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Reproductive Biology |
Instituto de Ecología, Universidad Nacional Autónoma de México (Morelia), Apartado Postal 27-3 (Xangari), Morelia, Michoacán 58089, Mexico
Received for publication March 1, 2002. Accepted for publication August 8, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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16 h in winter, 10 h in spring) as well as partly nocturnal (12 h in winter, 3 h in spring), and flowers were pollinated by bees, hummingbirds, and hawk moths. Manual cross-pollination was 37–49% effective in all populations. Self-pollination was 12% successful in the wild, but twice as successful (22–27%) in managed and cultivated populations. Diurnal pollination was 35–55% effective in winter and 100% in spring. Nocturnal pollination was successful only in winter (15%). Crosses among individuals were more effective within populations than among populations, including populations under a similar management regimen. The least successful crosses were between wild and cultivated populations. Flowers were produced in all populations from January to March, but flowering peaks differed by 1 mo among wild, managed, and cultivated populations and by 2 mo between wild and cultivated populations. The latter interrupted pollen exchange in May. Seeds from managed and cultivated populations germinated faster than those from wild individuals. Domestication has seemingly favored self-compatible P. chichipe plants with higher fruit yield, a longer period of fruit production, and faster seed germination, attributes that have resulted in partial reproductive barriers between wild and manipulated populations.
Key Words: Cactaceae • columnar cacti • domestication • Mexico • Polaskia chichipe • reproductive biology • Tehuacán-Cuicatlán Valley
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Currently, 20 species of these plants are sources of food in the region. People gather products of columnar cacti from wild populations, but seven species are also cultivated in home gardens. In addition, people manage wild populations in situ by enhancing the numbers of favorable plants when they clear natural vegetation. For some columnar cactus species, both cultivation and management in situ may involve domestication (Casas, Caballero, and Valiente-Banuet, 1999
), which is an evolutionary process, guided by humans, through which heritable morphological or physiological variation of plant populations is molded by artificial selection (see Darwin, 1868
; Harlan, 1992
). Cacti fruits are the main parts used, and characteristics such as size, pulp color and flavor, peel thickness, and thorniness are considered when people select individual plants to manage in situ and cultivate. Artificial selection is intense in home gardens, where plants are continually replaced by others with better attributes, but it is also practiced in managed in situ populations, where desirable phenotypes are maintained and propagated during the perturbation of natural vegetation areas (Casas et al., 1997
, 1999a
; Casas, Caballero, and Valiente-Banuet, 1999
).
Previous studies analyzed reproductive biology of columnar cacti in the context of their domestication in the Tehuacán Valley (Casas et al., 1999b
; Cruz and Casas, 2002
). In those cases, the authors concluded that artificial selection had not modified the species' reproductive biology and that the occurrence of both spatial and temporal barriers to pollen exchange among wild and manipulated populations was unlikely. Our study analyzed the case of Polaskia chichipe (Glosselin) Backeberg, endemic to the Tehuacán Valley. This cactus is markedly restricted to volcanic soils at elevations of 1600–2300 m, where it is a dominant element of the thorn-scrub forest type called "chichipera" (Valiente-Banuet et al., 2000
). Some of the wild populations are under in situ management, and the species is also cultivated in home gardens (Casas, Caballero, and Valiente-Banuet, 1999
). Humans propagate chichipe by planting branches, transplanting young plants, or sowing seeds from the desirable phenotypes (A. Carmona and A. Casas, unpublished data). More commonly, though, people tolerate seedlings and young plants of chichipe (derived from seeds in bird or human feces) in managed in situ populations and home gardens. They let the most vigorous young plants grow and then decide to leave or remove plants at reproductive age (
10 yr old) according to the presence of favorable or unfavorable characteristics. Polaskia chichipe is one of the columnar cacti with relatively high economic value in the region. Its fruits are sold fresh or dry for human consumption. The species appears to be undergoing domestication through artificial selection, and this process has seemingly resulted in morphological differentiation between wild and manipulated populations. Fruits and seeds from cultivated and managed in situ individuals are larger than those from unmanaged wild populations (A. Carmona and A. Casas, unpublished data).
The purpose of our study was to examine whether human management has modified the reproductive biology of P. chichipe in managed in situ and cultivated populations as compared with wild populations. Bravo-Hollis (1978)
described flowers of P. chichipe as diurnal, but no formal studies on reproductive biology have been conducted. Therefore, our first aim was to test if anthesis is diurnal and which animals are the probable pollinators. Studies on breeding systems in columnar cacti of the Tehuacán Valley have generally found that self-pollination fails to produce fruits (Casas et al., 1999b
; Valiente-Banuet et al., 1996
, 1997a
, b
). Therefore, if the reproductive pattern of P. chichipe is consistent with those of other columnar cacti, its breeding system would be self-incompatible. In some cultivated plant species, however, artificial selection has modified breeding systems, favoring self-compatible mutants because they give satisfactory yields even in absence of pollinators (Proctor, Yeo, and Lack, 1996
). Therefore, we considered an alternative hypothesis: artificial selection has favored numbers of self-compatible plants.
Because domestication of P. chichipe has resulted in morphological divergence in fruit and seed size between wild and manipulated populations, it is possible that mechanisms of reproductive isolation among these populations have helped to maintain such divergence. Spatial barriers would be possible if wild and manipulated populations were separated by distances greater than those that pollinators usually travel. Temporal barriers would operate if the flowering seasons of wild and manipulated populations occurred at different times. Reproductive barriers could be present if pollination were more effective within than among populations or among populations under the same management regimen than among populations under a different regimen.
In general, seeds from cultivated plants commonly germinate faster than those from wild plants, owing to the latter's dormancy and hard seeds (Hawkes, 1983
; Evans, 1996
). In a study of Stenocereus stellatus (Pfeiffer) Riccobono, Rojas-Aréchiga, Casas, and Vázquez-Yanes (2001)
found that artificial selection favored seedling vigor and rapid seed germination in cultivated variants. Because the management of P. chichipe involves selective recruitment of seedlings in home gardens and managed in situ populations and because artificial selection has determined more abundant phenotypes with larger seeds in these populations (A. Carmona and A. Casas, unpublished data), we hypothesized that seed germination could be influenced by the selective sparing of vigorous and dynamic emergent seedlings, and, therefore, cultivated and managed in situ plants would have seeds that germinated faster than those from wild plants.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Wild, managed in situ, and cultivated populations from the three villages were included in the analysis. Vegetation in wild populations is "chichipera" forest (Valiente-Banuet et al., 2000
). The elevation range of wild populations studied was 1955–2166 m. The managed in situ populations occurred in "chichipera" areas that were open for cultivation of maize, and individuals of P. chichipe had been spared (elevation range: 1860–2118 m). The cultivated populations were composed of individuals in home gardens of the villages studied (elevation range: 1881–1937 m). Patches of vegetation with wild and managed individuals of P. chichipe existed between the populations studied.
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Flower visitors
All insects that visited a sample of 20 flowers in each of the three populations of P. chichipe mentioned above were captured with entomological nets and forceps, and the time of each visit was recorded. Captured insects were preserved in 70% ethanol for later identification. Birds that visited flowers were photographed and captured with three mist nets per population. Frequency of visits of the different animal species to flowers of P. chichipe was recorded in the wild population of San Luis Atolotitlán in samples of 20 flowers from eight individuals in winter (23–24 January) and spring (29–30 March). The flowers were continually observed throughout anthesis. Observations were classified into 1-h intervals, and the averages of visits per flower per species were calculated per interval.
Breeding system
Field experiments were conducted in six populations (two of each management type), according to methods developed by Valiente-Banuet et al. (1996)
. For each of the following treatments, flower buds of at least 11 individuals per population were covered with exclusion bags just before anthesis.
1. Nonmanipulated self-pollination
Flower buds were left covered with exclusion bags from anthesis to the ripening or abortion of fruits. The number of individuals and flowers sampled per population type were 31 and 356 from wild, 28 and 352 from managed in situ, and 29 and 630 from cultivated.
2. Manual self-pollination
Pollen from a given flower was deposited on its own stigma with paint brushes, and the flower was then re-covered. To prevent cross-pollination, we washed the paint brushes with distilled water and ethanol after pollinating each flower, and then dried the brushes before reusing them. This treatment tested the hypothesis that failure of self-pollination is not due to physical factors related to flowers structure or to temporal factors related to behavior. A total of 24 individuals and 114 flowers from wild populations, 30 and 108 from managed in situ populations, and 29 and 118 from cultivated populations was sampled.
3. Manual cross-pollination
Pollen from the flowers of one individual was manually deposited on stigmas of a different individual, and the flowers were then re-covered with exclusion bags. A total of 14 individuals and 72 flowers from wild populations, 16 and 79 from managed in situ populations, and 15 and 73 from cultivated populations was sampled.
4. Natural pollination (control)
Flower buds just before anthesis were labeled and maintained without exclusion bags until the fruits began to grow. At that point, the flowers were covered to protect the fruits. A total of 29 individuals and 457 flowers from wild populations, 30 and 609 from managed in situ populations, and 26 and 599 from cultivated populations was sampled.
For each pollination treatment, fruit and seed set were determined, and differences between treatments per population type were analyzed with one-way analyses of variance (ANOVA). Seed viability was determined by germinating seeds resulting from the experiments described below.
Diurnal vs. nocturnal pollination
For each of the following treatments, a total of 20 flower buds from ten individuals in the wild population of San Luis Atolotitlán were bagged in winter (20–21 January) and spring (27 March). The bags were removed as indicated for each treatment, and then the flowers were re-covered for 1 mo, until the collection of successful or aborted fruits.
1. Complete diurnal pollination
This treatment covered the entire daylight period during which flowers were open. In winter, exclusion bags were removed from the flowers from 0800 to 1830 on the first day, the flowers were re-covered at night, and the bags were then removed from 0800 until the flowers closed on 21 January (1800). In spring, bags were removed from 0730 to 1930 on 27 March.
2. Diurnal pollination only on the first day
This treatment was used in the winter experiments to test whether complete diurnal pollination substantially increased the production of fruit. Exclusion bags were removed only during the first day of anthesis (from 0800 to 1830) and then the flowers were re-covered.
3. Diurnal pollination only on the second day
For the same purpose as treatment 2, and also in winter, exclusion bags were removed only during the daylight of the second day of anthesis (from 0800 to 1800).
4. Nocturnal pollination
Exclusion bags were removed from the flowers when it was dark. In winter, bags were removed from 1830 to 0730 of the following day, and in spring from 2000 to 0630, the flowers were then re-covered.
5. Control
Flower buds just before anthesis were labeled and were not covered with exclusion bags.
Phenology
Ten individuals in each of the wild, managed in situ, and cultivated study populations were observed for production of flowers and fruits throughout the reproductive season. Five principal branches per individual were randomly selected, and the number of flower buds, flowers in anthesis, immature fruits, and mature fruits was counted every 30 d.
Seed germination experiments
Seeds of three fruits per plant were obtained from 25, 27, and 30 individuals in wild, managed in situ, and cultivated populations, respectively, in San Luis Atolotitlán. A total of 30 randomly chosen seeds per plant were put on three layers of moist filter paper in plastic 9-cm-diameter petri dishes, which were arranged in a random design within a growth chamber. The chamber was set for alternating day/night temperatures (27°/12°C) and 14/10 h photoperiod in order to simulate the temperature and light conditions of natural germination. The number of germinating seeds (emerging hypocotyls) was counted every 24 h, and the germination percentage calculated per day per population. The germination capacity (GC) (percentage of seeds that germinated at the end of the experiment), the median germination rate (R50) (days required for 50% germination of the seeds), and the germination speed (R50') (days required for 50% of the seeds to germinate, according to Thompson and El-Kassaby, 1993
) were calculated. The GC data were transformed by arcsine, and R50 and R50' by (1 – [1/x + 1]), where x is the variable transformed, in order to normalize the calculated response variables and to achieve homogeneity of variances. The transformed data were analyzed by one-way ANOVA for testing differences between populations.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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12 h of which are at darkness, whereas in spring, flowers were open 13.12 ± 0.10 h (N = 60 flowers), only 2.82 ± 0.10 h (N = 60 flowers) of which were during the night. In the two seasons, flowers of the three populations studied were open in overlapping intervals. In most of the flowers observed, the outermost layer of tepals started to separate at 0900, pollen release occurred at 1300, and maximum turgidity of stigmas was reached at 1330 (Table 2). During winter, most flowers stayed open, with pollen available and stigmas turgid, until 1400 of the following day, when closing started to finish at 1700. In spring, most flowers began to close at 1700 and were closed at 2230 of the same day that anthesis started. At the beginning of anthesis, traces of nectar were perceived, and the maximum production was between 1300 and 1700, coinciding with the maximum turgidity of stigma (Fig. 2).
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0900 and continuing the whole day. The honey bees were most active between 1000 and 1200, although they also visited frequently between 1300 and 1600. Xylocopa mexicanorum was active between 0900 and 1700, with the highest activity between 1400 and 1600. The bumble bee Bombus pensylvanicus pensylvanicus De Geer visited flowers only between 1000 and 1100, with relatively low frequency. The meliponinaen bees Plabeia mexicana and P. frontalis Friese frequently visited flowers between 1200 and 1300 and again between 1500 and 1600.
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The hummingbird A. violiceps visited a considerable number of flowers from different individuals located >1 km apart. Although the birds' beaks were longer than the flower tubes of P. chichipe (4.5 ± 0.17 cm [mean ± 1 SE] and 1.83 ± 0.11 cm, respectively), hummingbirds commonly touch both anthers and stigmas with their beaks and faces during their visits. Sampling of pollen on the hummingbird visitors detected chichipe pollen on their heads and throats (María del Coro Arizmendi, Facultad de Estudios Superiores, Iztacala, Universidad Nacional Autónoma de Mexico, Mexico, unpublished data).
Black ants visited constantly throughout the day, destroying entire parts of P. chichipe flowers and buds. Beetles visited flowers during the day and part of the night, although at relatively low frequency. These insects were small (2.7 ± 0.23 mm [mean ± 1 SE]) and entered the flowers through lateral spaces between the tepals, staying close to the nectarous chamber at the base of the reproductive structures without touching anthers and stigma.
Among nocturnal visitors were unidentified moths, hemipterans, and Atta mexicana L. ants. The most frequent nocturnal visitors during both winter and spring were hawk moths, which reached nectar with their proboscises, eventually touching anthers and stigmas. Visits of hemipterans and ants occurred in spring between 2100 and 2200 and between 2000 and 2200, respectively, at a relatively low frequency. Hemipterans stayed mainly on the tepals, not penetrating into the flower. Atta mexicana ants were predatory on flowers and buds.
Breeding system
Treatments for testing natural pollination were in all cases >80% successful in yielding fruit, whereas treatments entailing manual cross-pollination were 37.5–49.37% successful (Table 5). Nonmanipulated self-pollination was successful in 45–46% of the individuals sampled in managed in situ and cultivated populations, but only in 19 of individuals sampled in wild populations. This treatment was 22–27% successful in flowers sampled in managed in situ and cultivated populations, but only 12% successful in the wild. Manual self-pollination was also less successful in the wild (12% of flowers, 17% of individuals) than in the managed in situ (24% of flowers, 44% of individuals) and cultivated (27% of flowers, 62% of individuals) populations (Table 5). Fruits produced by self-pollination reached maturity but seed production was significantly lower that in fruits resulting from both control and cross-pollination treatments (Table 5). Seedless fruits, seemingly partenocarpic and significantly smaller than those with seeds, were recorded in 8.2% of the nonmanipulated self-pollinated plants.
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DISCUSSION |
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16 h during the day in winter and 10 h in spring). Periods of higher nectar production (1300–1700) and frequency of visits to flowers (1000–1700) notably coincided with the time when pollen started to be released and stigma lobes were turgid. This information suggests that pollination of P. chichipe is conducted mainly by diurnal visitors. Among them, Xylocopa mexicanorum was consistently a frequent visitor throughout the reproductive season and visited P. chichipe more often than the other bee species. Apis mellifera, Plabeia mexicana, and P. frontalis were also frequent visitors in spring. All these bees invariably touched anthers and stigmas during their visits and loaded significant amounts of pollen, especially X. mexicanorum and A. mellifera. Foraging activity of all these bees entailed short flights to flowers of one or several individuals. However, the availability of nectar from a given individual was variable throughout the day. The variability apparently increased visits to flowers of different plants, which in turn appeared to favor pollen exchange. The hummingbirds were active during the period when pollination of P. chichipe apparently occurred, and they appeared to touch anthers and stigmas during their visits; thus, they could have a role in pollination of chichipe. Experiments that exclude the participation of bees and other flower visitors might confirm and measure the effectiveness of these birds as pollinators.
The bumble bee Bombus pensylvanicus pensylvanicus visited flowers of P. chichipe with low frequency and before pollen release and stigma maximum turgidity occurred. It is unlikely that this species is a pollinator of P. chichipe. It is also unlikely that ants, which prey on P. chichipe flowers, and beetles, which do not touch the anthers and style, have any role in pollination.
Anthesis was also partly nocturnal (flowers open for 12 h during the night in winter and 3 h in spring). According to our experiments, nocturnal visitors were effective pollinators only during winter. Nocturnal visits by hawk moths were frequent during winter, when flowers were open throughout the night, but their role as pollinators seemed to be irrelevant in spring.
The seemingly most important pollinators of P. chichipe were the same in the wild, managed in situ, and cultivated study populations. These populations were separated at most by 5.5 km. The distance that most of the bees visiting P. chichipe are able to fly has not been documented, but according to Metcalf and Flint (1974)
, A. mellifera may fly within a radius of nearly 2.5 km, indicating the possible movement of pollen at least between the wild and managed in situ populations (1.5 km apart). However, the populations studied were not discrete patches in the landscape. Groups of P. chichipe and of other columnar cacti (Polaskia chende [Gosselin] A. Gibson & K. Horak, Escontria chiotilla [F. A. C. Weber] Rose, and Myrtillocactus schenkii [J. Purpus] Backeberg) visited by the same bee species occurred between the study populations, sometimes creating continuous bridges of plants and thereby allowing pollen exchange between populations. Hummingbirds may cover distances >5.5 km/d (Arizmendi, 2001
). Therefore, if these birds pollinate chichipe, that would increase the probability of pollen exchange between populations. All these aspects make the existence of spatial reproductive barriers unlikely.
Experiments on the breeding systems revealed that manual crosses were generally more successful than self-pollination. Self-pollination was generally more successful in managed in situ populations (43–46% individuals, 24–27% flowers) and cultivated populations (45–62% individuals, 22–27% flowers) than in the wild (17–19% individuals, 12% flowers). Therefore, self-incompatibility appears to have been favored by human manipulation of populations. Fruits resulting from self-pollination treatments generally produced significantly fewer seeds than those from natural and manual cross-pollination treatments and had reproductive disadvantages compared with fruits from cross-pollination. However, because self-compatibility allows the possibility of maintaining fruit production during periods of scarcity of pollinators or their absence, individuals with this attribute would be relatively more productive and thus favored by artificial selection, by their sparing and enhancement by management in situ, and by their cultivation.
Patterns of fruit set from crosses between population types show levels of reproductive affinity in relation to the type of population management. In general, each population showed higher reproductive affinity when crossed with the other population under the same management regimen. The least successful crosses were between wild and cultivated populations, and crosses of managed in situ populations with wild and cultivated populations were intermediately successful. Although the nature of such affinity is as yet unknown, it represents a partial barrier to pollen exchange among populations under different management regimens.
Our phenological studies indicate that pollen can be exchanged among wild, managed in situ, and cultivated populations between January and March, when production of flowers overlap in the three population types. However, flowering peak varied in the three types: February in the wild populations, March in the managed in situ populations, and April in the cultivated populations. Such phenological differences mean that management increases the time P. chichipe fruits are available: fruit production in wild populations ends in June, whereas in the managed in situ populations it ends in July and in the cultivated populations in August. During the flowering peak, resources for pollinators are concentrated in a given area, and a significant proportion of the fruits produced from flowers opening then may therefore contain seeds with genes from the same population. In other words, although pollen exchange between populations is possible, during flowering peaks it may be more frequent among individuals within the same population. In addition, pollen flow between at least the wild and cultivated populations is interrupted from April to May when the wild population stops producing flowers. These features, together with self-pollination and differential affinity to pollen exchange among populations under different management regimens, may create partial barriers to pollen exchange between populations under different types of management, especially between wild and cultivated populations. A. Carmona and A. Casas (unpublished data) found significant differences in fruit and seed size among wild, managed in situ, and cultivated populations (and especially between wild and cultivated populations), which apparently are the result of artificial selection for larger fruits. But maintenance of morphological differentiation is seemingly favored by the partial barriers arising from differences in pollen affinity, blooming time, and breeding system.
The germination experiments revealed a relatively high total germination percentage (76–77%) of seeds from managed in situ and cultivated populations compared with the percentage (60%) recorded in the wild. The germination rate of seeds from managed in situ and cultivated populations was significantly higher than that of seeds from wild individuals. This feature could be related with seed size. A. Carmona and A. Casas (unpublished data) found that fruits and seeds were significantly larger and fruits had more seeds in managed and cultivated populations than in wild individuals. These authors consider that fruit size is directly related with seed size and number and that these latter characters could have resulted from artificial selection for larger fruits. In turn, the differences observed in germination rate could be a consequence of larger seeds. Human manipulation could have thus favored, indirectly, faster seed germination in P. chichipe, as it has in other cultivated columnar cacti (Rojas-Aréchiga, Casas, and Vázquez-Yanez, 2001
).
In sum, research to date has shown that wild populations of P. chichipe significantly differ in morphology, especially in fruit and seed size, as well as in breeding system and seed germination patterns, compared with both managed in situ and cultivated populations. All these differences are associated with human management and are therefore an apparent consequence of artificial selection.
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FOOTNOTES |
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2 Author for reprint requests (acasas{at}oikos.unam.mx
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Bravo-Hollis H. 1978 Las cactáceas de México, vol. 1. Universidad Nacional Autónoma de México, Mexico City, Mexico
Casas A. J. Caballero A. Valiente-Banuet 1999 Use, management and domestication of columnar cacti in south-central Mexico: a historical perspective. Journal of Ethnobiology 19: 71-95
Casas A. J. Caballero A. Valiente-Banuet J. A. Soriano P. Dávila 1999a Morphological variation and the process of domestication of Stenocereus stellatus (Cactaceae) in central Mexico. American Journal of Botany 86: 522-533
Casas A. B. Pickersgill J. Caballero A. Valiente-Banuet 1997 Ethnobotany and domestication in xoconochtli, Stenocereus stellatus (Cactaceae), in the Tehuacán Valley and La Mixteca Baja, México. Economic Botany 51: 279-292[ISI]
Casas A. A. Valiente-Banuet A. Rojas-Martínez P. Dávila 1999b Reproductive biology and the process of domestication of Stenocereus stellatus in central Mexico. American Journal of Botany 86: 534-542
Cruz M. A. Casas 2002 Morphological variation and reproductive biology of Polaskia chende (Cactaceae) under domestication in Central Mexico. Journal of Arid Environments 51: 561-576[CrossRef][ISI]
Darwin C. 1868 The variation of animals and plants under domestication. The Johns Hopkins University Press, Baltimore, Maryland, USA
Dávila P. J. L. Villaseñor R. L. Medina A. Salinas J. Sánchez-Ken P. Tenorio 1993 Listados florísticos de México. X. Flora del Valle de Tehuacán-Cuicatlán. Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico
Evans L. T. 1996 Crop evolution, adaptation and yield. Cambridge University Press, Cambridge, UK
Harlan J. R. 1992 Origins and processes of domestication. In G. P. Chapman [ed.], Grass evolution and domestication, 159–175. Cambridge University Press, Cambridge, UK
Hawkes J. G. 1983 The diversity of crop plants. Harvard University Press, Cambridge, Massachusetts, USA
MacNeish R. S. 1967 A summary of subsistence. In D. S. Byers [ed.], The prehistory of the Tehuacan Valley, vol. 1, 290–231. University of Texas Press, Austin, Texas, USA
Metcalf C. L. W. P. Flint 1974 Insectos destructivos e insectos útiles. Compañía Editorial Continental, Mexico City, Mexico
Proctor M. P. Yeo A. Lack 1996 The natural history of pollination. Harper Collins, London, UK
Rojas-Aréchiga A. Casas C. Vázquez-Yanes 2001 Seed germination of wild and cultivated Stenocereus stellatus (Cactaceae) from the Tehuacán-Cuicatlán Valley, Central México. Journal of Arid Environments 49: 279-287[CrossRef][ISI]
Thompson A. J. Y. A. El-Kassaby 1993 Interpretation of seed-germination parameters. New Forest 7: 123-132
Valiente-Banuet A. M. C. Arizmendi A. Rojas-Martínez L. Domínguez-Canseco 1996 Ecological relationships between columnar cacti and nectar-feeding bats in Mexico. Journal of Tropical Ecology 12: 103-119
Valiente-Banuet A. A. Casas A. Alcántara P. Dávila N. Flores M. C. Arizmendi J. L. Villaseñor J. Ortega J. A. Soriano 2000 La vegetación del Valle de Tehuacán-Cuicatlán. Boletín de la Sociedad Botánica de México 67: 25-74
Valiente-Banuet A. A. Rojas-Martínez M. C. Arizmendi P. Dávila 1997a Pollination biology of two columnar cacti (Neobuxbaumia mezcalaensis and Neobuxbaumia macrocephala) in the Tehuacán Valley, central Mexico. American Journal of Botany 84: 452-455[Abstract]
Valiente-Banuet A. A. Rojas-Martínez A. Casas M. C. Arizmendi P. Dávila 1997b Pollination biology of two winter-blooming giant columnar cacti in the Tehuacán Valley, central Mexico. Journal of Arid Environments 37: 331-341
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0.05 after Student's t tests. F = 136.51, df = 3, 410, P = 0.001
