuploidy, secondary associ- dropuntia cholla (Weber) Knuth and C. fulgida ation, cytomixis, extranuclear bodies (Ross 1981), can also become vegetative propagules. Since the inversions (Pinkava et al. 1973), and transloca- pericarpel surrounding the ovary is actually stem tions (Pinkava et al. 1985) have been discovered.

Rebman & Pinkava: Opuntia cacti of North America 481

Fig. 7. Young clonal individuals of the teddy-bear cholla (Cylindropuntia bigelovii (Engelmann) Knuth) take root near the base of an older plant as a result of vegetative propagation by stem detachment.

Although occurs in only about 28% of duction of novel features by mutation without all cacti investigated thus far, it plays a more im- displacing proven adaptations. In other words, portant role in the evolution of the subfamily polyploidy, as part of an evolutionary mechanism, Opuntioideae (64.3%), than in the Cactoideae may help to bring about something new without (12.9%) and the Pereskioideae (0.0%) (Pinkava et much detrimental impact. It appears that polyp- al. 1998). The highest levels of ploidy in the opun- loidy may be one of the main driving factors in the tioid group occur in the South American taxa— diversification of opuntias due to its common oc- (11x), (ca. currence. This process may also be responsible for 20x), and (30x). some reproductive strategies in the Cactaceae, According to Pinkava et al. (1998), the origin of i.e., gynodioecy and trioecy, since all cactus spe- most polyploid cactus species is probably from fer- cies determined thus far that stray from synoecy tilization involving unreduced gametes. This are polyploid. mechanism was determined as the main factor in Hybridization coupled with polyploidy, the pe- polyploidization because: 1) macropollen has been rennial habit, and asexual reproduction all play a found positively staining with cotton blue in dip- role in increasing the complexity of the evolution- loid species; 2) many opuntioid taxa are both 2x ary processes of the Cactaceae. In our studies of and 3x, but not 4x, suggesting that triploid indi- opuntias, intraspecific, interspecific, and interge- viduals are produced from the union of a reduced neric hybrids have been determined by interme- gamete (1x) and an unreduced gamete (2x) and diacy in morphological characters such as flower then reproduce vegetatively, rather than from 2x color and size, fruit shape, texture, and spination; × 4x hybridizations; 3) the morphology of inter- reduced stainability; proximity to putative specific and intergeneric hybrids derived from parents; and overlapping flower phenology. The parents with different ploidy levels show genome commonality of hybrid events in many opuntioid dosage effects on character expression, making taxa blurs species’ boundaries and has led to them more similar to the parent of higher genome much difficulty in accurately delineating taxa. dosage than to the parent of lower dosage. Hybrids can be rare and sterile, quite common Polyploidy adds supplementary DNA to a spe- and self-fertile, or backcross to the parent taxa. cies’ genome. This process can facilitate the intro- The effects of gene introgression between sympa- 482 Florida Entomologist 84(4) December 2001 tric parental species have allowed certain hybrid Of the groups within the Cactaceae, the opun- genotypes to survive and thrive (Anderson and tias are an extremely diversified and dominant Stebbins 1954). In cacti, hybridization in associa- component in many plant communities found tion with polyploidy and vegetative propagation throughout the New World, especially in arid re- may even yield new species able to invade habi- gions. However, they are still one of the least un- tats different from both parent taxa, such as for derstood groups in the cactus family. Although a (Engelmann) Knuth lot of recent knowledge has been gained about the (Mayer et al. 2000). opuntioids and their evolutionary and ecological Various techniques traditionally employed to strategies, they are still an enigmatic group. There help elucidate hybrid events and taxa include is no doubt that many discoveries about their nat- morphological studies, chromosome counts, and ural history and phylogeny which have yet to be lactophenol pollen stains. Unfortunately, most of encountered will help us to better understand this these studies have their limitations when exam- fascinating and challenging group of cacti. ining very complex hybrid processes. It is hoped that future chemical and molecular analyses will ACKNOWLEDGMENTS help to unravel and provide much more insight into the reticulate evolution that seems prevalent We would like to thank Mike Simpson, Andrew Saly- in the phylogenies of many opuntias. won, and Judy Gibson for reviewing this manuscript. We also appreciate Raul Puente for his identifications of TAXONOMIC CHALLENGES the figures of Consolea and Nopalea, and Annette Win- ner, Karen Rich, and Stefanie Ickert-Bond for their help The opuntias have long been a taxonomic prob- with the figures. lem for a variety of reasons. 1.) Dried specimens of cacti used for morphological studies usually are REFERENCES CITED poorly prepared and many characteristics are lost or altered during herbarium specimen prepara- ANDERSON, E., AND G. L. STEBBINS, JR. 1954. Hybridiza- tion. As a result, type specimens are often inade- tion as an evolutionary stimulus. Evolution 8: 378- quate and non-descriptive causing subsequent 388. nomenclatural difficulties (i.e., Cylindropuntia BAKER, M. A., AND D. J. PINKAVA. 1987. A cytological typology, in Rebman 1995). 2.) Like all cacti, it is and morphometric analysis of a triploid apomict, Opuntia (kelvinensis (subgenus Cylindropuntia, difficult to make good herbarium specimens of Cactaceae). Brittonia 39: 387-401. opuntias due to all of the cutting, scraping, flat- BARTHLOTT, W. 1983. Biogeography and evolution in tening, and drying that is required. For this rea- neo- and paleotropical Rhipsalinae, pp. 41-248. In son, many botanists do not collect opuntias and K. Kubitzki [ed.]. Dispersal and Distribution. Son- herbarium collections are usually very depauper- derbd. naturnaturwiss. Ver. Hamburg 7, Hamburg. ate in cactus specimens. This oversight creates a Barthlott, W. 1988. Über die systematischen Gliederun- lack of distributional knowledge and an incom- gen der Cactaceae. Beitr. Biol. Pflanzen 63: 17-40. plete record of morphological variability present Barthlott, W., and D. R. Hunt. 1993. Cactaceae, pp. 161- in most species, and should be considered one of 196. In K. Kubitzki [ed.], The Families and Genera of Vascular Plants. Vol. II. Flowering Plants. Springer the biggest limitations to the taxonomic research Verlag Berlin. in the opuntias. 3.) Many vegetative characters DEL CARMEN MANDUJANO, M., C. MONTAÑA, AND L. E. can be quite drastically influenced by environ- EGUIARTE. 1996. Reproductive ecology and inbreed- mental factors. Morphological features such as ing depression in (Cactaceae) in growth habit, stem pubescence, spine length and the : Why are sexually derived number per areole can be phenotypically plastic recruitments so rare? Amer. Jour. Bot. 83: 63-70. and may change significantly depending upon lo- CRONQUIST, A. 1988. The Evolution and Classification of cal growing conditions. 4.) Many opuntias hybrid- Flowering Plants. Ed. 2. Botanical Gar- ize with other sympatric taxa producing novel, den, Bronx. DAVIS, G. L. 1966. Systematic Embryology of the An- combined, or intermediate character states be- giosperms. Wiley & Sons, Inc., New York. tween species which can blur the boundaries be- FLEMING, T. H., S. MAURICE, S. L. BUCHMANN, AND M. tween species. 5.) The opuntias can reproduce by D. TUTTLE. 1994. Reproductive biology and relative vegetative propagation, adventive embryony, and male and female fitness in a trioecious cactus, self-fertility. These reproductive mechanisms pringlei (Cactaceae). Amer. Journ. Bot. help to sustain particular genetic combinations, 81: 858-867. perpetuate hybrids and as a result, create taxo- GIBSON, A. C., AND P. S. NOBEL. 1986. The Cactus nomic enigmas for the systematist. 6.) There is a Primer. Harvard Univ. Press, Cambridge, MA. lack of interest by amateur collectors and hobby- HOFFMAN, M. T. 1992. Functional dioecy in Echinocer- eus coccineus (Cactaceae): Breeding system, sex ra- ists thus providing little knowledge of species tios, and geographic range of floral dimorphism. from cultivated plants. 7.) There is a deficiency of Amer. Journ. Bot. 79: 1382-1388. detailed botanical investigations (e.g., systematic MAUSETH, J. D., AND W. HALPERIN. 1975. Hormonal monographs and population studies) focusing on control of organogenesis in the various genera within the opuntioid group. (Cactaceae). Amer. Journ. Bot. 62: 869-877. Rebman & Pinkava: Opuntia cacti of North America 483

MAYER, M., J. REBMAN, AND L. WILLIAMS. 2000. Molec- PINKAVA, D. J., AND B. D. PARFITT. 1982. Chromosome ular evidence for the hybrid origin of Opuntia prolif- numbers in some cacti of western North America— era (Cactaceae). Madroño 47: 109-115. IV. Bull. Torrey Bot. Club 109: 121-128. MCCARTEN, N. 1981. Fossil cacti and other succulents PINKAVA, D. J., J. REBMAN, AND M. BAKER. 1998. Chro- from the late Pleistocene. Cact. Succ. Journ. (U.S.) mosome numbers in some cacti of western North 53: 122-123. America—VII. Haseltonia 6: 32-41. MCFARLAND, J. D., P. G. KEVAN, AND M. A. LANE. 1989. PINKAVA, D. J. 2001 (ined.). The Opuntioideae (Cacta- Pollination biology of Opuntia imbricata (Cactaceae) ceae). In Editorial Committee. Flora of North Amer- in southern Colorado. Can. Journ. Bot. 67: 24-28. ica. Oxford Univ. Press, New York. NEGRÓN-ORTIZ, V. 1998. Reproductive biology of a rare POWELL, A. M., A. D. ZIMMERMAN, AND R. A. HILSEN- cactus, Opuntia spinosossima (Cactaceae), in the BECK. 1991. Experimental documentation of natural Florida Keys: why is seed set very low? Sex. Plant hybridization in Cactaceae: Origin of Lloyd's Hedge- Reprod. 11: 208-212. hog Cactus, Echinocereus (lloydii. Plant Syst. Evol. NISBET, R. A., AND D. T. PATTEN. 1974. Seasonal tem- 178: 107-122. perature acclimation of a prickly-pear cactus in REBMAN, J. 1995. Biosystematics of Opuntia subgenus south-central Arizona. Oecologia 15: 345-352. Cylindropuntia (Cactaceae), the chollas of Lower OSBORN, M. M., P. G. KEVAN, AND M. A. LANE. 1988. California, Mexico. Ph.D. dissertation. Arizona State Pollination biology of Opuntia polyacantha and University, Tempe, AZ. (Cactaceae) in southern Colo- REBMAN, J. 1998. A new cholla (Cactaceae) from Baja rado. Pl. Syst. Evol. 159: 85-94. California, Mexico. Haseltonia 6: 17-21. PARFITT, B. D. 1985. Dioecy in North American Cacta- ROBINSON, H. 1974. Scanning electron microscope stud- ceae: A review. Sida 11: 200-206. ies of the spines and glochids of the Opuntioideae PINKAVA, D. J., M. A. BAKER, B. D. PARFITT, M. W. (Cactaceae). Amer. Journ. Bot. 61: 278-283. MOHLENBROCK, AND R. D. WORTHINGTON. 1985. ROSS, R. 1981. Chromosome counts, cytology, and repro- Chromosome numbers in some cacti of western duction in the Cactaceae. Amer. Journ. Bot. 68: 463- North America—V. Syst. Bot. 10: 471-483. 470. PINKAVA, D. J., AND M. G. MCLEOD. 1971. Chromosome VALIENTE-BANUET, A., A. ROJAS-MARTÍNEZ, M. DEL numbers in some cacti of western North America. CORO ARIZMENDI, AND P. DÁVILA. 1997. Pollination Brittonia 23: 171-176. biology of two columnar cacti (Neobuxbaumia mez- PINKAVA, D. J., M. G. MCLEOD, L. A. MCGILL, AND R. C. calaensis and Neobuxbaumia macrocephala) in the BROWN. 1973. Chromosome numbers in some cacti of Tehuacan Valley, central Mexico. Amer. Jour. Bot. 84: western North America—II. Brittonia 25: 2-9. 452-455.