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Reproductive Biology |
Departamento de Ecología Evolutiva, Instituto de Ecología, Apartado postal 70-275, C.U., Universidad Nacional Autónoma de México, CP 04510, D.F., Mexico
Received for publication May 24, 2002. Accepted for publication September 17, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Agavaceae • Agave lechuguilla • bees • Chihuahuan desert • hawk moths • hummingbirds • latitudinal gradient • pollination • population differentiation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Baker and Hurd, 1968
; Faegri and Van der Pijl, 1971
; Proctor and Yeo, 1973
). Although most of the studies have interpreted floral morphology and color as an adaptation to the locally most efficient pollinators (but see Aigner, 2001
), relatively few of them have studied these traits within and among populations (Galen, 1989
, 1996
; Armbruster, 1990
; Herrera, 1990a
, b
, 1993
; Johnston, 1991
; Andersson and Widen, 1993
; Conner, Davis, and Rush, 1995
; Inoue, Maki, and Masuda, 1996
; Melendez-Ackerman, Campbell, and Waser, 1997
). Based on the geographic mosaic model proposed by Thompson (1994
, 1997)
, one may expect plant–pollinator interactions to vary among populations, generating a complex pattern of differential adaptation. In this paper we analyze and compare the variation in floral traits, fecundity, and the associated changes in their floral visitors in 11 populations of Agave lechuguilla on a latitudinal gradient in the Chihuahuan desert.
The plants in the Agave genus are long-lived succulent rosettes (Gentry, 1982
). Agave can be abundant and dominant in vast areas of Mexico, in particular in xerophytic environments (Gentry, 1982
; Nobel, 1988
). Schaffer and Schaffer (1979)
suggested that pollinators are the most important factor in the evolution of their reproductive biology and life history, given their monocarpy. A high dependence of pollinators has been suggested in some species of the genus (Howell and Roth, 1981
; Eguiarte, Souza, and Silva-Montellano, 2000
). Usually, it is assumed that bats, mainly the genus Leptonycteris, pollinate Agave (Howell, 1979
; Gentry, 1982
; Arizaga and Ezcurra, 1995
). In particular, Arizaga et al. (2000a
, b)
demonstrated that bats of genera Leptonycteris and Choeronycteris pollinate the paniculated Agave macroacantha (subgenus Agave). Nevertheless, a large number of species of insects and birds also visit Agave flowers (Schaffer and Schaffer, 1977
; Kuban, Lawley, and Neill, 1983
; Martínez del Rio and Eguiarte, 1987
; Kuban, 1989
; Eguiarte, Souza, and Silva-Montellano, 2000
; Slauson, 2000
). Schaffer and Schaffer (1977)
found that several species in the Littaea subgenus (spicate Agave; A. schotii, A. parviflora, and A. toumeyana) in Arizona, USA, have flower and nectar traits that suggest co-adaptation to pollination by bees and are mainly pollinated by large bees from the genera Bombus and Xylocopa.
Agave lechuguilla is an excellent system to study plant–pollinator interactions in a geographic mosaic context, as it is a species with an unusually broad distribution for an Agave. Agave lechuguilla is found throughout the Chihuahuan desert ranging from the Valley of Mexico up to southern Texas and New Mexico, USA (Gentry, 1982
; Briones, 1994
). Additionally, Gentry (1982)
described geographic variation in the size and color of its flowers. Moreover, the distribution of potential pollinators changes along A. lechuguilla's distribution. In its southern range, nectarivorous bats and hummingbirds are more abundant and diverse (Arita, 1991
; Johnsgard, 1993
; Arita and Santos del Prado, 1999
). To the north, the diversity of bees increases (Ayala, Griswold, and Bullock, 1993
). Based on that information, we addressed the following questions: How do flower color and morphology of A. lechuguilla vary along this latitudinal gradient? Does the pollinator assemblage change with latitude? If syndrome adaptation to a specific pollinator occurs in the case of A. lechuguilla, we may expect to find clinal variation in floral traits corresponding to the variation in the pollinators.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) is found mainly on limestone soils. The flowering season is in summer, from late May to September (Gentry, 1982
). The inflorescence is a spike, as in all species in the subgenus Littaea, and the flowers produce pollen and nectar during the night (Gentry, 1982
; Freeman and Reid, 1985
). Flowers are protandrous, and they open from the bottom to the top of the spike forming a ring of ca. 30 simultaneously open flowers (A. Silva-Montellano, personal observation). Pollen is made available on the first night that flowers open. Stigmas are receptive for the 3–4 d that follow. Nocturnal nectar production declines with flower age (Freeman and Reid, 1985
). Nectar characteristics are described in Freeman et al. (1983)
and in Cadaval (1999)
. Clonal propagation is important in the species, producing large clonal patches in all the distribution.
Studied populations
The study populations were sampled to cover most of the natural distribution of the species in a latitudinal gradient, from 20° N to 32° N, and we attempted to locate a study site at every latitudinal degree (Fig. 1; Table 1). We studied 11 populations, starting from Pachuca, Hidalgo (population 1), in the northern Valley of Mexico, up to Ciudad Juarez, Chihuahua (population 10), near the USA border. For the Mapimi population (M) we have only partial data because we were not able to reach the population during the rainy season.
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We calculated the Lang's humidity index for each locality (= total annual precipitation [in millimeters]/mean annual temperature [in degrees Celsius]; Mohr and Van Baren, 1954
) using information from the nearest climate station (García, 1988
). Table 1 shows that populations 1–4 were more mesic, whereas populations 6, M, 9, and 10 were more xeric.
Density of rosettes was estimated in 100-m2 quadrants (four replicates per site). The density of reproductive individuals (inflorescences) was estimated using the nearest neighbor method (Krebs, 1989
). We followed the standard sampling procedure: setting 12 random points in the field (about 3 ha), we recorded the distance from those points to the nearest plant and from a random individual to a second one. This gave a first density estimation, which was corrected from possible biases using Diggle's formula (Krebs, 1989
). We performed four replicates of this sampling procedure per site in order to compare among populations.
Color and morphology of flowers
In each population (except M), we randomly selected 15–20 reproductive individuals. From each individual we analyzed seven flowers at the same stage, i.e., young flowers before anther dehiscence (see Freeman and Reid, 1985
). Fresh color of each flower was recorded with a Munsell chart (Wilde and Voigt, 1952
). Color data were obtained as the addition of the values of chroma and hue, which permits distinguishing individual differences within populations. Flowers were video-filmed, digitized, and measured using the Morphosys program (Fig. 2; Meacham and Duncan, 1990
), following Domínguez et al. (1998)
.
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). We noted whether they contacted the stigmas or the anthers and the way that they access the resources in the flowers: frontal or by the side of the corolla, avoiding the stigma. Focal inflorescences were selected because they were easy to observe, in particular during the night. For each focal inflorescence, we measured its total height, estimated the volume of the rosette (in liters) using its diameters and height, and counted the number of open flowers. In each site, observations were done during the periods of high visitor activity, from 0700 to 1000 and from 1900 to 2200. All observations were done in silence a few meters away from the focal plant to avoid any disturbance to visitors such as vertebrates, but getting closer at times to characterize the behavior of the insect species. Each focal inflorescence was observed in periods of 10 min until 3 h were completed. These observations lasted 2 d for each site, accumulating a total of 12 observation hours (six diurnal and six nocturnal) per site, giving a total of 114 observation hours. Visitors were identified as morphospecies in the field, using collections of insects from the same sites, while vertebrates (birds) were identified using field guides. Insect identifications were corroborated by sending specimens to specialists. Data on nocturnal visitors in population 3 are lacking because of weather conditions.
Fecundity estimates
Fecundity data were collected during March of 1997. In each population, we randomly selected 30–50 inflorescences from the previous reproductive season. For each inflorescence we recorded the total number of flowers (as the number of flower scars) and the total number of mature fruits. For each plant we measured the volume of the rosette (using its diameter and height), and the height of the inflorescence to control for any factors related to the size of the plant on the fecundity output. The rosettes at the time of recording the fecundity conserve their former size, since the rigidity of the leaves allows them to maintain their length despite becoming thinner because of resource and water allocation during flowering and maturing of fruits.
Statistical analyses
Differences among populations in densities of rosettes and inflorescences were tested using one way ANOVAs. Linear regressions were used to determine the relationship between size of the plants and number of flowers, transforming both variables to natural logarithms to improve linearity. Correlations were used to compare flower morphology characters. Based on these correlations and the fact that we measured few traits, we selected corolla length and the corolla diameter to analyze the latitudinal patterns, because they describe the shape of the flowers and are biologically meaningful in relation to the access of the visitors to the flowers. We compared variation in flower morphometry among populations with nested ANOVAs (Sokal and Rohlf, 1995
), using the individual scores of the two selected traits for populations, individuals within populations and flowers within individuals. Individuals within populations was assigned as the random variable in the analysis. Changes in latitude for all characters were tested using regressions for repeated values of Y, where every point in each latitude corresponds to an individual plant value (Sokal and Rohlf, 1995
). Color data are presented as the proportion of a specific color (red) of the individuals in each population along the latitudinal gradient, and arcsine square-root transformed to fit normality. We used ANCOVA analysis to determine the effect of rosette volume with respect to the reproductive output among populations. The relationship between fecundity and frequency of visits was analyzed with a simple correlation but using the populations means, due to differences in sample size between the variables. Analyses were conducted using JMP program (SAS, 1995
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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There were significant differences in the size of a rosette and the total number of flowers per inflorescence among populations (ANOVA volume rosette: N = 350, df = 10, F = 22.8, P < 0.0001; ANOVA number of flowers: N = 350, df = 10, F = 43.47, P < 0.0001). Individuals were larger in the southern distribution (Fig. 3a; range of the population means = 111.6–38.3 L in populations 2–M, respectively; N = 350, F = 172.2, slope = –5.1, t = –13.1, P < 0.0001) and populations produced fewer flowers in the north (Fig. 3b; range of the population means = 575.6–133.9 in populations 3–10, respectively; N = 350, F = 240.4, slope = –32.9, t = –15.5, P < 0.0001). There was also a strong correlation between both characters among populations (using all the measured plants: N = 350, R2 = 0.546, F = 419.9, slope = 0.81, t = 20.5, P < 0.0001). The correlations was also observed within each of the 11 populations.
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The remaining visitors were a heterogeneous collection of insects, mainly small bees and wasps, which accounted for 12.3% of the total visits. This last group robbed nectar or pollen and because of their heterogeneity and low proportion per species were not included in the analysis.
In the 54 total hours of nocturnal observation, we were not able to detect a single bat visit, despite our expectations. This lack of visits by bats was confirmed by further and more detailed observations the next year in two selected populations (1 and M; Silva-Montellano, 2001
).
We estimated the frequency of visits per flower (number of visits/number flowers, in each inflorescence) in all the populations to avoid the effect on pollinators of the larger density of flowers in the southern populations. For the total set of pollinators, we found differences among populations (ANOVA populations df = 8, F = 4.1, R2 = 0.339, P < 0.0006), and we found also a pattern related to latitude (Fig. 6; slope = –0.039, t = –4.76, P < 0.0001), which explains 24% of the variance in frequency of visitation, decreasing toward northern populations. For each of the major potential pollinators, we detected the same patterns of decreasing in frequency of visits per flower toward northern populations (Table 6). For Hyles lineata (slope = –0.016, t = –2.82, P = 0.0063), latitude explains 10% of the variance in visitation frequency. For large bees (slope = –0.029, t = –4.36, P < 0.0001), latitude represents almost 20% of that variance, and the hummingbirds (slope = –0.009, t = –2.27, P = 0.0261) had a similar pattern in latitude, which explains 6% of the variance, although their visits were nearly an order of magnitude smaller. We found no significant pattern of visitation related to latitude for the main robber, Apis mellifera, although there were important differences among populations (Table 6).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). These traits suggest adaptation in the south to nocturnal pollinators, such as bats and/or hawk moths, whereas in the north it seems to change due to diurnal pollinators, mainly bees. In this respect the role of red color in tepals could be difficult to interpret in northern populations, since bees are relatively insensitive to it (Faegri and Van der Pijl, 1971
; Proctor and Yeo, 1973
). On the other hand, hummingbirds are attracted to red color (Proctor and Yeo, 1973
) but their visits decreased to the north. In addition, there is evidence that bees, especially Xylocopa, visit some red flowers extensively (Scott, Buchmann, and O'Rourke, 1993
). In all the studied traits we found not only a clinal pattern, but we also estimated significant differences among most of the populations, indicating geographic differentiation and suggesting adaptation at a local scale. Additionally, in most of the traits we found that a substantial component of the variation was due to the differences among individuals within the populations. This may indicate genetic differences among them and will favor the possibility of natural selection acting within each population. Unfortunately, we do not know the genetic basis of this morphological differentiation, and explicit genetic experiments will be needed to advance in this point. Also, environmental or age factors could be contributing to differences among individuals. We also have to consider the effect of vegetative propagation on the expression of the characters, as it maintain genotypes in the populations, retarding the change by pollination pressure.
We found more visits by pollinators towards the south and fewer in the north, which may possibly contribute to the differences in fruit set. We expected to correlate the differences in the reproductive traits among populations with differences in the pollinators on the latitudinal gradient: more bat visits in the south and more bee visits in the north. Nevertheless, the visitor data indicated not a single bat visit and no clear differences in the proportions of the different groups of visitors in the gradient. In general, bees are the most important visitors to the flowers all along the gradient.
Floral visitors
The shape and the pale color of the southern flowers suggest pollinators adapted to a nocturnal habit. The Agave genus is traditionally regarded as bat pollinated (Arizaga et al., 2000a
, b)
, but hawk moths and other animals are important visitors to their flowers (Eguiarte, Souza, and Silva-Montellano, 2000
; Slauson, 2000
). Hawk-moth-pollinated flowers are very similar to bat-pollinated ones, but are smaller and have fewer resources (Baum, 1995
; Cadaval, 1999
). Nevertheless, we were surprised by the total lack of visits by nectarivorous bats in the range of distribution of A. lechuguilla. This may be because our observations were limited, i.e., in other populations or sites or in other years bats may be present or even abundant. At present we only know that observations in other years in selected populations of Agave spp. (including A. lechuguilla) in the Chihuahuan desert also have not recorded a single bat visit (A. Silva, M. Mandujano, and J. Golubov, UNAM, unpublished data). Declines in the population sizes of nectarivorous bats, in particular Leptonycteris, have been reported (Howell, 1979
; Howell and Roth, 1981
; Wilson et al., 1985
; Eguiarte and Búrquez, 1988
). This, coupled with the fact that they are a far rarer species in the Chihuahuan desert than in the Sonoran desert and on the Pacific slope of Mexico as well as their migratory habits and foraging behavior, may make them rare and unreliable pollinators in the Chihuahuan desert (Howell, 1979
; Cockrum, 1991
; Fleming and Nuñez da Silveira, 1993
; Wilkinson and Fleming, 1996
; but see Kuban, 1989
; and Hoyt, Altenbach, and Hafner, 1994
).
Hawk moths were the most common potential pollinators in three of the nine evaluated populations. As mentioned above, hawk moths are common visitors to Agave flowers, and in some cases may be the most important pollinators. On the other hand, hawk moths are very unreliable pollinators, as they may not be active on cold nights due to physiological restrictions (Martinez del Rio and Búrquez, 1986
). Also, their population sizes may fluctuate as a consequence of changes in their larval feeding plant populations, differences in weather, or in parasitoid populations in the previous year (Janzen, 1988
; Haber and Frankie, 1989
).
Overall, the more common visitors to A. lechuguilla flowers were bees. The visitation frequency of large bees was higher in the south than in the north. Nevertheless, given the morphology of the flowers, we suspect that in the north they were more important as pollinators, because the sizes would allow them better pollen transportation and because the fecundity of northern A. lechuguilla plants seems to be more limited by pollinators. Considering their foraging behavior and the local sizes and shapes of the flowers, Xylocopa californica bees of the north may be more efficient pollinators than the B. pennsylvanicus of the south. Data from detailed experiments in other years suggest that this is true (Silva-Montellano, 2001
). We have no explanation for the lack of visits of B. pennsylvanicus in the north, despite the fact that they visit other Agave species in Big Bend National Park in Texas (Kuban, 1989
). Xylocopa californica bees use dead flowering stalks of A. lechuguilla as nest sites (Scott, Buchmann, and O'Rourke, 1993
), providing the opportunity to be closer than B. pennsylvanicus to the flowers of A. lechuguilla. Hummingbirds had a secondary role as pollinators, because of their lower visitation frequency, and they seemed to use the flowers opportunistically, depending on the other available resources and competition with other organisms.
Our results agree with the interspecific observations of Schaffer and Schaffer (1977)
and of Freeman et al. (1983)
on the evolution of nectar and morphology adapted to bee pollination in some northern (Arizona) species of Agave.
Two critical questions arise from our observations: why do the southern populations maintain a bat pollination syndrome if there are no bats? And why do the flowers in the north maintain nectar and pollen production at night? The easiest answer may be to invoke "phylogenetic constraints," but the fact that the northern populations changed in floral morphology indicates that some of the traits have changed. This situation may be explained by three different scenarios: (1) Perhaps in the south the selective pressures are less strong. (2) Probably the northern populations have had more time to adapt, because in the south the bat populations have disappeared more recently or because gene flow with other southern bat-pollinated populations or species swamped the efficiency of natural selection. (3) An intriguing possibility was recently raised by Aigner (2001)
; he suggests that in some cases floral traits may show adaptation to minor or less effective pollinators. We do not have data at the present moment to solve this problem, and we believe the solution will not be easy to determine. The other question is why the nocturnal nectar and pollen production is maintained in all the populations. This could be the result of "phylogenetic constraints," as all the species in Agave and Manfreda that have been studied (see review in Eguiarte, Souza, and Silva-Montellano [2000]
) had similar nectar production and pollen release patterns. On this point we have to reconsider the role of the main robber A. mellifera as an important force in the maintenance of the nocturnal characteristics of the flowers, because they remove most of the pollen in the early morning, preventing the change to diurnal pollination.
General pattern and evolution
We consider that in A. lechuguilla the differences in floral characteristics along the gradient are mainly adaptive, given the consistency of the clinal patterns and large population sizes and abundance of the populations, coupled with very high levels of genetic variation and gene flow (Silva-Montellano, 2001
). Both reproductive traits and animal visitors highlight the problem of understanding the process of adaptation to the pollinators and the reproductive ecology of a species. For each population, the suite of reproductive traits is different. There is not a single "typical" or "average" population. In this particular case, the variation in most traits is more or less congruent and coordinated and follows a clear clinal pattern. The situation for the visitors seems to be more critical, as we showed that they change in space, but given that the data on floral visitors is really an instantaneous "photograph" of a few days in a few plants, it is logical that there is going to be large variation within and among sites and years. These patterns clearly relate to the coevolution mosaic ideas of Thompson (1997)
. In each population the distribution of floral characters may be different, and the pollinators will be different (in species or abundance). The result could be differential adaptation to each population, which, combined with gene flow, extinction, and colonization, will generate a complicated tapestry of adaptation and coevolution not very different from the shifting balance ideas of Wright (1931
, 1932)
.
Conclusion
It is clear from the differences and variability of patterns, not only among populations but also among individuals in each population, that the pollination syndrome characterization, although attractive as a practical and general descriptive tool, may be more of a burden than an asset in detailed evolutionary studies (Waser, 1983
; Herrera, 1996
; Waser et al., 1996
; Aigner, 2001
). The requirement of specificity to the most effective pollinator could be one of the major restrictions in using this concept in a practical way, especially if there are several different pollinators with the concomitant difficulties in determining their respective efficiency or in categorizing alternative behaviors and visitation patterns of one pollinator in particular (Thompson and Pellmyr, 1992
; Sahley, 1996
; Temeles, 1996
; Bruneau, 1997
; Aigner, 2001
). Resource-rich flowers, such as those of Agave, attract a broad range of animals that use the flowers, and in some conditions these animals can be efficient pollinators. Many of the floral traits may be better understood as general exaptations (Gould and Vbra, 1982
), rather than good adaptations to the pollinators we may see in a given moment. Geographic and temporal variation in floral visitors, reproductive traits, and their interaction, and detailed studies of adaptation should acknowledge the complex geographic mosaic of the interaction (Thompson, 1997
) in a model involving differential adaptation, local extinction, and colonization in a metapopulational landscape generating a shifting balance-like evolution. This is a daunting perspective, but if it is not taken into account, we will only have inadequate sketches of the evolution of the reproductive traits of flowering plants.
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FOOTNOTES |
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2 Author for reprint requests (asilva{at}miranda.ecologia.unam.mx
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Andersson S. B. Widen 1993 Pollinator-mediated selection on floral traits in a synthetic population of Senecio integrifolius (Asteraceae). Oikos 66: 72-79[CrossRef][ISI]
Arita H. 1991 Spatial segregation in long-nosed bat, Leptonycteris nivalis and Leptonycteris curasoae, in Mexico. Journal of Mammalogy 72: 706-714
Arita H. K. Santos Del Prado 1999 The conservation of nectar-feeding bats in Mexico. Journal of Mammalogy 80: 31-41[CrossRef]
Arizaga S. E. Ezcurra 1995 Insurance against reproductive failure in a semelparous plant: bulbil formation in Agave macroacantha flowering stalks. Oecologia 101: 329-334[CrossRef][ISI]
Arizaga S. E. Ezcurra E. Peters F. Ramirez de Arellano E. Vega 2000a Pollination ecology of Agave macroacantha (Agavaceae) in a Mexican tropical desert. I. Floral biology and pollination mechanisms. American Journal of Botany 87: 1004-1010
Arizaga S. E. Ezcurra E. Peters F. Ramirez de Arellano E. Vega 2000b Pollination ecology of Agave macroacantha (Agavaceae) in a Mexican tropical desert. II. The role of pollinators. American Journal of Botany 87: 1011-1017
Armbruster W. S. 1990 Estimating and testing the shapes of adaptive surfaces: the morphology and pollination of Dalechampia blossoms. American Naturalist 135: 14-31[CrossRef][ISI]
Ayala R. T. Griswold H. Bullock 1993 The native bees of Mexico. In T. P. Ramamoorthy, R. Bye, A. Lot, and J. Fa [eds.], Biological diversity of Mexico, 179–228. Oxford University Press, Oxford, UK
Baker H. P. Hurd 1968 Intrafloral ecology. Annual Review of Entomology 13: 385-414[CrossRef][ISI]
Baum D. 1995 The comparative pollination and floral biology of baobabs (Adansonia-Bombacaceae). Annals of the Missouri Botanical Garden 82: 322-348[CrossRef][ISI]
Briones O. 1994 Origen de los desiertos mexicanos. Ciencia 45: 263-279
Bruneau A. 1997 Evolution and homology of bird pollination syndromes in Erythrina (Leguminosae). American Journal of Botany 84: 54-71[Abstract]
Cadaval A. 1999 Estudio evolutivo de los azúcares del néctar de Agave lechuguilla en el desierto de Chihuahua. Undergraduate dissertation, Facultad de Ciencias, Universidad Nacional Autónoma de México, D.F., México
Cockrum L. 1991 Seasonal distribution of northwestern populations of the long-nosed bat Leptonycteris sanborni (Phyllostomatidae). Anales del Instituto de Biología, UNAM. Sección Zoología 62: 181-202
Conner J. R. Davis S. Rush 1995 The effect of wild radish floral morphology on pollination efficiency by four taxa of pollinators. Oecologia 104: 243-245
Dafni A. 1992 Pollination biology: a practical aproach. Oxford University Press, Oxford, U.K
Dominguez C. L. Eguiarte J. Nuñez-Farfan R. Dirzo 1998 Flower morphometry of Rhizophora mangle (Rhizophoraceae): geographical variation in Mexican populations. American Journal of Botany 85: 637-643[Abstract]
Eguiarte L. A. Búrquez 1988 Reducción en la fecundidad de Manfreda brachystachya, (Cav.) Rose, una agavácea polinizada por murciélagos: los riesgos de la especialización en la polinización. Boletín de la Sociedad Botánica de México 48: 147-149
Eguiarte L. V. Souza A. Silva-Montellano 2000 Evolución de la familia Agavaceae: filogenia, ecología evolutiva de la reproducción y genética de poblaciones. Boletín de la Sociedad Botánica de México 66: 131-150
Faegri K. L. Van der Pijl 1971 The principles of pollination ecology, 2nd ed. Pergamon Press, Oxford, UK
Fleming T. R. Nuñez L. da Silveira 1993 Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis. Oecologia 94: 72-75[CrossRef][ISI]
Freeman C. E. W. Reid 1985 Aspects of the reproductive biology of Agave lechuguilla (Torr). Desert Plants 7: 75-80
Freeman C. E. W. Reid J. Becvar R. Scogin 1983 Nectar sugar composition in some species of Agave (Agavaceae). Madroño 30: 153-158
Galen C. 1989 Measuring pollinator-mediated selection on morphometric floral traits: bumble bees and the alpine sky pilot, Polemonium viscosum. Evolution 43: 882-890[CrossRef][ISI]
Galen C. 1996 Rates of floral evolution: adaptation to bumble bee pollination in an alpine wildflower, Polemonium viscosum. Evolution 50: 120-125[CrossRef][ISI]
García E. 1988 Modificaciones al sistema de clasificación climática de Köpen. Offset Larios S. A., D.F., México
Gentry H. 1982 Agaves of continental North America. University of Arizona Press, Tucson, Arizona, USA
Gould S. E. Vbra 1982 Exaptation: a missing term in the science of form. Paleobiology 8: 4-15[Abstract]
Haber W. A. G. W. Frankie 1989 A tropical hawk moth community: Costa Rican dry forest Sphingidae. Biotropica 21: 155-172[CrossRef][ISI]
Herrera C. 1990a The adaptedness of the floral phenotype in a relict endemic, hawk moth-pollinated violet. 1. Reproductive correlation of floral variation. Biological Journal of the Linnean Society 40: 263-274[CrossRef]
Herrera C. 1990b The adaptedness of the floral phenotype in a relict endemic, hawk moth-pollinated violet. 2. Patterns of variation among disjunct populations. Biological Journal of the Linnean Society 40: 275-291[CrossRef]
Herrera C. 1993 Selection on floral morphology and environmental determinants of fecundity in a hawk moth-pollinated violet. Ecological Monographs 63: 251-275[CrossRef]
Herrera C. 1996 Floral traits and plant adaptation to insect pollinators: a devil's advocate approach. In D. Lloyd and S. Barrett [eds.], Floral biology: studies in floral evolution of animal-pollinated plants, 65–87. Chapman and Hall, New York, New York, USA
Howell D. J. 1979 Flock foraging in nectar-feeding bats: advantages to the bats and the host plants. American Naturalist 144: 23-49
Howell D. J. B. Roth 1981 Sexual reproduction in Agaves: the benefits of bats; the cost of semelparous advertising. Ecology 62: 1-7[CrossRef][ISI]
Hoyt R. A. J. S. Altenbach D. J. Hafner 1994 Observations on long-nosed bats (Leptonycteris) in New Mexico. Southwestern Naturalist 39: 175-179[CrossRef][ISI]
Inoue K. M. Maki M. Masuda 1996 Evolution of Campanula flowers in relation to insect pollinators in islands. In D. Lloyd and S. Barrett [eds.], Floral biology: studies in floral evolution of animal-pollinated plants, 377–400. Chapman and Hall, New York, New York, USA
Janzen D. H. 1988 Ecological characterization of a Costa Rican dry forest caterpillar fauna. Biotropica 20: 120-135[CrossRef][ISI]
Johnsgard P. 1993 The hummingbirds of North America. Smithsonian Institute Press, Washington, D.C., USA
Johnston M. 1991 Natural selection on floral traits in two species of Lobelia with different pollinators. Evolution 45: 1468-1479[CrossRef][ISI]
Krebs C. 1989 Ecological methodology. Harper and Row, New York, New York, USA
Kuban J. 1989 The pollination biology of two populations of the Big Bend century plant, Agave havardiana Trel.: a multiple pollinator syndrome with floral specialization for large vertebrate pollinators. Ph.D. dissertation, Syracuse University, Syracuse, New York, USA
Kuban J. J. Lawley R. Neill 1983 The partitioning of flowering century plants by Black-chinned and Lucifer Hummingbird. Southwestern Naturalist 28: 143-148[CrossRef][ISI]
Martinez del Rio C. A. Búrquez 1986 Nectar production and temperature dependent pollination in Mirabilis jalapa L. Biotropica 18: 28-31[CrossRef][ISI]
Martinez del Rio C. L. Eguiarte 1987 Bird visitation to Agave salmiana: comparisons among hummingbirds and perching birds. Condor 89: 357-363[CrossRef][ISI]
Meacham C. T. Duncan 1990 MorphoSys. University of California, Berkeley, California, USA
Melendez-Ackerman E. D. Campbell N. Waser 1997 Hummingbird behavior and mechanisms of selection on flower color in Ipomopsis. Ecology 78: 2532-2541[ISI]
Mohr E. C. J. F. A. Van Baren 1954 Tropical soils. Interscience Publishers, London, UK
Nobel P. 1988 Enviromental biology of agaves and cacti. Cambridge University Press, Cambridge, UK
Percival M. 1965 Floral biology. Pergamon Press, Oxford, UK
Proctor M. P. Yeo 1973 The pollination of flowers. Collins, London, UK
Sahley C. T. 1996 Bat and hummingbird pollination of an autotetraploid columnar cactus Weberauerocereus weberbaueri (Cactaceae). American Journal of Botany 83: 1329-1336[CrossRef][ISI]
SAS. 1995 JMP statistics and graphics guide. SAS Institute, Cary, North Carolina, USA
Schaffer W. V. Schaffer 1977 The reproductive biology of Agavaceae. I: Pollen and nectar production in four Arizona agaves. Southwestern Naturalist 22: 157-168
Schaffer W. V. Schaffer 1979 The adaptative significance of variations in reproductive habit in Agavaceae. II: Pollinator foraging behavior and selection for increased reproductive expenditure. Ecology 60: 1051-1069[CrossRef][ISI]
Scott P. E. S. L. Buchmann M. K. O'rourke 1993 Evidence for mutualism between a flower-piercing carpenter bee and ocotillo: use of pollen and nectar by nesting bees. Ecological Entomology 18: 234-240
Silva-Montellano J. A. 2001 Ecología reproductiva y genética de poblaciones de Agave lechuguilla (Torr.) en un gradiente latitudinal. Ph.D. dissertation, Instituto de Ecología, Universidad Nacional Autónoma de México. D.F. México
Slauson L. A. 2000 Pollination biology of two chiropterophilous agaves in Arizona. American Journal of Botany 87: 825-836
Sokal R. F. J. Rohlf 1995 Biometry, 3d ed. W. H. Freeman, New York, New York, USA
Temeles E. 1996 A new dimension to hummingbird-flower relationships. Oecologia 105: 517-523[CrossRef][ISI]
Thompson J. 1994 The coevolutionary process. University of Chicago Press, Chicago, Illinois, USA
Thompson J. 1997 Evaluating the dynamics of coevolution among geographically structured populations. Ecology 78: 1619-1623[CrossRef][ISI]
Thompson J. O. Pellmyr 1992 Mutualism with pollinating seed parasites amid co-pollinators: constraints on specialization. Ecology 73: 1780-1791[CrossRef][ISI]
Waser N. 1983 The adaptive nature of floral traits: ideas and evidence. In L. Real [ed.], Pollination biology, 163–201. Academic Press, Orlando, Florida, USA
Waser N. M. L. Chittka M. V. Price N. M. Williams J. Ollerton 1996 Generalization in pollination systems, and why it matters. Ecology 77: 1043-1060[CrossRef]
Wilde S. A. G. K. Voigt 1952 The determination of color of plant tissues by the use of standard charts. Agronomy Journal 44: 499-500
Wilkinson G. S. T. H. Fleming 1996 Migration and evolution of lesser long-nosed bats Leptonycteris curasoae, inferred from mitochondrial DNA. Molecular Ecology 5: 329-339[CrossRef][Medline]
Wilson D. E. R. Medellín D. V. Lanning H. Arita 1985 Los murciélagos del noreste de México, con una lista de especies. Acta Zoológica Mexicana 8: 1-26
Wright S. 1931 Evolution in Mendelian populations. Genetics 16: 97-159
Wright S. 1932 The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the VI International Congress of Genetics 1: 356-366
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