| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
What's this? |
Reproductive Biology |
2Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, A. P. 27-3 (Santa María de Guido), Morelia, Michoacán 58089 Mexico
Received for publication February 16, 2006. Accepted for publication September 13, 2006.
ABSTRACT
Stenocereus stellatus is an endemic, self-incompatible, columnar cactus found in central Mexico where many of its wild populations have been fragmented. As an economically important species of fruit-producing cactus, S. stellatus occurs in wild, managed in situ, and cultivated populations. The objectives of this study were to determine the effective pollinators of S. stellatus, to compare pollinator visits and reproductive parameters among the three types of populations, and to determine if nectar feeding-bats are moving among populations. Effective pollinators were the nectarivorous bats Choeronycteris mexicana, Leptonycteris curasoae, and L. nivalis. Fewer total visits per flower per night and fewer visits by Choeronycteris were observed in cultivated populations, while the opposite pattern was observed for Leptonycteris. One aggressive interaction was filmed in which Choeronycteris was physically displaced by Leptonycteris, and Choeronycteris visits were significantly affected by Leptonycteris visits. Cultivated populations received more pollen grains and had more fruit set. Variation in pollinator visits between different populations and the consequent effects on reproductive success were likely a result of competition between bat species, and differences in foraging and in sensitivity of bat species to human populations. Three marked L. curasoae traveled 15 km from their roosting site to their foraging area, and one visited cultivated and managed populations, suggesting that this species may be particularly important in moving pollen among populations.
Key Words: bat–plant interaction • Cactaceae • central Mexico • Choeronycteris mexicana • domestication • Leptonycteris spp • pollination biology • Stenocereus stellatus
Several studies have documented that a change in diversity and abundance of pollinators in fragmented or altered habitats can lead to a reduction in reproductive success of plants. In insect-pollinated plants, reduced pollinator visitation in fragmented habitats results in lower seed set (Jennersten, 1988
; Dewenter and Tscharntke, 1999
) and lower fruit set (Aizen and Feinsinger, 1994
; Ghazoul et al., 1998
). Nevertheless, in one recent study of bat-pollinated bombacaceous trees, the effects of forest fragmentation on bat pollinators and plant reproductive success varied depending upon the plant species (Quesada et al., 2004
). The authors attributed this variability to the effects that forest fragmentation may have on differences in flowering patterns, bat foraging behavior, and plant self-incompatibility systems. More research is needed to quantify the effect of habitat change on bat pollinators for other plant species.
Nectarivorous bats play an important role in the maintenance and regeneration of tropical forests by moving pollen large distances (Law and Lean, 1999
). In particular, their role as mobile links connecting habitats that otherwise would be isolated is essential for the reproductive success of isolated plant populations (Heithaus et al., 1975
; Fuchs et al., 2002
; Stoner et al., 2002
; Quesada et al., 2003
, 2004
; see Ghazoul, 2005
for a review). For example, in a rainforest in tropical Australia, Law and Lean (1999)
showed that bats are effective pollinators in fragmented landscapes due to the quantity of pollen that they carry and the large distances they cover. In the tropical dry forest of Jalisco, Mexico, greater bat visitation rate in undisturbed forest results in higher reproductive success for the bombacaceous tree Ceiba grandiflora Bartlett when compared to trees in fragmented habitats (Quesada et al., 2003
).
Forty-two of 70 columnar cactus species of the tribes Pachycereeae and Cereeae distributed in Mexico produce flowers with chiropterophilic characteristics that include large white flowers with copious pollen and nectar that are open at night (Valiente-Banuet et al., 1996
). Most of these cactus species are self-incompatible and require a vector to transfer pollen between genetically different plants to produce viable seeds (Valiente-Banuet et al., 1996
). Bats are primary pollinators for many columnar cacti (Howell and Schropfer, 1981
; Petit, 1995
; Nassar et al., 1997
; Valiente-Banuet et al., 2002
, 2004
; Ibarra-Cerdeña et al., 2005
). Previous studies have compared the pollination biology of cacti growing in various habitat types and under different forms of human management that include wild, managed in situ, and cultivated populations of several columnar cacti (Casas et al., 1999b
; Cruz and Casas, 2002
; Otero-Arnaiz et al., 2003
). However, these studies did not compare the effectiveness of bat pollinators of cacti in different habitat types such as cultivated home gardens, managed in situ, and wild populations.
In northern Oaxaca, México, wild populations of the columnar cactus Stenocereus stellatus (Pfeiffer) Riccobono, an economically useful cactus valued for its fruit, have been fragmented by agriculture and towns. In this region S. stellatus is found in three types of populations: (1) cultivated home gardens where cacti are subjected to artificial selection by people; (2) managed in situ populations where desired plants are selectively left in place and their abundance is commonly enhanced through vegetative propagation as vegetation is cleared for silviculture and agriculture; and (3) wild populations in areas of tropical dry forest (Casas et al., 1997
, 1999c
). Fruits are harvested from cacti in all three population types.
Flowers of this cactus open mostly at night, and nocturnal visitors, presumably nectar-feeding bats, are responsible for fruit production (Casas et al., 1999b
). Cultivated populations of S. stellatus present more pollinator resources than those in the managed or wild populations because plant density is significantly higher in home gardens than in managed and wild populations. Plants in cultivation also have a greater peak in flowering, with more individuals in flower and significantly more flowers per individual than the managed and wild populations (Casas et al., 1997
, 1998
, 1999b
). Reproductive success in terms of quantity of fruit produced per individual and fruit size also is greater in cultivated populations than in managed or wild populations (Casas et al., 1997
). It is surprising that reproductive success of S. stellatus is greatest in home gardens because cultivated populations are located within towns and surrounded by disturbed habitat. In general, plant reproductive success of animal-pollinated plants is usually lower in disturbed areas (Jennersten, 1988
; Aizen and Feinsinger, 1994
; Ghazoul et al., 1998
; Dewenter and Tscharntke, 1999
; Quesada et al., 2003
). The greater genetic diversity observed in cultivated populations (He = 0.333 ± 0.063) compared to managed (He = 0.265 ± 0.069) or wild populations (He = 0.278 ± 0.064) may be one factor influencing the greater fruit production and larger fruit size in this population (Casas et al., 2006
). Alternatively, this discrepancy may be associated with artificial selection favoring individuals that produce more and larger fruits with more and larger seeds in cultivation (Casas et al., 1997
, 1999c
) or with different rates of pollinator visitation in home gardens, managed, and wild populations of S. stellatus.
This study was designed to compare pollinator visits between different populations and to test the hypothesis that a higher pollinator visitation rate results in greater pollen deposition and greater reproductive success (fruit set and seed production) in S. stellatus. If pollen is limited by pollinator visitation, we expect to find higher pollen deposition, fruit set, and seed production in populations that receive more pollinator visits. The objectives were to (1) identify the effective pollinator of S. stellatus; (2) estimate and compare the number of pollinator visits within the three populations (wild, managed in situ, and cultivated); (3) determine if the presence of one pollinator affects the other; (4) determine if pollinators are moving among the different populations; and (5) document pollen deposition, fruit set, and seed production in the three different populations. A concomitant goal of this study is to generate recommendations for the management of this important fruit resource.
MATERIALS AND METHODS
Study site
The study was conducted from 15 June to 20 August, 2003, in the town of Chinango, Oaxaca within La Mixteca Baja in central Mexico. La Mixteca Baja is located south of the Tehuacan Valley in northern Oaxaca (Fig. 1). This region is within the Balsas River basin and comprises a complex mountainous zone with altitudes ranging from 600 to 3000 m above sea level (a.s.l.). The town of Chinango is approximately 1600 m a.s.l. Average annual temperature in this region is 21°C with average annual precipitation of 721 mm (García, 1988
). Thorny scrub and tropical dry forest are found in lower elevation dry areas, while oak forest characterizes the higher elevation areas. Stenocereus stellatus is native to tropical dry forest and thorny scrub, where the annual precipitation ranges from 600 to 800 mm. Typical soil types of this area are alluvial and sandstone derivates. Indigenous Mixtec people within this region obtain their livelihood from raising goats, cultivating corn and beans, weaving palm leaves for handcrafts, and producing and selling fruits of S. stellatus and S. pruinosus (Otto) Buxbaum (Casas et al., 1997
).
|
). It is one of the most economically important species of fruit producing cacti in Mexico; this cactus is also used for firewood, living fences and forage (Casas et al., 1997
, 1999a
). This species naturally occurs in the Tehuacán Valley and in the southern portion of the Balsas River basin in the states of Morelos, Puebla, Guerrero, and Oaxaca.
As an arborescent cactus, S. stellatus is a succulent plant that ranges from 2–6 m in height, characteristically branching from the base. It produces crowns of light pink, tubular flowers at the top of the branches (Bravo-Hollis, 1978
). Flowers have a single pistil and numerous anthers. Flowering initiates in April and finishes in September with peak flowering in July. Anthesis occurs approximately 1–2 h after dark, and nectar is produced from 2000 to 0700 hours. This species is self-incompatible, and the most likely pollinators are the nectar-feeding bats Leptonycteris curasoae Miller, L. nivalis Saussure and Choeronycteris mexicana Tschudi. Other species such as hawkmoths (Sphinigidae) have also been observed visiting the flowers and are considered potential pollinators (Casas et al., 1999b
).
Leptonycteris curasoae and L. nivalis are recognized as species in danger of extinction by The Endangered Species Act of the United States (Shull, 1988
). In Mexico, these species are classified as threatened according to the Secretaría del Medio Ambiente y Recursos Naturales (SEMARNAT, 2001
). Leptonycteris curasoae is distributed from the southwestern United States to Colombia (Koopman, 1993
). Leptonycteris nivalis is distributed from southern Texas to Guerrero and Morelos, Mexico. Some populations of L. curasoe in Mexico travel to the southwestern United States, arriving at maternity caves in March and April, and returning to the south in September and October (Cockrum, 1991
), while others form resident populations in central Mexico (Rojas-Martínez et al., 1999
; Stoner et al., 2003
; Galindo-G. et al., 2004
). It is known that Leptonycteris curasoae can travel up to 100 km to forage in a single night (Horner et al., 1998
). Leptonycteris spp. roost in caves and form colonies of hundreds or thousands of individuals (Nowak, 1994
). Leptonycteris nivalis and L. curasoae are the largest nectar-feeding bats found in the New World: L. curasoae weigh 20–27 g with a forearm length of 53–57 mm, and L. nivalis weigh 25–35 g with a forearm length of 56–61 mm (Nowak, 1994
).
Choeronycteris mexicana is distributed from the southwestern United States through Mexico and on the Pacific slope of Central America to southern Honduras (Jones and Carter, 1976
). In Mexico this species is classified as threatened according to the Secretaría del Medio Ambiente y Recursos Naturales (SEMARNAT, 2001
). Choeronycteris mexicana is medium sized, weighing 14–19 g, with an average forearm length of 43–49 mm (Nowak, 1994
).
We sampled 11 study sites in Oaxaca, Mexico, to quantify bat visitation patterns to S. stellatus flowers. The cultivated population in our study was distributed among home gardens within the town of Chinango, Oaxaca, Mexico. Five different gardens within the town were selected for sampling (C1 to C5; Fig. 2). Northwest of Chinango, wild and managed populations of S. stellatus were located in an area called La Barcina. The distance between home gardens in Chinango and the surrounding managed and wild populations in La Barcina was approximately 3.5 km. The managed populations were contiguous with the wild populations, but were distinct because they were located within agricultural parcels. Observations were recorded in three managed populations (M1, M2, and M3) and three wild populations (W1, W2, and W3). The minimum distance between wild and managed populations was 200 m and the maximum distance was 1 km.
|
|
Flower foraging activity
We documented activity of pollinators with digital video cameras (Sony DCR-TRV27) following Stoner et al. (2002)
during the flowering season of S. stellatus, June–August 2003. Filming began at anthesis (at c. 2130–2200 hours) and continued for six continuous hours (until 400 hours). Flowers were then individually marked and covered with a mesh bag. The following data were collected for each flower filmed: (1) bat species (or other visitor), (2) feeding style (hovering or hanging from flower), (3) contact with reproductive organs as estimated by insertion of head into flower (tip of snout, most of snout up to eyes, whole snout up to ears), (4) hour of visit, and (5) total number of visits to the flower. Although L. curasoae could not be distinguished from L. nivalis, Leptonycteris was distinguished from C. mexicana, which has a smaller body, shorter forearm, and longer snout. If only the tip of the snout was introduced into the flower, it was assumed that the bat did not drink nectar and no contact was made with the stigma or anthers. If the snout was inserted all the way to the eyes or ears, contact was made with both the stigma and anthers and it was considered an effective visit; contact with the anthers was evident because upon removing the snout, the bats' face was covered with pollen.
To compare the number of flower visits for each population type (cultivated, managed, or wild), we used generalized linear models with the GENMOD procedure (SAS, 2000; Stokes et al., 2000
). The model used population type and site nested within population type as the categorical independent variables and the number of flower visits as the response variable. In the first analysis, total flower visits of both bat species served as the dependent variable with number of open flowers on the plant as a covariate. A second analysis was performed in which visits of C. mexicana served as the dependent variable, with number of visits of Leptonycteris and number of open flowers on the plant as covariates; this was done due to a recorded aggressive interaction between C. mexicana and Leptonycteris. Finally, a third analysis used the number of visits of Leptonycteris as the dependent variable, with the number of visits of C. mexicana and open flowers on the plant as covariates. A Poisson distribution with a logarithmic link function was used for total flower visits and C. mexicana visits, while L. curasoae visits followed a normal distribution.
Bat pollinator movement
Bat pollinator movement was evaluated using radio telemetry. Mist nets were used to capture bats within each of the populations, and radio transmitters (BD-2A; Holohil Systems, Carp, Ontario, Canada) were placed on the back of the bats with latex cement (skin bond). As recommended by Aldridge and Brighman (1988)
, the mass of the radio transmitters (0.72 g) was less than 5% of the average weight of the bats. To register bat activity, an automatic data logger (Model SRX Configuration #3; Lotek Engineering, Newmarket, Ontario, Canada) was placed within a population on the same night that flowers were filmed.
Pollen deposition, fruit set, and seed production
To quantify the number of pollen grains deposited on the stigmas, styles from filmed flowers were collected 36 h after anthesis and preserved in FAA (formalin-acetic acid-alcohol). Twenty-three styles were collected from cultivated populations, 25 from managed and 20 from wild. The styles were then fixed and stained with aniline blue (Martin, 1959
), and the pollen grains deposited on the stigma were observed with epifluorescence microscopy. A photograph of each stigma was taken with a digital camera, and the program SigmaScan Pro (1999, version 5.0) was used to count the number of pollen grains on the stigma. The size and shape of pollen grains were compared with pollen collected directly from the anthers of S. stellatus to insure that only conspecific pollen grains were counted. To determine if pollen grains deposited on the stigma depended upon population type (cultivated, managed, or wild) we used a generalized linear model with the GENMOD procedure (SAS, 2000; Stokes et al., 2000
). The model used population type and site nested within population type as the categorical independent variables and the number of pollen grains deposited on the stigma as the response variable (SAS, 2000; Stokes et al., 2000
).
Plants that were filmed also were monitored for fruit set by marking 5–10 additional floral buds on each filmed plant in cultivated, managed, and wild populations. Floral buds and filmed flowers were examined weekly to determine if they developed into fruit. Filmed flowers and floral buds after opening were covered with mesh bags to protect the fruits from external agents. Fruit set was estimated for each plant by dividing the number of fruits developed from the filmed flowers and marked flower buds by the sum of the total number of floral buds marked and the number of flowers filmed. Data were normalized with a square root arcsine transformation, and fruit set was compared between populations using ANOVA (PROC GLM; SAS, 2000). Statistically significant differences between populations were determined using the Bonferroni test of multiple pairwise comparisons.
Fruits were collected from the filmed flowers within each population, and the number of seeds produced was counted. The number of seeds produced was compared between populations using ANOVA (PROC GLM; SAS, 2000). Statistically significant differences between populations were determined using the Bonferroni test of multiple pairwise comparisons.
RESULTS
Foraging behavior
A total of 111 flowers were filmed: 59 from cultivated populations, 29 from managed populations, and 23 from wild populations (Table 1), with 6809 flower visits registered in the three populations. The most common visitor was the hog-nosed bat Choeronycteris mexicana, which accounted for 76% of all visits (5168), followed by the long-nosed bat Leptonycteris spp. (19%, or 1326 visits), and sphyngid moths (5%, or 315 visits). Only the bats were effective pollinators of S. stellatus, because they were the only ones that appeared to make direct contact with anthers and stigmas. Bats introduced their heads into the flowers up to their ears (8% of cases), or up to their eyes (90% of cases), allowing them to make contact with the reproductive structures without damaging them. Both of these foraging strategies resulted in their snout being completely covered with pollen when they extracted their head from the flower. In only 2% of the visits did they approach the flower without inserting their head into the flower. Sphyngid moths were assumed to be nectar robbers because they extended their proboscis to drink nectar apparently without making contact with the floral reproductive structures.
Choeronycteris mexicana fed while hovering in the air in front of the flower in 100% of the visits (N = 5168 visits). The great majority of Leptonycteris visits (N = 1326 visits) used the same feeding technique; however, during eight visits we observed Leptonycteris hanging from the flower with their back feet while drinking nectar. The average visit duration was brief for both species averaging 0.118 ± 0.002 (SE) s for C. mexicana and 0.121 ± 0.024 (SE) s for Leptonycteris.
One instance of interference competition between C. mexicana and Leptonycteris was recorded in the wild population located at the W2 site. The taped interaction shows C. mexicana arriving at the flower and inserting its snout to drink nectar while hovering. While C. mexicana was drinking nectar, a Leptonycteris flew up to the same flower and bit C. mexicana on the top of the back while grabbing its lower body with its hind feet and pulling it away. Upon successfully removing C. mexicana, the Leptonycteris began to feed at the flower.
Visitation rates
Significant differences were found in the mean number of visits per flower among populations when total visits of C. mexicana and Leptonycteris were analyzed. Overall fewer visits per flower were observed in the cultivated population than in the managed and wild populations (
2 = 35.47, df = 2, P < 0.0001; managed-wild: 2 = 1.36, P = 0.243, managed-cultivated: 2 = 13.17, P < 0.0003, wild-cultivated: 2 = 29.26, P < 0.0001; Fig. 3A); nevertheless, a significant effect of site nested within habitat was found (2 = 31.25, df = 8, P < 0.0001; Fig. 3B) showing variation in this pattern. Furthermore, the number of open flowers significantly affected the total number of visits (2 = 16.13, df = 1, P < 0.0001).
|
2 = 37.61, df = 2, P < 0.0001; managed-wild: (2 = 1.79, P = 0.1804, managed-cultivated: 2 = 12.03, P < 0.0005, wild-cultivated: 2 = 28.74, P < 0.0001; Fig. 4A). Again, a significant effect of site nested within habitat was found (2 = 47.33, df = 8, P < 0.0001; Fig. 4B), and the number of open flowers on the filmed plant significantly affected flower visits (2 = 18.93, df = 1, P = < 0.0001). In addition, the number of visits of C. mexicana was significantly affected by the number of visits of Leptonycteris (2 = 11.5, df = 1, P < 0.0008).
|
2 = 13.06, df = 2, P < 0.0015; managed-wild: 2 = 2.4, P = 0.1215, managed-cultivated: 2 = 13.03, P < 0.0003, wild-cultivated: 2 = 4.18, P < 0.0408; Fig. 5A). Again a significant effect of site nested within habitat was found (2 = 60.22, df = 8, P < 0.0001; Fig. 5B), and the number of open flowers on the filmed plant significantly affected flower visits (2 = 7.31, df = 1, P < 0.006). The number of Leptonycteris visits was not affected by the number of visits of C. mexicana (2 = 1.36, df = 1, P = 0.24).
|
|
Pollen deposition and reproductive success
Twenty-three styles were collected from cultivated populations, 25 from managed, and 20 from wild populations to count pollen grains. The number of pollen grains deposited on the stigma was significantly different between populations (2 = 9.27, df = 2, P < 0.0097; Fig. 6). Cultivated populations received significantly more pollen grains than managed populations (2 = 9.26, P = 0.0023), but no differences were found between cultivated-wild (2 = 4.18, P = 0.0408) or managed-wild (2 = 9.26, P = 0.023). No significant differences were found between sites within populations (2 = 12.49, df = 8, P = 0.1308).
|
|
This study confirms that Leptonycteris spp. and Choreonycteris mexicana are effective pollinators of S. stellatus. In 98% of their floral visits they made direct contact with the reproductive structures by introducing their face into the flower and covering their face with pollen. These results confirm Casas et al. (1999b)
, who concluded, through experimental crosses and mist net captures, that these bats are the principle pollinators of S. stellatus. Our results also suggest that sphyngid moths function as nectar robbers because they did not make contact with the reproductive structures of the plant. A similar observation was registered for several bombacaceous species in which sphyngid moths extracted nectar with their long tongue but did not contact floral reproductive organs (Stoner et al., 2002
; Quesada et al., 2003
, 2004
).
Flower visitation
Total visits per flower per night were greater in cultivated than managed or wild populations. The same pattern was observed when analyzing only Leptonycteris spp. visits. Nevertheless, the opposite pattern was observed for C. mexicana, where significantly fewer visits were observed in the cultivated than the managed or wild populations. Furthermore, all three analyses showed that the number of open flowers on the plant affected the number of visits and showed significant variation over sites. The observed patterns were likely a result of competition between bat species, differences in foraging behavior, and/or differences in sensitivity of bat species to human-populated centers.
In areas with fewer resources, or in places where the natural vegetation has been fragmented, nectarivorous bats display territorial or aggressive behavior (Howell, 1979
; Howell and Schropfer, 1981
; Lemke, 1984
). In our study one aggressive interaction was observed between Leptonycteris and C. mexicana on a cactus within a wild population. A Leptonycteris individual physically displaced a C. mexicana individual from a S. stellatus flower. We do not know how common these aggressive interactions are, but the fact that aggression was observed between these two species and that the number of visits of Leptonycteris significantly affected the number of visits of C. mexicana, suggests that competition is occurring between these nectarivorous bats. On average, Leptonycteris is a larger bat than C. mexicana and potentially is out-competing the smaller bat for resources. This might explain the discrepancy in number of visits between Leptonycteris and C. mexicana in different populations.
Differences in foraging behavior between Leptonycteris and C. mexicana also may explain the variation in visits per night observed in the different population types. Previous studies have documented that Leptonycteris frequently forages in groups (Howell, 1979
). Although no published information exists about foraging behavior in C. mexicana, during the course of our study only single individuals were captured during mist net sampling. This suggests that C. mexicana may be a solitary foraging species. Species that forage in groups benefit from foraging where there is a greater density of resources. The cultivated population likely provided a more attractive foraging area for Leptonycteris than managed and wild populations because home gardens have a higher density of plants (Casas et al., 1997
) and a greater percentage of flowering individuals (Casas et al., 1999b
). Because Leptonycteris travel long distances to forage, they are likely to frequent areas with greater resources. Another factor may be the proximity of foraging areas to the roosting site. The cultivated populations in Chinango were approximately 3.5 km closer to the roosting site (Cueva del Obispo, Fig. 1) of Leptonycteris than the managed and wild populations and are potentially more attractive as a foraging ground. The roosting site of C. mexicana is unknown.
Sensitivity of each bat species to human-populated areas also might explain differences in their foraging among different population types. Previous studies have shown that Leptonycteris is not affected by disturbed areas and is found foraging equally as often in disturbed as in undisturbed areas (Quesada et al., 2004
). This has been attributed to its large size and ability to forage over a large area or to commute long distances between roosting sites and foraging areas. No information exists about C. mexicana regarding its ability to adapt to disturbed areas, but other small-sized nectarivorous bats (i.e., Musonycteris harrisoni) are sensitive to disturbed areas and principally forage in undisturbed habitats (Stoner et al., 2002
).
Radio telemetry data indicated that Leptonycteris traveled 15 km from their roosting area in the Cueva del Obispo in Nochistlan, to the foraging area in Chinango. Furthermore, Leptonycteris was documented by radio telemetry visiting both the cultivated population in Chinango and the managed population 3.5 km farther away. These movement patterns suggest that Leptonycteris may be an especially important pollen vector, which travels long distances and transfers pollen among the distinct populations of S. stellatus. These results are similar to those found for the flying fox, Syconycteris australis Matschie, which pollinates the rainforest tree Syzyigium cormiflorum F. Muell. in Australia (Law and Lean, 1999
). Fragmented areas did not inhibit the movements of this nectarivorous flying fox, which is important in maintaining gene flow between isolated populations through pollen movement.
Implications of foraging behavior on reproductive success
Fruit set in both the wild (37%) and managed (34%) populations was significantly lower than in the cultivated population (70%). The relatively high fruit set (70%) we observed in cultivated populations of S. stellatus was similar to that found by Casas et al. for this species under cultivated conditions (1999a, 73%).The fruit set we observed in the wild population of S. stellatus, however, is lower than that reported by Casas et al. (1999b; 65%) for S. stellatus and for most other species of columnar cacti in the wild (Petit, 1995
; Valiente-Banuet et al., 1996
; Nassar et al., 1997
). The variable fruit set we observed between populations may be a consequence of pollinator visits, increased pollen loads, increased genetic diversity, or a combination of these factors.
Although flowers in the cultivated population received fewer total visits, they received significantly more visits from Leptonycteris, and they received significantly more pollen grains on the stigmas. These data suggest that Leptonycteris may be a particularly important pollinator for this cactus. Because flowers from managed and wild populations received more visits from C. mexicana than cultivated populations, but fewer pollen grains were deposited, the lower fruit set observed in managed and wild populations suggests that C. mexicana may not be as effective a pollinator as Leptonycteris. The lower density of both plants and flowers in managed and wild populations might have resulted in multiple visits to the same flower or plant, leading to geitonogamous crosses and no fruit set. Increased time spent foraging within a particular plant raises the probability of transferring pollen to flowers on the same plant, as has been found with other bat-pollinated species (Quesada et al., 2004
; Law and Lean, 1999
). This would likely result in diminishing the number of effective pollen donors (from outcrossed plants). Although C. mexicana visited flowers from managed and wild populations significantly more frequently than flowers from the cultivated population, the bats may have been foraging longer within the same plant due to the lower density of flowers. Therefore, the pollen loads of many of their visits in managed and wild populations may have included pollen from one or few pollen donors.
Because there were more flowers available in the home gardens, total population-wide floral visitation rate (not analyzed) might be greater in the cultivated population, while at the same time individual flower visitation rates were low, because there were more flowers available in the home gardens. The cultivated population has a higher percentage of flowering individuals (Casas et al., 1999b
), which means that on a given night, bats might visit more flowers on different plants while visiting each flower less frequently. If this were the case, then there is the potential that the pollen loads that bats transferred in the cultivated population had higher genetic diversity than in other population types. As a self-incompatible plant, S. stellatus must receive pollen from genetically different individuals to set fruit. Our study suggests that plants in cultivation were pollinated more effectively, perhaps by receiving genetically diverse pollen, and therefore set more fruit.
Another important factor that may be contributing to the higher fruit set observed in the cultivated area is the management S. stellatus populations receive in the gardens. Although human manipulation and transformation of natural areas generally result in biodiversity decreases, in certain cases human management can maintain or increase genetic diversity (Gadgil et al., 1993
; Haverkort and Millar, 1994
). In Chinango, people introduce new cacti and add to the variation of S. stellatus in their home gardens. This management results in both greater density and greater variety of S. stellatus in cultivation (Casas et al., 2006
). With greater density and diversity of individuals in cultivation, pollen originating from neighbors is more likely to be from genetically distinct individuals. This is an important advantage for a self-incompatible species. Furthermore, the environmental conditions in home gardens may promote higher fruit set through reduction of interspecific competition, cultivation of the soil, and addition of nutrients.
Management of S. stellatus in home gardens appears to be an important practice that reduces the negative impacts usually associated with human alteration of the habitat and cultivation. The home gardens in Chinango represent a reservoir of genetic diversity of S. stellatus (Casas et al., 2006
), as well as important resources for nectar-feeding bats within the area. Our results show that these gardens may be a key factor in maintaining diversity through fruit and flower production for an important columnar cactus in the region and may serve to connect fragmented populations in managed and wild areas. Finally, our results suggest that more intensive management (i.e., the introduction of a greater density of genetically different plants) in the managed in situ populations may result in attracting more pollinators and ultimately result in greater fruit set, not only for the managed populations, but possibly the contiguous wild populations as well.
FOOTNOTES
1 The authors thank E. Pérez-Negrón and J. A. Soriano for assistance in the field; H. Ferreira, A. Valencia Garcia, and G. Sánchez Montoya for technical support; M. Quesada for statistical analyses, and L. G. Herrera Montalvo and two anonymous reviewers for helpful comments for revising an earlier draft of this article. Financial support for this research was provided by SEMARNAT-CONACYT (2002-C01-0544), DGAPA, UNAM (IN220005), and the Royal Botanic Gardens, Kew (Cacti Study). 
4 Author for correspondence (kstoner{at}oikos.unam.mx
)
LITERATURE CITED
Aizen M. A. Feinsinger P.. 1994. Forest fragmentation, pollination and plant reproduction in a Chaco dry forest, Argentina. Ecology 75: 330-351.[CrossRef][Web of Science]
Aldridge H. D. J. N. Brigham R. M.. 1988. Load carrying and maneuverability in an insectivorous bat: a test of the 5% "rule" of radio-telemetry. Journal of Mammalogy 69: 379-382.[CrossRef]
Bravo-Hollis H.. 1978. Las cactáceas de México, vol. I Universidad Nacional Autónoma de México, Cuidad de México, D.F., México.
Casas A. Caballero J. Valiente-Banuet A.. 1999a. Use, management and domestication of columnar cacti in south Central México: a historical perspective. Journal of Ethnobiology 19: 71-95.
Casas A. Caballero J. Valiente-Banuet A. Rojas-Martínez A. Dávila P.. 1999b. Reproductive biology and the process of domestication of the columnar cactus Stenocereus stellatus in central Mexico. American Journal of Botany 86: 534-542.
Casas A. Caballero J. Valiente-Banuet A. Soriano J. A. Dávila P.. 1999c. Morphological variation and the process of domestication of Stenocereus stellatus (Cactaceae) in central Mexico. American Journal of Botany 86: 522-533.
Casas A. Cruse-Sanders J. Morales E. Otero-Arnaiz A. Valiente-Banuet A.. 2006. Maintenance of phenotypic and genotypic diversity in managed populations of Stenocereus stellatus (Cactaceae) by indigenous people in central Mexico. Biodiversity and Conservation 15: 779-898.[CrossRef][Web of Science]
Casas A. Pickersgill B. Caballero J. Valiente-Banuet A.. 1997. Ethnobotany and domestication in Stenocereus stellatus (Cactaceae) in the Tehuacán Valley and La Mixteca Baja, Mexico. Economic Botany 51: 279-292.[Web of Science]
Casas A. Valiente-Banuet A. Caballero J.. 1998. La domesticación de Stenocereus stellatus (Pfeiffer) Riccobono (Cactaceae). Boletín de la Sociedad Botánica de México 62: 129-140.
Cockrum E. L.. 1991. Seasonal distribution of northwestern populations of the long-nosed bat family Phyllostomidae. Anales del Instituto de Biología, UNAM, Serie Zoológica 62: 181-202.
Cruz M. Casas A.. 2002. Morphological variation and reproductive biology of Polaksia chende (Cactaceae) under domestication in Central Mexico. Journal of Arid Environments 51: 561-576.[CrossRef][Web of Science]
Dewenter I. S. Tscharntke T.. 1999. Effects of habitat isolation on pollinator communities and seed set. Oecologia 121: 432-440.[CrossRef][Web of Science]
Fuchs E. J. Lobo J. A. Quesada M.. 2002. Effects of forest fragmentation and flowering phenology on the reproductive success and mating patterns of the tropical dry forest tree Pachira quinata. Conservation Biology 17: 149-157.
Gadgil M. Berkes F. Folke C.. 1993. Indigenous knowledge for biodiversity conservation. Ambio 22: 151-156.[Web of Science]
Galindo-G C. Sánchez-Q A. Quijano R. H. Herrera-M L. G.. 2004. Population dynamics of a resident colony of Leptonycteris curasoae (Chiroptera: Phyllostomidae) in central México. Biotropica 36: 382-391.[Web of Science]
García E.. 1988. Modificaciones al sistema de clasificación climática de Kopen Instituto de Geografía, Universidad Nacional Autónoma de México, Cuidad de México, Distrito Federal, México.
Ghazoul J.. 2005. Pollen and seed dispersal among dispersed plants. Biology Reviews. 80: 413-443.[CrossRef]
Ghazoul J. Listion K. A. Boyle T. J. B.. 1998. Disturbance-induced density-dependent seed set in Shorea siamensis (Dipterocarpaceae), a tropical forest tree. Journal of Ecology 86: 462-473.[CrossRef]
Haverkort B. Millar D.. 1994. Constructing diversity: the active role of rural people in maintaining and enhancing biodiversity. Etnoecológica 2: 51-64.
Heithaus E. R. Fleming T. H. Opler P. A.. 1975. Foraging patterns and resource utilization in seven species of bats in seasonal tropical forest. Ecology 56: 841-854.[CrossRef][Web of Science]
Horner M. A. Fleming T. H. Sahley C. T.. 1998. Foraging behavior and energetics of a nectar feeding bat, Leptonycteris curasoae (Chiroptera: Phyllostomidae). Journal of Zoology, London 244: 575-586.[CrossRef]
Howell D. J.. 1979. Flock foraging in nectar-feeding bats: advantages to the bats and to the host plants. American Naturalist 114: 23-49.[CrossRef][Web of Science]
Howell D. J. B. Schropeer B.. 1981. Sexual reproduction in agaves: the benefits of bats; the cost of semelparous advertising. Ecology 62: 1-7.[CrossRef][Web of Science]
Ibarra-Cerdeña C. N. Iñiguez-Dávalos L. I. Sánchez-Cordero V.. 2005. Pollination ecology of Stenocereus queretaroensis (Cactaceae) a chiropterophilous columnar cactus in a tropical dry forest of Mexico. American Journal of Botany 92: 503-509.
INEGI (Instituto Nacional de Estadística, Geografía e Informática).. 2002a. Topographical map E14-6, scale 1:250 000, grid each 10 000 m Cuidad de México, Distrito Federal, México.
INEGI (Instituto Nacional de Estadística, Geografía e Informática).. 2002b. Topographical map E14B85, scale 1:50 000, grid each 1000 m Cuidad de México, Distrito Federal, México.
Jennersten O.. 1988. Pollination in Dianthus deltoids (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conservation Biology 2: 359-366.
Jones J. K. Jr. Carter D. C.. 1976. Annotated checklist, with keys to subfamilies and genera. In R. J. Baker, J. K. Jones, and D. C. Carter [eds.] Biology of bats of the New World family Phyllostomatidae part I. Special Publications of the Museum of Texas Technological University vol. 10: 7-38.
Koopman K. F.. 1993. Order Chiroptera. Mammal species of the world, a taxonomic and geographic reference, 2nd ed Smithsonian Institution Press, Washington, D.C., USA.
Law B. S. Lean M.. 1999. Common blossom bats (Syconycteris australis) as pollinators in fragmented Australian tropical rainforest. Biological Conservation 91: 201-212.
Lemke T. O.. 1984. Foraging ecology of the long-nosed bat Glossophaga soricina with respect to resource availability. Ecology 65: 538-548.[CrossRef][Web of Science]
Martin F. W.. 1959. Staining and observing pollen tubes in the style by means of fluorescence. Stain Technology 34: 436-437.
Nassar J. M. Ramírez N. Linares O.. 1997. Comparative pollination biology of Venezuelan columnar cacti and the role of nectar-feeding bats in their sexual reproduction. American Journal of Botany 84: 918-927.[Abstract]
Nowak R. M.. 1994. Walker's bats of the world Johns Hopkins University Press, Baltimore, Maryland, USA.
Otero-Arnaiz A. Casas A. Bartolo C. Pérez-Negrón E. Valiente-Banuet A.. 2003. Evolution of Polaskia chichipe (Cactaceae) under domestication in the Tehuacan Valley, central Mexico: reproductive biology. American Journal of Botany 90: 593-602.
Petit S.. 1995. The pollinators of two species of columnar cacti on Curazao, Netherlands Antilles. Biotropica 27: 538-541.[CrossRef][Web of Science]
Quesada M. Stoner K. E. Lobo J. A. Herrerías Y. Palacios-Guevara C. Munguía-Rosas M. A. O.-Salazar K. A.. 2004. Effects of forest fragmentation on pollinator activity and consequences for plant reproductive success and mating patterns in bat pollinated bombacaceous trees. Biotropica 36: 131-138.[Web of Science]
Quesada M. Stoner K. E. Rosas-Guerrero V. M. Palacios-Guevara C. Lobo J. A.. 2003. Effects of habitat disruption on the activity of nectarivorous bats (Chiroptera: Phyllostomidae) in a dry tropical forest: implications for the reproductive success of the neotropical tree Ceiba grandiflora. Oecologia 135: 400-406.[Web of Science][Medline]
Rojas-Martínez A. Valiente-Banuet A. Arizmendi M. Alcántara- Eguren A. Arita H. T.. 1999. Seasonal distribution of the long nosed bat (Leptonycteris curasoae) in North America: does a generalized migration pattern really exist?. Journal of Biogeography 26: 1065-1077.[CrossRef][Web of Science]
SEMARNAT (Secretaría de Medio Ambiente y Recursos Naturales).. 2001. Norma Oficial Mexicana NOM-059-ECOL-2001. Diario Oficial de la Federación. Órgano del Gobierno Constitucional de los Estados Unidos Mexicanos. CDLXXXVIII. No. 10 SEMARNAT, Cuidad de México, Distrito Federal, México.
Shull A. M.. 1988. Endangered and threatened wildlife and plants; determination of endangered status for two long nosed bats. Federal Register 53: 38456-38460.
Stokes M. E. Davis C. S. Koch G. G.. 2000. Categorical data analysis using the SAS system, 2nd ed SAS Institute, Cary, North Carolina, USA.
Stoner K. E. O.-Salazar K. A. R.-Fernández R. C. Quesada M.. 2002. Population dynamics, reproduction and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation. Biodiversity and Conservation 12: 357-373.[Web of Science]
Stoner K. E. Quesada M. Rosas-Guerreo V. Lobo J. A.. 2002. Effects of forest fragmentation on the Colima long-nosed bat (Musonycteris Harrisoni) foraging in tropical dry forest of Jalisco, Mexico. Biotropica 34: 462-467.[Web of Science]
Valiente-Banuet A. Arizmendi M. C. Rojas-Martínez A. Casas A. Godínez-Alvarez H. Silva C. Dávila P.. 2002. Biotic interactions and population dynamics of columnar cacti. In T. H. Fleming and A. Valiente-Banuet [eds.] Columnar cacti and their mutualists: evolution, ecology and conservation 225-240 University of Arizona Press, Tucson, Arizona, USA.
Valiente-Banuet A. Arizmendi M. C. Rojas-Martínez A. Dominguez-Canesco L.. 1996. Geographical and ecological correlates between columnar cacti and nectar-feeding bats in Mexico. Journal of Tropical Ecology 12: 103-109.
Valiente-Banuet A. Molina-Freaner F. Torres A. Arizmendi M. C. Casas A.. 2004. Geographic differentiation in the pollination system of the columnar cactus Pachycereus pecten-aboriginum. American Journal of Botany 91: 850-855.
CiteULike Complore Connotea Del.icio.us Digg Facebook Reddit Technorati Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  J. Rojas-Sandoval and E. Melendez-Ackerman Pollination biology of Harrisia portoricensis (Cactaceae), an endangered Caribbean species Am. J. Botany, December 1, 2009; 96(12): 2270 - 2278. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Kuriakose, P. A. Sinu, and K. R. Shivanna Domestication of cardamom (Elettaria cardamomum) in Western Ghats, India: divergence in productive traits and a shift in major pollinators Ann. Bot., March 1, 2009; 103(5): 727 - 733. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
