a small floral diameter (40-45 mm), such as Ferocactus histrix and Diadasia spp., medium-sized bees are less-frequent visitors. Instead, smaller bees (e.g., Ashmeadiella spp., 5-7 mm in body length) are the major pollinators (del Castillo 1994). These bees also are less common flower visitors for opuntias and, because of their small size, when they do enter flowers, they may do so without touching the stigma (del Castillo and González-Espinosa 1988). Cacti with small, bowl-shaped flowers, such as Epithelan-tha spp., are probably mostly autogamous and depend little on pollinators to set seed (Grant and Grant 1979c). Small bees visit the small, bowl-shaped flowers of Mam-millaria spp. Pollinators are needed even for certain self-compatible species to set seed, such as O. lindheimeri (Grant et al. 1979). Usually nectar is the main reward for bees. Some species, however, do not produce nectar, e.g., O. lindheimeri (Grant et al. 1979). Because this species coexists with nectar-producing opuntias with the same floral design, this may be considered an example of Batesian mimicry for cacti (Roy and Widmer 1999). It may also be an adaptation for moisture conservation (Grant and Hurd 1979).
The number of cacti that produce bee flowers suggests that this flower type is the most successful, or at least most common where cacti evolved. Perhaps its major disadvantage lies in the promiscuity of the pollinators, which may be a problem in areas rich in cactus diversity, where pollination among different species or genera is common (Leuck and Miller 1982; Grant and Hurd 1979; García-Sánchez 1984; del Castillo 1994). Promiscuity enhances hybridization and probably promotes evolutionary changes of the breeding system or the pollinator syndromes. A filter that maintains the individuality is the specificity of the pollination mechanisms (Linskens 1983).
Typical hummingbird flowers are red, diurnal, tubular, and zygomorphic. The stamens usually rise well above the tepals. Interestingly, this floral syndrome is more common in epiphytic cacti from humid habitats, such as cloud forests, than other cactus habitats. Many epiphytic species of Schlumbergera (McMillan and Horobin 1995), Diso-cactus, and Nopalxochia also have this floral syndrome. Opuntia spp. seems to have an interesting evolutionary transition from a bee-pollinated syndrome to the hummingbird syndrome. Some species have color variations that diverge from the typical yellow flower of many bee-pollinated cacti to red, while preserving the same floral shape (Arias-Moreno and Arreola-Nava 1995). The flowers of O. stenopetala are red, have a closed perianth, are nearly tubular, and are attractive to hummingbirds. Nopalea, which is closely related to Opuntia, has a typical hum mingbird flower and is commonly visited and probably pollinated by these birds. In addition, the South American genus Tacinga, which is intermediate between Nopalea and Opuntia, has flowers with erect and non-sensitive stamens (typical of Nopalea) and narrow, green, recurved petals (Britton and Rose 1937).
Pollination by bats occurs for columnar cacti, such as Carnegiagigantea (Alcorn et al. 1961), Neobuxbaumia spp. (Valiente-Banuet et al. 1997), Pachycereuspringlei (Fleming et al. 1994), Pilosocereus spp. (Zappi 1994), Stenocereus pruinosus (Valiente-Banuet et al. 1997), and S. stellatus (Ramírez-Mireles 1999). Bat-pollinated flowers are usually large, robust, nocturnal, white or cream, and odoriferous, and produce abundant nectar. The flowers of columnar cacti attract bees and hummingbirds during the daytime and moths during nighttime (Valiente-Banuet et al. 1997). Leptonycteris spp. are common pollinators of cacti with bat-attracting flowers, and they may consume the pollen (Alcorn et al. 1961). Symbiosis with bats has at least three advantages for cacti: (1) lower promiscuity compared to bee flowers, (2) long distance flying (Fleming et al. 1994), and (3) seed dispersal by the bats (Fleming et al. 1994; Valiente-Banuet et al. 1997).
Moths commonly visit large, nocturnal, white, discshaped flowers, which are partially zygomorphic (most of the stamens lie on one side of the flower) and have a large nectarial chamber. Many genera of epiphytic cacti, such as Hylocereus (Ramírez-Mireles 1999), Echinopsis, Epiphylum, and Selenicereus (Rowley 1980), bear these flowers. Flowers of Hylocereus open at dusk but may remain open until the next morning, when they are visited by bees and bumblebees, which appear to be the major pollinators (Ortíz-Hernández 1999; Ramírez-Mireles 1999). Nectar is a major reward for moths. In their attempt to reach the nectary, moths visiting flowers of Hylocereus leave many of their wing scales on the style, darkly staining it and thus providing an easy means for detecting moth visits (Y. Ortíz-Hernández, personal communication). Some cylindropun-tias have nocturnal disc-shaped flowers, instead of the typical diurnal bowl-shaped flowers (Grant and Hurd 1979).
Whereas bees, bats, hummingbirds, and moths are attracted by cactus flowers and pollinate them, the role of other flower visitors, such as beetles, ants, and birds other than hummingbirds, is not well established. Beetles commonly visit flowers of many species of cacti, such as those with bowl-shaped flowers (e.g., Echinocereus, Ferocactus, Echinocactus, Mammillaria, and Opuntia; Grant and Connell 1979; Grant and Grant 1979a; Grant and Hurd 1979; García-Sánchez 1984; del Castillo and González-
Espinosa 1988; del Castillo 1994). However, they are not good pollinators, as few pollen grains adhere to their bodies. Also, some beetles stay in a single flower, chewing floral parts. In fact, beetles in the genera Camptodes, Carpophilus, and Trichochrous invade the flowers in large groups and perform few flights among them (Grant and Connell 1979; Grant and Hurd 1979; García-Sánchez 1984; del Castillo and González-Espinosa 1988; del Castillo 1994). These beetles may self-pollinate the flowers directly or by stimulating thigmotrophic movements of the stamens, favoring the deposition of self-pollen on the stigma. In most cases, however, beetles may be nectar and pollen thieves. For Pilo-socereus, a columnar cactus pollinated by bats, small beetles lay eggs in the flowers. The emerging larvae perforate the ovary and the stem (Zappi 1994).
Carnegiea gigantea in the Sonoran Desert can be pollinated by western white-winged doves, although they are not the main pollinator (Alcorn et al. 1961). In the Galápagos Islands, finches are common visitors of Opuntia echios and O. helleri, from which they remove the stigma to gain access to pollen and the nectar. In getting a short-term benefit, they potentially suffer in the long term through a diminished supply of seeds, which they also eat during the dry season (Grant and Grant 1981). Ants also visit cactus flowers. They may be attracted by the extrafloral nectaries, a modified spine that secretes nectar in various genera, such as Coryphantha, Ferocactus, and Opuntia. Nectar production usually coincides with flowering or fruiting. Ants do not pollinate the flowers, but they may help protect the plant from potential herbivores. For Ferocactus histrix, territorial and entomophagous ants (genera Dorymyrmex and Iridomyrmexx) consume the nectar of extrafloral nectaries. They may even build their nests on top of the plants (del Castillo 1988a). For O. acantho-carpa, ants attracted by the extrafloral nectaries may increase fruit set and decrease fruit abortion by reducing the herbivore activity of coreid (Hemiptera: Coreidae) bugs (Pickett and Clark, 1979).
Outcrossing is common among cacti. Of the 55 taxa studied by Ross (1981), seeds are produced upon self-pollination in only 11 taxa and by cross-pollination in the other 44 taxa. Cacti have several adaptations favoring outcrossing: self-incompatibility, dichogamy, herkogamy, and unisexu-ality. Incompatibility is a genetic barrier in the progamic phase that may take place between pollen and stigma or during the development of pollen tubes in the style. The latter occurs for some Opuntia spp. (Bullock 1985; Rosas 1984; Negrón-Ortiz 1998), for varieties of Hylocereus spp.
(Ramírez-Mireles 1999), and for Schlumbergera (McMillan and Horobin 1995). The inhibition of the pollen tube in the style, after it has penetrated the stigma, is a characteristic of the gametophytic system of incompatibility (Lewis 1979; de Nettancourt 1997). But cacti do not share all of the characteristics typical of this incompatibility mechanism. For instance, the pollen in cacti is tri-nucleate (Benson 1979), whereas pollen in the typical gametophytic system is bi-nucleate (de Nettancourt 1997).
Other examples of obligate outcrossing cacti are Carnegia gigantea (Alcorn et al. 1961), Ferocactus histrix, Nop alea auberi (R. del Castillo, personal observations), Neobuxbaumia spp. (Valiente-Banuet et al. 1997), Opuntia helleri, and O. echios (Grant and Grant 1981). Self-incompatibility also occurs for Astrophytum, Pediocactus, Stenocereus griseus, S. repandus, S. horrispinus, and Thelo-cactus (Nassar et al. 1997) and in clones of Cereus peru-vianus, Hylocereus costaricensis, and H. polyrhizus (Weiss et al. i994a,b, 1995). For O. leucotricha, both selfing and interspecific hybrid crosses lead to low rates of fruit and seed set relative to outcrossing (Trujillo and González-Espinosa 1991).
In several hermaphroditic species of cacti, male and female organs mature at different times inside the flower. This phenomenon, called dichogamy, may reduce self-fertilization. For instance, in Hylocereus spp. cultivars, the stigma becomes receptive about 3 hours after the anthers dehisce (Ramírez-Mireles 1999), and pollen germinability is highest at anthesis. For F histrix, pollen is released 1 to 2 days after anthesis. At this stage, the stigma lobes are closed, and the pollinators usually land directly on the stamens to reach the nectary. In this way, pollen can be easily collected. After 2 to 3 days of opening, the stigma lobes expand and are used by pollinators as a landing platform, and pollen from others flowers can be deposited (del Castillo 1994). Therefore, selfing within the same flower is avoided but the transfer of pollen from one flower to another in the same plant (geitonogamy) is not, as flowering is sequential.
Whereas dichogamy implies a temporal separation in the maturation of male and female flower parts, herkog-amy is the spatial separation of anthers and stigma. The degree to which the stigmatic area is in contact with the anthers influences the probability of selfing. Grains of self pollen can occur on the lower portions of the stigma, which is in contact with the anthers, whereas outcross pollen is deposited on the upper surface of the stigma, as seen in a cultivar of O. ficus-indica (Fig. 5.1; Rosas and Pimienta 1986). Moreover, the fraction of the stigmatic surface in contact with the anthers is positively correlated with the rate of autogamy for Opuntia (Trujillo and González-Espinosa 1991). For Hylocereus undatus, the distance between the stigma and anthers is large, thus decreasing the probability of autogamy (Y. Ortíz-Hernández, personal communication). This distance—and thus the probability of outcrossing—can change during the flowering season (Grant et al. 1979). The distance between the style and the stigma of Nopalea spp. changes during flower maturation. During opening when the pollen is released, the distance is less, increasing later when the stigma becomes receptive.
While most cacti are hermaphroditic, interesting exceptions occur for Echinocereus, Mammillaria, Neobux-baumia, Opuntia, Pachycereus, and Selenicereus (del Castillo 1986a; Fleming et al. 1994; Valiente-Banuet et al. 1997). Atrophied organs of the non-functional sex and close hermaphroditic relatives of unisexual individuals suggest that unisexuality is a derived condition for cacti, as for other flowering plants. Unisexuality appears to have evolved several times independently. Dioecious populations (a population containing both male and female individuals) have been detected in Echinocereus coccineus, Opuntia robusta, and O. stenopetala (del Castillo and González-Espinosa 1988; Fleming et al. 1998). Trioecy (male, female, and hermaphroditic individuals in a single population) is reported for O. robusta and Pachycereuspringlei (del Castillo and González-Espinosa 1988; Fleming et al. 1998), gynodioecy (female and hermaphroditic individuals) for P pringlei (Fleming et al. 1998), and androdioecy (male and hermaphroditic individuals in the same population) for Neobuxbaumia mezcalaensis (Valiente-Banuet et al. 1997).
Cacti have a great range of polyploidy (Pinkava et al. 1977, 1985; Cota and Philbrick 1994). The significance of polyploidy, however, has not been related to the biology of the plants, particularly the mode of reproduction (Ross 1981). Changes in polyploidy can modify the breeding system of plants by at least two mechanisms: (1) by modifying the magnitude of inbreeding depression, and (2) by breaking down incompatibility mechanisms. Some species of cacti that have low rates of inbreeding depression are tetraploids —e.g., O. robusta (Sosa and Acosta 1966) and Pachycereus pringlei (Fleming et al. 1994). Ross (1981) reviewed 55 taxa of cacti and noted that polyploidy is correlated with self-fertility. In other families, chromosome doubling breaks down incompatibility mechanisms (Lewis 1979). Differences in inbreeding depression among diploids and poly-ploids probably have large influences on the evolution of polyploidy and breeding systems of cacti. Triploidy and tetraploidy most likely originated from fertilization in volving gametes that had not undergone a reduction in their chromosome number (Lewis 1980), and fertilization of unreduced gametes accounts for several intraspecific polyploid Opuntia hybrids (Pinkava et al. 1985). A comparison of the ploidy level with the mode of reproduction in the Cactaceae suggests that polyploidy is more likely to become established in self-fertile or apomictic (producing seeds in the absence of fertilization) taxa (Ross 1981).
The processes that occur from the arrival of pollen grain deposition onto the stigma to when the sperm reach the egg cell have received little attention (Rójas-Aréchiga and Vázquez-Yanes 2000). For the progamic phase of Opuntia ficus-indica, anther dehiscence occurs just before or at the time of flower opening, so pollen grains can start germination on the stigmas a few hours before the flowers open (Rosas 1984). Each stigma receives many pollen grains, but only a few germinate (about 30%; Weiss et al. 1993). Consequently, relatively few pollen tubes grow in the upper part of the style—from 300 to 350 per flower (Table 5.1). Pollen grain germination and pollen tube growth occur relatively rapidly, with over 20 pollen tubes occurring at the base of the style within 24 hours after flower opening, increasing to 65 tubes by 48 hours after flower opening. By the time the style wilts (72 hours after pollination), the number of pollen tubes at the base of the style exceeds 100 (Table 5.1).
Ovule fertilization is porogamous for both Opuntia and Stenocereus, because the pollen tubes penetrate the ovule through the micropyle before reaching the embryo sac (Rosas and Pimienta 1986; Ortega 1993). The first ovules with signs of fertilization occur 2 days after flower opening for Opuntia. At this time, the percentage of fecund ovules is low (2%), reaching 46% 2 days later. Because of the high number of ovules per flower (over 250), the ovule fertilization continues until 10 days after pollination. Ovule viability is high, because the percentage of ovules that are fertilized and transformed in seeds is high (over 80%; Rosas and Pimienta 1986).
Early ontogeny of cactus flowers, including the initiation of floral organs, is similar to that in many other species. In the Northern Hemisphere, flower bud differentiation for most cacti begins at the end of winter and the beginning of spring; anthesis begins in the spring followed by the development of fruit, which mature during the summer, e.g., for Opuntia spp. (Bravo-Hollis 1978; Trujillo 1982; del Castillo and González-Espinosa 1988; Pimienta-Barrios 1990;
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