Yosef Mizrahi, Avinoam Nerd, Park S. Nobel
Horticultural Reviews. (1997)18: 291-320.

I. INTRODUCTION

In a stimulating article, Vietmeyer (1990) pointed out that relatively few plant species, most of which were domesticated thousands of years ago, serve as food for humans and animals, as medicinal plants, and as industrial crops. Other species may be the new crops that will tolerate the changing climatic conditions on earth-global warming and locally dryer conditions as a result of atmospheric CO² increases-serving in marginal, infertile, dry lands where common crops fail. Such new crops can provide diversification to enable sustainable agricultural systems and can offer commercial opportunities. Cacti may have the proper characteristics to fulfill such roles.

Cacti are native to North and South America and the West Indies (Gibson and Nobel 1986). They are known around the world as unusual looking plants coming from hot, dry, and hostile desert areas. The dicotyledonous family Cactaceae has 122 genera with approximately 1600 species, nearly all of which characteristically have spines and exhibit stem succulence (Gibson and Nobel 1986; Nobel 1988). Of the three subfamilies, the smallest (Pereskioideae) contains about 20 species, all of which have prominent leaves. About 250 species occur in the Opuntioideae, about half of which are platyopuntias with flattened stem segments known as pads or cladodes, including the widely cultivated Opuntia ficus-indica  (L.) Miller. The remaining cacti, which are in the Cactoideae, are diverse in morphology and include small collectable species (e. g., in genus Mammillaria ), barrel-shaped species, tall columnar species, and epiphytic vine-like species that climb on other plants (Nobel 1994). Cacti appear in various habitats, from harsh hot deserts through tropical rain forests to cold areas with freezing temperatures. Most cacti grow in and arid semiarid zones with high summer temperatures; indeed, they are among the most tolerant of high temperatures of all plant species, tolerating 50 to 55^° C when properly acclimated. Unfortunately, many species of cacti with agricultural potential are damaged by freezing temperatures, such as epiphytic cacti in the genera Hylocereus   and Selenicereus   that are native to tropical forests. Cacti shows great adaptability to various soil conditions as they can grow in poor, infertile desert soil and have tolerance to wide range of soil pH (Nobel 1988). Their remarkable adaptability together with the their unique shapes, sizes and appearances have spread cacti around the world.

Cacti were introduced into the Maditerranean region as early as the sixteenth century, when ships returned from the newly "discovered" America carrying cladodes of Opuntia. Today, O. ficus-indica   andother species of this genus grow so well around the Mediterranean Sea that many consider them to be natives. Yet special care should be taken when introducing plants from one area into another, especially plants as adaptive as cacti. Introduced cacti have become dangerous weeds, as in the famous case of Australia. In 1832 platyopuntias were used as hedges north of Sydney, and in 1839 a single specimen of Opuntia stricta   was introduced into Sydney as an ornamental. They became naturalized and could not bere moved by plowing, since cutting the cladodes increased the number of propagation units and enhanced the spreading. Birds also spread the seeds. To make things worse, in 1914, Burbank's collection of various opuntias was introduced into Australia as forage. By 1925 prickly pear cacti suchas O. ficus-indica, O. stricta , and O. vulgaris   were infesting range lands in a rate of 100 ha/hour and 10 million hectares were infested in Queensland (Nobel 1994). Not until the natural insect enemy of the secacti, Cactoblastis cactorum , was introduced from Mexico were they controlled. Similar occurrences happened in South Africa, indicating the strong adaptation of the Cactaceae to various conditions.

Today, cacti are grown in most countries around the world. There are many national societies of cactus enthusiasts. Germplasm exchange is becoming increasingly common, and journals on cacti are published in many countries. Because of the beauty of their flowers and the uniqueness of their shoots, they are important indoor and outdoor ornamentals and gardening plants, as seen in the Huntington Botanical Garden in Pasadena, California. There is also a whole industry of cacti as ornamentals, mainly as potted flowering plants. For example, the Christmas cactus Schlumbergera truncata   and the Easter cactus Rhipsalidopsis gaertneri   are widely enjoyed, and manuals exist for their cultivation. Ornamental cacti deserve an entire chapter and are not be covered in this review.

Cacti increasingly serve as agricultural and industrial crops, including as animal feed, vegetables, and fruits. Cacti are most widely used in Mexico, which has a cactus as part of its national emblem, as depicted on its flag and coins. Much research on cacti has been done in Mexico, although most of the resulting publications are not widely disseminated or translated into other languages. In 1992, the Food and Agricultural Organization of the United Nations (FAO) established the "cactus pear network" with the aim of promoting the cactus pear as important fruit crop worldwide, and a comprehensive book on cactus pear has been published by FAO (Barberaet. al 1995). This review describes the biology of this interesting family of plants and discusses the potential of various species of cacti that may serve as important crops.

II. BIOLOGICAL CHARACTERISTICS OF CACTI

A number of books on the biology of cacti are available (Gibson and Nobel 1986; Nobel 1988, 1994; Pimienta-Barrios 1990). In this review, only certain aspects of cactus biology relevant to horticulture are emphasized, including the special structures and physiological processes; reproductive biology is discussed elsewhere in this volume (Nerd and Mizrahi 1996).

A. Shoots, Crassulacean Acid Metabolism

The most distinguishing vegetative feature of the Cactaceae is the areole, which occurs on a raised portion of the stem referred to as a tubercle or on a rib, which is a linear array of fused tubercles (Gibson and Nobel 1986). Areoles have meristematic activity and produce spines, including the nasty thin deciduous spines termed glochids that are a characteristic of opuntias (nasty because they contain barbs that cause glochids to become implanted in the skin of anyone who carelessly touches a cladode or unbrushed platyopuntia fruit). An areole can also produce another organ, such as a new cladode or a fruit (or even an entire plant). Cactus fruits also have areoles on their surfaces; an areole of the fruits of O. ficus-indica   can even produce an entire new plant, underscoring the many possibilities for vegetative reproduction among cacti.

The massiveness of the stems of cacti indicates that considerable amounts of water can be stored in their shoots. Indeed, such water storage can keep certain opuntias and barrel cacti alive for up to 3 years in the absence of water uptake from the soil (Nobel 1988). Perhaps more importantly, stomata opening and net CO² uptake can occur for 2 to 7 weeks for such cacti without uptake of soil water, because metabolic activity then relies on water stored in the stems. Succulence also occurs at a cellular level for cacti, because the cells typically contain a large, water-filled, central vacuole that can represent 85 to 90% of the cell volume.

The large central vacuoles suggest the most unusual feature of cacti among cultivated plants-they utilize a pathway for CO2 fixation known as Crassulacean acid metabolism (CAM). CAM was originally discovered in the Crassulaceae about 200 years ago based on nocturnal increases in tissue acidity detectable by human taste buds; CAM occurs in about 7% of the approximately 300. 000 species of vascular plants (Nobel 1988, 1994). Essentially all CAM plants evolved in water-limited environments, such as in deserts or within tree canopies without access to large soil volumes. Water loss rates for plants depend on the difference in water vapor concentration (or partial pressure) between inside the leaves or stems and the ambient air, differences that average 5- to 10-fold less at night than during the daytime because of lower plant temperatures at night. Stomatal opening at night thus leads to less water loss by CAM plants than for stomata opening during the daytime by C3 and 4 plants (Fig. 6. 1A).

C3 plants have the 3-carbon phosphoglycerate as their first photosynthetic product and comprise about 92% of vascular plant species, and C4 plants have a 4-carbon acid such as malate or aspartate as their first photosynthetic product and comprise about 1% of vascular plants, including many agriculturally important species (e. g., maize and sorghum).

A widely held view is that CAM species grow slowly. This is certainly true for various species of Mammillaria , which may be only 15 cm tall after growing for 100 years. However, the CAM pathway is only slightly more costly in terms of utilization of light energy for net CO2 uptake than is the C4 pathway and actually is less expensive than the C3 pathway, for which 20 to 40% of the fixed CO2 is generally released by photorespiration at a high energetic cost (Nobel1991 g 1994). CAM plants therefore can take up a relatively large amount of CO2 (Fig. 6. 1B) with respect to the water lost by transpiration (Fig. 6. 1A), so their water-use efficiency (ratio of CO2 uptake to water loss) is high. Averaged over a season, the water-use efficiency in mmol CO2 per mol H2O typically is 1. 0 to 1. 5 for C3 plants, 2 to 3 for C4 plants, and 4 to 10 for CAM plants (Nobel 1988). Moreover, certain irrigated CAM plants can have an annual productivity that exceeds that of nearly all cultivated C3 and C4 species. In particular, Opuntia amyclaea Tenore and O. ficus-indica can produce an above ground dry weight of at least 45 t ha-1 yr-1 (two species of agave, Agave mapisaga and A. salmiana, and pineapple, Ananas comosus, are other CAM plants that are nearly as productive), whereas such high productivities have been recorded for only a few C3 and C4 species (Nobel 1991, 1994). Thus, certain CAM species are inherently extremely productive, which can have a major impact on future cultivation of cacti.

B. Roots, Salinity Tolerance

The roots of cacti, unlike the shoots, are non succulent. The roots are typically shallow (5-15 cm deep) and even for a large arborescent cactus occur chiefly in the upper 30 cm of the soil (Gibson and Nobel 1986). Irrigation water is generally applied only to the usual rooting depth, but excessive irrigation can force roots to lower soil layers. As the soil dries, fine lateral roots generally die, while larger roots become covered with a corky layer (periderm). The root water conductivity decreases about 10-fold during soil drying, which reduces water loss from the plant tissues to the soil (North and Nobel 1992; Huang and Nobel 1994). However, water loss to a drying soil is prevented mainly by the large decreases in soil hydraulic conductivity, which can decrease 106-fold as the soil dries and water continuity among soil particles is lost (Nobel and Cui 1992).

The many preformed root primordia (sites for new lateral roots) located beneath the periderm of the main roots grow rapidly when the soil is remoistened, increasing the water and mineral absorption capacity in a matter of days. For platyopuntias, roots generate easily from areoles in contact with the ground, so vegetative propagation can occur for cladodes laid on the soil surface as well as those placed vertically in the soil. Original plant orientation should be retained for stem cuttings of columnar cacti, whose roots develop from meristems located in the vascular cambium of the stem. For epiphytic cacti, such adventitious roots can be formed all along the stem and emerge through its epidermis (Gibson and Nobel 1986). Although root generation in cacti is easy, the time varies from weeks to months, is species and temperature dependent, and can be accelerated by externally applied hormones.

Salinity stress has two major components: water stress and ion toxicity (Mass 1986). Cacti are relatively tolerant of water stress but are sensitive to salinity (Nobel et al. 1984; Berry and Nobel 1985; Silverman et al. 1988; Nerd et al. 1991a, 1993b). When salinity occurs in the natural habitats of certain species such as Cereus validus Haworth, the roots dieback and uptake of Na⁺ is avoided (Nobel et al. 1984; Nobel 1988). Ca²⁺ can often negate the toxic effect of Na⁺ (Rengel 1992). Indeed, when cacti are irrigated with water in which the ratios of Na⁺ to Ca²⁺ + Mg²⁺ and of Cl^- to (SO₄)^2- are low, they do not suffer from salinity stress (Nerd et al. 1993b). When Ca²⁺ is not abundant in the soil or the irrigation water, gypsum can be added to reduce salinity stress. Despite their drought tolerance, most cacti are commercially unsuitable to saline areas, unless special precautions regarding water and soil are taken, such as can be best learned from local field trials. The few genotypes of Opuntia  that exhibit salt tolerance should be used in breeding programs.

III. CACTI AS ANIMAL FEED

Wild and domestic animals eat cactus stems, especially species of the subgenus Opuntia (Russell and Felker 1987a; Nobel 1994). Their high water-use efficiency makes certain opuntias ideal feed crops for semiarid regions where drought is common and animal food is scarce. For high-density plantings (24 plants m-1.) and under proper management including irrigation, yields of 40 to 50 t aboveground dry weight ha-1, yr-1 can be obtained for platyopuntias, as already indicated (Nobel 1991, 1994).

Similar biomass yields occur only among the highest producing C3 and C4 plants, which have a much lower water-use efficiency. Besides opuntias grown for harvesting to provide fodder for cattle and other animals, cactican be used as forage by free-ranging cattle.

In cases where animals are allowed to graze opuntias, the spines can be burned off before the cladodes are eaten. This requires specialized burners with attendant costs of the propane fuel (Maltsberger 1991). In southern Texas this option is 30 to 40% cheaper than the cost of available relief food provided during drought (Russell and Felker 1987a). Although spineless genotypes are available, they are generally less resistant to drought. Indeed, the ranchers prefer the spiny types, because livestock do not generally consume the unburned cladodes, which remain untouched until needed. If range cattle had access to spineless genotypes, they would be consumed in preference to the native grasses and thus eliminated. Although spines can also be burned off for cladodes used as fodder, mechanically chopping the cladodes, sometimes followed by fermentation, also makes them palatable to livestock (Fuentes-Rodriguez 1992).

Although confusion exists in the taxonomy of opuntias used as animal feed, Opuntia ficus-indica is the most common species worldwide (Russell and Felker 1987a), O. lindheimeri Engelm, is used in southern Texas (Maltsberger 1991; Nobel 1994), and O. rastera Weber, O. robusta Wendland in Pfeiff., O. engelmanii Salm-Dyck, O. megacantha Salm-Dyck, and O. phaeacantha Engelm. are used in Mexico (Fuentes-Rodriguez1991). When these plants are not cultivated, yields tend to be much lower than the maximal possible but are still higher than yields for C3 or C4 plants grown under drought and otherwise harsh conditions (Nobel 1994).

Growth conditions affect the quality of cladodes as an animal feed, so nutritional analysis should be made on such feed before use (Maltsberger1991). Cladodes consist mainly of water, usually about 85 to 95% by fresh weight (Fuentes-Rodriguez 1991), but during water stress the water content may drop to 60% (Nobel 1994). In nutritional value, cladodes are similar to immature maize silage on a dry matter basis (Maltsberger 1991); they are relatively high in fiber (average of 18%) and minerals (19%), low in fats (1-4%), and medium in proteins (generally 4-8% total, with 1-2% digestible). Digestibility of cladodes is high (72%), and carbohydrates can account for up to 71% of their dry weight (Fuentes-Rodriguez 1991, 1992; Maltsberger1991). Like many other green plant tissues, cladodes contain carotene (a precursor to vitamin A), and vitamin C. Protein supplementation should always be considered (e. g. , cotton seed, which is available in southern Texas and elsewhere, is a good source). Micro- and macronutrient supplementation should also be considered (Maltsberger 1991). The content of nitrogen and other minerals in cladodes can be increased by fertilization (Nerd and Mizrahi 1992; Nerd et al. 1993a). A clone of Opuntia stricta Haworth has been identified with high nitrogen and phosphorus contents that satisfy the feed requirements of cattle (Nobel 1994). The laxative properties of cladodes can be avoided by gradually increasing the cladode portion in the feed (Maltsberger 1991). Because consumption of cladodes can improve the flavor of milk and the color of the butter produced from it, milk from cladode-fed cows commands higher prices in Mexican markets (Russell and Felker 1987a).

Numerous countries (Mexico, Brazil, United States [mainly Texas], Peru, Chile, South Africa, and Tunisia) are already producing significant amounts of animal feed from opuntia cladodes (Nobel 1994), reflecting their low maintenance cost, efficient production, and sustainability (Hamilton 1992). Selected cultivars of opuntias with high yields and high-quality cladodes should play an increasingly important role in the livestock industry on a regular basis, not just as a drought relief source of feed. With the proper management, these cacti can be a competitive source of feed, especially where water shortage is a problem. However, a major problem for the expansion of the cultivation of cacti in the United States and other countries is the plants' sensitivity to freezing temperatures (Russell and Felker 1987b). Most members of subgenus Opuntia growing in the wild or cultivated are heavily damaged by nighttime temperatures of -10° C, although certain wild opuntia species growing in northern latitudes can tolerate temperatures below -20° C when properly acclimated, such as Opuntia fragilis (Nutt.) Haworth and O. humifusa (Rafinesque) Rafinesque, both of which are native to Canada (Nobel and Loik 1990; Loik and Nobel 1993). Indeed, breeding efforts between cold-tolerant native species and highly productive but cold sensitive commercial species should be a major objective of programs to expand the cultivation of cacti (Nobel et al. 1995; Nobel 1996).

IV. CACTI AS VEGETABLES

A traditional vegetable of Mexico is the nopalito, the name for the young cladodes of various species of platyopuntia, such as Opuntia -ficus-indica, O. streptacantha Lem., O. amyclaea, O. robusta, O. inermis DeCandolle, and Nopalea cochenillifera (L.) Salm-Dyck (Cantwell et al. 1992; Flores 1992; Pimienta-Barrios 1993). This unique vegetable, which usually is roasted, blanched, or cooked after the spines and the young leaves are removed, has great potential for other countries as well. Nopalitos are sold in the Mexican markets in several forms, the simplest being the freshly harvested cladodes. Often they are sold after the spines, young leaves, and edges are sliced off and sometimes after being cut into strips or small cubes. This vegetable is utilized in many forms, including salad sand cooked dishes with meat. Even a delicious cactus pie can be prepared, which tastes apple-like, perhaps reflecting the high malic acid levels in both apples and nopalitos (Master 1959).

The nutritional value of nopalitos is similar to that of many other vegetables; they contain mostly water (88-95%), some carbohydrates (3-7%), and minerals (about 1. 3%, mainly Ca2+) . Like most leafy vegetables, nopalitos are low in proteins (about 1%) and fiber (about 1%, which is still more than twice that of lettuce; Rodriguez-Felixand Cantwell 1988). They are a typical source of two important vitamins, -carotene (18-38 mg per 100 g fresh weight) and ascorbic acid as vitamin C (10-18mg per 100 g fresh weight). Nopalitos are less nutritious than spinach but more nutritious than lettuce (Cantwell 1991). Mucilage, which is secreted from the cut ends of the cladodes, deters some potential consumers but can be minimized by boiling in water for a few minutes with some sodium bicarbonate or salt. Consumption of nopalitos can reduce the blood sugar levels in diabetics who are not insulin dependent (Ibanez-Camacho and Roman-Ramos1979; Meckes-Lozoya and Roman-Ramos 1986; Frati et al. 1983, 1988, 1989, 1990) and also can reduce fats and cholesterol, especially the low-density cholesterol (Frati et al. 1983; Fernandez et al. 1990, 1992), underscoring the great potential of nopalitos as a crop.

Nopalitos come to Mexican markets from wild as well as backyard plantsof various species, from established orchards where the plants are grown as for fruits (Rodriguez-Felix and Cantwell 1988), and from special plantations with dense plantings to maximize vegetative production. "The Nopalitos Capital" is Milpa Alta, where high-quality cultivars, mainly of O. ficus-indica, are grown. The cladodes are traditionally bailed in round bundles (Color Plate 1) before being sent to the markets. Over 5000 ha of nopalitos are cultivated in Mexico (Pimienta-Barrios 1993); the limited plantings in the United States are mostly in southern California and Texas, where the main cultivated species is Nopalea cochenillifera. Cladodes of the specific cultivar of N. cochenillifera are spineless and less mucilaginous, greener, and more tender than those of the various Opuntia species grown for nopalitos. Young cladodes of N. cochenillifera are often sold in U. S. supermarkets under a botanically incorrect term, "cactus leaves" (cladodes are stems).

Fig 1. Young cladodes (nopalitos) of Opuntia ficus-indica in a traditional round pack in Milpa Alta, ready to be shipped to a Mexico City market.

Photo 28. Сactus salade link

Photo 29. Nopalitos link

Although more research is needed on its growth and management (Mick1991, 1992), N. cochenillifera is planted as cuttings with about20 cm between individual cladodes along rows in soil beds with 8 rows about20 cm apart. Fifty cladodes can be harvested in one year from a single cladode planted in the spring (the first harvest is obtained in 3-4 months). High fresh weight yields of 400 to 600 t ha-1yr-1 are possible under the severe pruning that stimulates vegetative growth. Cultivar 1308 is sensitive to freezing temperatures, so it is grown under plastic tunnels filled with straw during the wintertime risk period, when ambient outside temperatures can be -10° C. These tunnels are also used to lengthen the cladode production period in the spring and autumn, when outside temperatures are too low (Mick 1991)(Color Plate 2).

Fig 2. Oputnia ficus-indica growing in a soil bed with tunnel for year-round production of nopalitos in Milpa Alta, Mexico.

Opuntia ficus-indica, O. inermis, and O. amyclaea can have young cladodes that are low in spines. These nopalitos reach their market size of about 20 cm in length within 20 to 30 days, depending on the weather. The shelf life of this vegetable is usually a few weeks, provided that proper postharvest techniques are applied (Cantwell et al. 1992). Diurnal variation in acidity because of CAM metabolism can impose a unique postharvest problem, because morning-harvested cladodes are very acidic, whereas afternoon-harvested cladodes contain only 10 to 20% as much acidity (Rodriguez-Feliz and Cantwell1988). The acidity of harvested cladodes decreases with time and after1 week of storage at 20° C reaches a plateau (Cantwell et al. 1992), so packages should be marked with the earliest day for consumption to guarantee consistent acidity levels in the cladodes. Proper marketing and consumer information about their quality and many uses are essential before the tremendous potential of nopalitos will be realized worldwide (Flores 1991. 1992). Several books and leaflets have been published describing the many dishes that can be prepared from nopalitos, such as, Cookin With Cactus (Haggerton1992).

The bases of the flower buds of N. cochenillifera (Color Plate3) can also be used as a tasty vegetable (L. Scheinvar, Autonomous University of Mexico, Mexico City, personal communication). The flower base contains glochids that must be removed before use, suggesting that the absence of spines and glochids from the cladodes of N. cochenillifera is controlled by other genes.

Fig 3. Flowering plant of Nopalea cochenillifera, whose spineless cladodes are used for nopalitos and whose glochid-containing flower bases (reseptacles) are used as a delicate low-mucilage vegetable.

When this species is grown for nopalito production with intensive cladode removal, flower buds are generally not formed, although much about N. cochenillifera remains to be determined by future research. Another cactus used as a vegetable in Mexico is Acanthocereu stetragonus (L.) Humlk. (L. Scheinvar, personal communication), which is an epiphyte that may require a trellising system and shade. This cactus lacks mucilage, which may make it more attractive to potential consumers than nopalitos. Basic agricultural research is needed before exploiting A. tetragonus as a crop, which is also true for the leafy nonsucculent cactus Pereskia grandiflora, whose young stems are cooked as a vegetable in Vietnam (N. T. Nguyen, University of Hanoi, personal communication).

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LITERATURE CITED

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