Candelario MONDRAGÓN-JACOBO and Salvador PÉREZ-GONZÁLEZ
Instituto Nacional de Investigaciones
Facultad de Química
The nopal or opuntia is generally recognized as a fruit crop for semi-arid subtropical conditions around the world, although it is grown commercially for this purpose only in five countries: Chile, Italy, Mexico, South Africa and USA. However, it is more important as a forage and fodder plant, considering the extent of wild and cultivated areas in countries where it is a native plant, as well as where opuntia has become naturalized. Statistics on worldwide estimated area range from >687 000 ha (Nobel, 1994) to 2.3 million ha (De la Cruz, 1994), the latter figure includes low-density populations scattered across northern Mexico. It has been estimated that 92% of these resources are potentially useful as stock feed.
Two anatomical features of the plant imply that acceptance of opuntia fruit in the international market could be slow and perhaps limited: the actual fruit quality (i.e. seediness) and the peel glochids. The presence of thorns on the most productive and high quality fruit cultivars discourages new growers in non-traditional growing areas. For vegetable use, the mucilage seems to be the most important limiting factor for new consumers. Utilization as a fodder or forage, however, seems to be more feasible. Opuntia can provide a continuous, valuable supply of fresh fodder during the dry season, given its succulent non-deciduous vegetative structure, a feature rarely found in other forage species. The fodder will in turn be transformed into more prized commodities: milk, meat, leather and wool.
Animal husbandry on a limited scale is a common survival strategy in semi-arid lands. In many countries, domestic animals also represent social status, because they are an asset that can be readily utilized. Pastoral societies are present in all arid and semi-arid undeveloped regions of the world, making intensive use of native grasslands. As a result, depletion of grasslands is a widespread problem around the semi-arid belt of the world, contributing to desertification. The search for plants that can withstand climatic constraints and help stem land deterioration is continuous. In this context, opuntia has interesting potential, as already shown in its centres of diversity and many other areas of the world that, for historical reasons, have benefited from opuntia introduction and dispersal.
Systematic collection and characterization of germplasm from native as well as naturalized populations, and continued efforts at breeding, are needed to find new selections and to develop new cultivars for desertified areas, areas that currently are running out of options to recover their biological productivity.
Attempts to breed opuntia date back to the early 1900s, when Luther Burbank in California envisioned the development of spineless varieties for fodder (Dreyer, 1985) that could be cultivated around the globe and make productive vast tracts of barren land. It is noteworthy that opuntia entered the international scene as a fodder crop, contrasting with its traditional utilization as a fruit and vegetable plant in Mexico.
In this chapter we review the importance of the germplasm base of fodder and forage opuntia, the extent of its variability and utilization, and the need for long-term conservation efforts. The techniques, research progress, breeding constraints and goals associated with developing fodder varieties are also discussed.
Natural hybridization of opuntia is common. It is related to polyploidy and appears to be one of the major causes of diversity. Asexual reproduction is an adaptive answer to the low germination rates and seed predation found in this group (Del Castillo, 1999). Hybridization in natural populations of Southern California was elucidated by Walkington (1966, cited by Gibson and Nobel, 1986) based on morphological and chemical studies. These findings indicated that plants of Opuntia occidentalis came from a cross between two native platyopuntias: O. ficus-indica and O. megacantha. The hybrid was reported as having features of both parents. Scheinvar (1995) reported that in wild populations of opuntias, plants located in the periphery of the population show greater variability than those growing in the middle, probably due to a greater exposure to genetic exchange with other species and genotypes.
Partial as well as total cross-pollination is found in cultivated accessions; thus cultivated types are likely the result of cross-pollination. All Mexican cultivars are reported as products of hybridization of O. ficus-indica with different wild opuntia forms (Pimienta-BarRíos and Muñoz-Urias, 1995).
Opuntia flowers are also capable of self-pollination, and bagged flowers are able to set fruit (Nerd and Mizrahi, 1994). Self-pollination was confirmed by Wang et al. (1997) with a hybridization trial involving six Opuntia species. The success of self-pollination is also confirmed in commercial orchards, where large blocks of a single cultivar set fruits and seeds without the apparent need for special pollinating varieties, as reported by Damigella (cited by Nerd and Mizrahi, 1995, and Mondragón, 1999).
Opuntia flowers are hermaphrodite, but they can be emasculated and isolated with some difficulty to perform controlled crosses. Opuntia breeding principles and techniques were described by Mondragón and Bordelon (1998) and Mondragón (1999), some refinements to the techniques were added by Bunch (1997). The following steps are taken when emasculating opuntia flowers: (1) brush the glochids from the exterior of the buds to allow easy handling; (2) excise the corolla, using as few strokes as possible, thereby avoiding wounds and mechanical damage to the style; (3) carefully remove the stamens and anthers, cutting close to the base; (4) rinse thoroughly with clean water to get rid of residual pollen and anthers; (5) clean the wounded surface with a paper towel; (6) allow 15-20 minutes to promote drying of the wounded tissues; (7) cover the flower with a glassine or paper bag, and seal it with a rubber band; and (8) label.
The seeds are extracted from ripe fruits, then washed and sun-dried. Disinfection with diluted (10%) commercial bleach is recommended before planting. Germination is enhanced by scarification, i.e. immersed in hot water at 80°C and allowed to cool off at room temperature, followed by overnight soaking. The seeds can be planted in standard germination media. High temperatures (30-35°C) and regular irrigation are needed to attain good germination rates (Mondragón, 1999). Germination starts after a week, but can continue for up to two months, depending on seed condition, cultivar and species.
Once the first cladode attains 5-10 cm they can be transplanted to small plastic bags or pots and placed in a nursery. Plant growth in the nursery can be accelerated by providing long-day illumination and fertigation. Plants having a second cladode (25-40 cm total height) are mature enough to tolerate field conditions, but still they are sensitive to frosts, therefore they should be planted after any risk of chilling temperatures is over.
The ability to generate apomictic seedlings derived from the nucellar tissue of the seed and the length of juvenility are the most important constraints for opuntia breeding. Apomixis has been reported in several species of Opuntia, including O. aurantiaca Lindl., O. dillenii Haw., O. glaucophyla Wendl., O. leucantha Link., O. rafinesquii Engelm., O. tortispina Engelm., and O. ficus-indica (L.) Mill. (Tisserat et al., 1979). Within cultivated opuntias, apomixis is also a widespread phenomenon. Mondragón (1999), working with 17 breeding populations of Mexican origin grown under greenhouse conditions, found that all entries produced maternal seedlings, though at different rates. An exploratory trial of apomicts identification with phenotypic and molecular markers was also conducted. Seedlings emerging late were found to be associated with a random amplified polymorphic DNA (RAPD) banding pattern similar to that of the maternal entry, providing a tool for early screening of apomictic seedlings.
Another effective approach to separate sexual seedlings has been used by the Italian breeding programme. Assuming that the largest embryo present in the seed is of sexual origin, they are rescued from the seeds and grown in nutrient media (Chessa and Nieddu, 1999) thereby increasing the number of zygotic individuals for field evaluation.
Opuntia can reach the reproductive stage after the second to fifth year of planting when started from cuttings, according to cultivar and growing conditions. Plants derived from seeds of a cross between cv. Cristalina and cv. Reyna (both of which set fruit after the third year when propagated from cuttings) under optimum conditions in northern Guanajuato, Mexico, also started bearing fruits at the third year (Mondragón and Fernandez, unpub. observation). However, some important traits that qualify a fodder cultivar - including nutritional value, digestibility and lack of spines - can be evaluated after the second year of planting. To evaluate plant productivity, fully-grown cuttings can be obtained at the end of the second year (Mondragón, personal observation).
Numerous opuntia species are utilized as forage in northern Mexico. Fuentes (1991) and Flores and Aranda (1997) reported the use of 10-18 species, 15 of which are platyopuntias. O. streptacantha, O. megacantha, O. leucotricha, O. robusta, O. rastrera, O. lindheimeri, O. engelmannii, O. cantabrigiensis, O. macrocentra and O. phaeacantha are the most important regarding abundance, distribution and preference by ranchers. The most frequently used are O. engelmannii and O. lindheimeri (De la Cruz, 1994). All the above-mentioned species are thorny and have to be processed for more efficient use. O. robusta presents spiny and spineless types, but individuals with smooth pads are predated by rodents during the juvenile phase and are not usually found in the wild. O. ellisiana is valued in South Texas and used in situ after burning off the spines (Felker, 1995).
Even some obnoxious species harmful to livestock, like O. mycrodasys (or blinding prickly pear, named after the damage caused by the numerous glochids) are consumed when other species become scarce (De la Cruz, 1994). Varieties of all species can be found close to the original stock, originated by chance seedlings of sexual origin. Most of the wild accessions have been reported as having low ploidy levels (4x and 6x), although O. streptacantha cv. Cardona presents 2n = 2x = 88, as observed by Muñoz-Urias et al. (1995).
The utilization of whole plants to feed cattle is endangering wild populations of opuntia in northern Mexico. Too often, they are completely uprooted to increase the collected volume and monetary income, severely diminishing the chances for recovery. The problem cannot be solved easily because the plants are harvested to be utilized in suburban dairy operations, far away from the native locations and benefiting other users, besides the landlords. The germplasm available in these areas has been barely evaluated and the risk of loss of valuable individuals is a real threat. The effects on opuntia variability can be disastrous and permanent. An initiative to enforce rational utilization and in situ conservation of wild opuntia is needed, along with intensive efforts to rescue useful germplasm.
Backyard orchards containing opuntia are commonly seen in semi-arid central Mexico. They represent an intermediate stage in opuntia domestication, and were also the source of propagules for the earlier commercial orchards (Pimienta-Barrios, 1990). Fruit clones are important in these sites, but clones for multiple use - fruit and vegetable, fodder and vegetable, etc. - are also present in these domestic collections. Mixed stocks of spiny and spineless genotypes are widely available. Plants in the yard represent feedstuff readily available for domestic livestock during the dry season. Spineless genotypes are preferred for easier handling.
The family orchards are the best sites to find individuals of sexual as well as clonal origin growing in close vicinity. Opuntia is capable of cross-pollination, allowing the possibility of chance seedlings derived from natural crosses. In these places, seedling predation may be lower and growing conditions are improved by waste water and manure of domestic animals. Collection efforts in Mexico have been focused mainly in backyards, but a complete evaluation of suitability as fodder and productivity under cultivation is lacking.
Hybridization in opuntia was first claimed by Luther Burbank in the early 1900s, which led to the development of the so-called spineless cactus. Burbank saw it as having immense potential for cattle forage in desert areas. Several cultivars were developed, and Burbank aggressively marketed five of them (Dreyer, 1985). They were said to be the product of extensive crossing and selection among accessions shipped from Mexico and other countries. Today, four of these cultivars still remain in the South African collection.
Disregarding the obvious importance of opuntia as a valuable resource for Mexico, the plant remained nearly forgotten by the Mexican scientific community for more than half a century. Formal breeding was initiated in Mexico in the 1960s. The Universidad Autónoma Agraria Antonio Narro initiated research, selecting for cold-hardy Opuntia (Martinez, 1968, Borrego et al., 1990). During the same decade, the late Dr F. Barrientos of the Colegio de Postgraduados de Chapingo pioneered the first hybridizations of opuntia in Mexico.
The COPENA series of cultivars were developed by the Colegio de Postgraduados of the Escuela Nacional de Agricultura. Cvs CPF1, CPF2 and CPF3 were selected for fodder production, and cv. CPV1 for vegetable use (Barrientos, 1965a, b), but all belong to O. ficus-indica. The mature pads of CPV1 are useful as fodder. Currently, only CPF1 and CPV1 can be found, planted in small plots in central Mexico.
COPENA F1 or cv. CPF1 produces long, thin, green pads, excellent for human consumption when tender. The fruits of this cultivar are light green, with thin pericarp and a slight blush. Under rainfed conditions, at least one flush of pads per growing season is produced. Cv. CPV1 is a vegetable cultivar whose mature pads can also be used for fodder.
Cv. Pabellón has ovoid, thick, dark green pads; adult plants produce red tasty fruits similar to the fruits obtained from cv. Roja Lisa, a fruit cultivar. It is probably a selection from Aguascalientes, Mexico. Both entries are now available in most of the germplasm banks recently formed.
Cvs ANF1 and ANV1 are cultivars developed during the 1960s by the Universidad Autónoma Agraria Antonio Narro (UAAAN). Described as spineless and suitable for fodder production, plantations were promoted primarily in northern Mexico, but with limited success, probably due to the lack of interest in opuntia cultivation for fodder production as a result of the abundance of the wild resource. They are only available at the source.
Northeast Brazil is the most important growing area for fodder opuntia in the world. Cvs Palma Gigante and Palma Redonda (both O. ficus-indica Mill.) are widely cultivated in dry areas. Together with cv. Palma Miuda (Nopalea cochinellifera Salm-Dick), which tolerates more humid conditions, they are the mainstay of commercial production of this crop.
These cultivars have small and sweet fruit without commercial importance. They were introduced to Brazil by the Portuguese during the colonial era. IPA-Clone 20 was selected from open pollinated seeds of Palma Gigante (O. ficus-indica Mill.). In field trials, IPA-Clone 20 produced 50% more fodder than the maternal entry (Arruda and Warumby, 1999).
O. ficus-indica is believed to have been introduced to South Africa at least 250 years ago (Zimmerman and Moran, 1991), giving this country the oldest record of opuntia introduced as a fodder crop. Modern introduction started in 1914, including 22 entries: 19 green leafed and three blue leafed accessions, by way of true-to-type seed. From this initial collection, and assuming cross-pollination, numerous crossbred cultivars have been found. These selections were obtained by Luther Burbank in California from material collected in Central America (Wessels, 1988).
The selections Robusta, Monterey and Chico, described as blue-leafed spineless cultivars (probably O. robusta, based on the bluish hue of the cladode and the red fruit and flesh) were imported to South Africa as seed from Burbank Nurseries, to be cultivated as stock fodder (Wessels, 1988). Robusta and Monterrey are highly productive, while Chico presents some cold resistance. All spineless or Burbank opuntias bear tiny bristles (glochids) around areoles and on the fruit surface (Brutsch and Zimmerman, 1990).
The early efforts in selection and genetic improvement were unsustained. A fresh start at breeding is underway in Italy, Mexico, South Africa and USA, based on the utilization of local germplasm. This renewed interest, encouraged by the Food and Agriculture Organization of the United Nations (FAO), has resulted in the collection of wild and semi-domesticated accessions, publication of information on crop management practices, and development of new uses for opuntia (Barbera, 1995).
DArrigo Brothers, a produce company based in California, USA, supports a private breeding programme aimed at improving fruit quality of their spineless commercial cultivar Andy Boy (similar to cv. Rossa, which is grown and marketed in Italy). Even though they are involved in neither the development of fodder nor vegetable varieties, the programme is selecting only spineless cultivars, which could be evaluated by other parties.
Texas A&M University, Kingsville, (TAMUK) has been involved since 1982 in collection and introduction of opuntia to the USA, as well as agronomic research and extension. The programme focuses on the development of freeze-tolerant cultivars, as chill damage is a common problem in the region (Wang et al., 1997). In 1996, the first round of crosses marked the beginning of a long-term breeding programme. In 1998, the genetic material was transferred to Universidad Nacional Santiago del Estero, Argentina, where the work continued vigorously. TAMUK is also responsible for the popularization of the vegetable opuntia and opuntia products in Texas. Cv. Spineless 1308 (an accession originally collected in the humid tropical region of Tamazunchale, Mexico) has been extremely successful among growers and consumers.
Another active breeding programme is located in Sassari, Italy, involved mainly in improving fruit quality. Their interest also focuses on spineless cultivars. Additionally, the programme is working with other opuntias of ornamental value.
Opuntia breeding started in Brazil in 1985, with 85 clones obtained from seeds derived from open pollination of cv. Palma Redonda, plus 17 other clones from several Brazilian locations. Continuous introduction of genetic material from Algeria, Mexico, South Africa and USA has increased the number of entries to 1400 clones at the Instituto Pernambucano do Pesquisa Agropecuaria, (Cordeiro and Alburquerque, this volume), making it the highest number of fodder clones in evaluation anywhere in the world. Higher productivity and better nutritional value, as well as adaptation to more humid and warmer environments, are the goals of this programme.
Hybridization of cold-tolerant native species with highly productive but cold-sensitive commercial species should be a major objective of breeding programmes to expand the cultivation of opuntia (Gregory et al., 1993; Mizrahi et al., 1997). The most important opuntia cultivars are generally irreversibly injured at temperatures of -5 to -10°C (Russell and Felker, 1987b; Nobel and Loik, 1993). Certain wild Opuntia species, such as O. fragilis (Nutt.) Haworth and O. humifusa (Rafinesque), both native to Canada, can tolerate temperatures below -20°C when properly acclimatized (Nobel and Loik, 1993). Cold tolerance is an important feature for opuntia production (fruit as well as forage) in the southern USA, where freezing temperatures occur occasionally (Parish and Felker, 1997). Susceptibility to freezing is the primary factor limiting the expansion of opuntia as fodder and forage in cattle-producing areas of the USA. Russell and Felker (1987b) reported that O. ellisiana in Texas endured -9°C without apparent damage, while fruit and fodder accessions from Brazil, Chile, Mexico and South Africa presented different degrees of frost damage. The South African spineless fodder cultivars were the least affected.
In the early 1900s, Uphoff (1916) reported that species of cacti having relatively thick integuments (cuticle, epidermis, crystal-bearing layers, and several layers of thick walled cells) were more resistant to low temperature than those with thinner integuments. According to Goldstein and Nobel (1991), reduced water content and accumulation of organic solutes and mucilage may be partially responsible for cold acclimatization.
A key issue in cold hardiness is the length of the onset period of freezing temperatures, as noted by Gregory et al. (1993). In Opuntia, the lack of freeze hardiness is probably not due to the lack of tolerance to cold temperatures per se, but the range of day to night temperatures, from 28°C down to -12°C in a single day in Texas, which does not allow the plant to properly acclimatize and express cold tolerance.
Borrego et al. (1990) reported that selection for cold-hardy genotypes was initiated in the Universidad Antonio Narro in northern Mexico by Dr Lorenzo Medina in 1963, taking advantage of an unusual -16°C frost event. The best 31 individuals were selected, together with outstanding fruit and vegetable regional genotypes that also survived the frost, collected from backyards. Some of these clones were later introduced to southern Texas by P. Felker.
Parish and Felker (1997) found several promising clones in their experimental orchard at Kingsville, Texas, an area with recurrent frost and low temperatures of about -12°C. Clone 1436, obtained from Saltillo, Mexico, was found to have high yield and good fruit quality. Two other clones, 1452 and 1458, collected in northern Mexico from areas in the highlands exposed to late frosts and light snow cover, are also promising. These findings indicate the existence of genes for cold tolerance and the possibility of opuntia cultivation in colder regions.
Development of hybrids with improved cold hardiness was undertaken at Kingsville, Texas, using the spiny O. lindheimeri as a source of cold-tolerance genes (O. lindheimeri and O. ellisiana have been observed to tolerate -20°C) and spineless accessions of good fruit quality from Mexico (Wang et al., 1997). Any spineless segregant has potential to be used in cultivated conditions as a fruit or fodder cultivar.
O. robusta typically does not tolerate frost, as observed in Texas with cvs Robusta, Monterey and Chico, none of which tolerated a -12 C frost registered in 1989 (Felker, 1995).
The presence of spines on the pads is a serious impediment to widespread utilization of opuntia. Spineless pads are thought to be the result of domestication by man, because plants with smooth pads do not prosper in the wild. The inheritance mode of this trait has not been identified, but reversal of spineless back to spiny forms has been reported in South Africa. Zimmerman and Moran (1991) reported that there is evidences that only spineless forms were introduced to South Africa more than 250 years ago, and they reverted back to the original spiny form over a period of nearly 200 years. Spiny plants are more aggressive and better adapted to spread. These clues suggest the existence of recessive genes associated with spininess, and confirm the ability of opuntia to reproduce from seed. All breeding programmes aim to produce spineless forms.
Striking differences in plant vigour have been observed within seedling populations derived from selfing and crossing, suggesting that these differences are probably derived from the plants own capacity to photosynthesize as well to absorb nutrients and water. This might be expressed as a higher bud density and capacity to budbreak in spring, resulting in more cladodes per plant or larger size. It is an important selection trait, particularly if associated with spineless pads, digestibility or nutritional value.
Given that fodder production involves partial or total utilization of the vegetative structure, the capacity to produce new cladodes and to recover quickly from pruning are the more important features to be manipulated through breeding. The size of the cladodes is determined by the genotype (Mondragón, 1999), and to a lesser extent by the planting layout and soil fertility. For higher biomass yield in cultivated stands, it is preferable to have cultivars with medium-sized cladodes suitable for close planting.
Protein content varies significantly according to cladode age, with mature pads having higher percentages. The differences persist among varieties and species. Crude protein varied widely when Fuentes (1991) compared six opuntias from northern Mexico. The lowest value was observed in O. rastrera (2.8%) compared to 5.1% recorded in O. ficus-indica. The latter sample most probably was obtained from a backyard or from a commercial plantation. According to Murillo et al. (1994), differences have been observed between O. lindheimeri var. tricolor (2.81%), which has higher protein content than O. lindheimeri var. lindheimeri (4.0%). The genetic component of this trait is difficult to separate because it is strongly influenced by soil fertility and crop management. Therefore, selection for cultivars with high protein content must be conducted under carefully controlled conditions. It is doubtful that the genetic gain of protein content associated with selection can surpass the effects of efficient management of soil fertility.
There are a number of pests that affect opuntia, and variations in susceptibility to pests have been observed but not thoroughly studied. Wild cochineal (Dactilopius coccus Costa) and stinky bugs (Chelinidae tabulata) seem to prefer some spiny cultivars (Mondragón, pers. observation). Soft black rot (Erwinia sp.) is a serious disease affecting forage and vegetable plantations in Italy, Mexico and other countries, and there are no reports of tolerance among commercial varieties. Even though there are options for chemical control, tolerant cultivars would offer a safer and more economical alternative for growers.
Collection of opuntia germplasm is performed on the basis of major use: fruit, vegetable or forage. New hybrids will have to be subjected to a wider evaluation to increase the output of breeding programmes. Breeding for multiple uses is an immediate objective to be pursued by the research programmes. The suitability of tender pads to be used as a vegetable can be judged during the juvenile phase, after the first year planted in the field. Mature pads, needed to evaluate fodder potential, can be obtained after second year, without hindering the growth or development of the plants. Several combinations can be expected in regard to use: fruit+forage cultivars and vegetable+fodder, as well as the usual single-use cultivars.
Local tastes and preferences for vegetables can slow down the acceptance of tender opuntia in those countries without a tradition of human consumption of Opuntia. Therefore, the most important combination for growers - other than Mexicans - will be forage+fruit. Evaluation of protein content and nutritional value should be included as a routine for all new cultivars. There is little information on the usage of fruits as a supplement to mature pads, and the effects on the nutritional value of an opuntia-based diet, an alternative of use in countries without a tradition of fruit consumption.
The new cultivars have to be devoid of thorns to facilitate cultivation, fodder handling and feeding. Modification of cropping systems could allow the introduction of opuntia to new locations; the practice of multiple cropping based on the local staple crops will allow gradual introduction of opuntia to new growers. Outstanding spiny cultivars, which are less affected by wild rodents, can be directed towards ecological applications, such as recovery of degraded lands. Vigorous exchange of spineless genotypes among breeding programmes should be encouraged.