BIOTROPICA 38(5): 635642 2006

10.1111/j.1744-7429.2006.00179.x

Bat Pollination Breakdown in the Caribbean Columnar Cactus Pilosocereus royenii 1

Bert Rivera-Marchand2 and James D. Ackerman Department of Biology, University of Puerto Rico, P. O. Box 23360, San Juan, PR 00931-3360, U.S.A.

ABSTRACT
Generalized pollination systems may be advantageous on island systems or regions of substantial disturbance. We examined whether or not specialization breakdown has occurred in a presumably bat-pollinated columnar cactus, Pilosocereus royenii, on Puerto Rico, an island subjected to periodic hurricanes. The owers show characteristics related to bat pollination including nocturnal anthesis, morphology, and amount and quality of nectar reward. The cactus produces owers whose styles are temporally and mechanically separated from its anthers and do not self-pollinate. Hand manipulations indicated that it is partially self-incompatible or suffers some inbreeding depression. In 217 h of observations conducted biweekly over the course of 1 yr, P. royenii received visits from bats, moths, bees, and birds, but the only effective pollinator was the carpenter bee, Xylocopa mordax. Only four bat visits were recorded, all prior to stigma receptiveness. Floral morphology of P. royenii was signicantly more variable than that of other bat-pollinated species of the genus. We propose that infrequent bat visits are a consequence of a population crash and that oral variability is due to either relaxed selection for bat pollination or a transitional stage from bat pollination to bee pollination.

RESUMEN
Los sistemas de polinizaci on generalizada pueden ser ventajosos en sistemas de islas o regiones de perturbaci on sustancial. Examinamos si un colapso de especializaci on ha ocurrido en el cactus columnar (Pilosocereus royenii [L.] Byles & Rowley [Cactaceae]) aparentemente polinizado por murci elagos en Puerto Rico, una isla peri odicamente sujeta a huracanes. Las ores demuestran caracter sticas relacionadas con la polinizaci on por murci elagos, incluyendo apertura nocturna, morfolog a, cantidad y calidad de recompensa de n ectar. Las ores producen estilos que est an mec anicamente y temporalmente aisladas de las anteras las cuales son incapaces de autopolinizarse. Manipulaciones manuales indican que esta especie es parcialmente autoincompatible o sufre de depresi on endog amica. En 217 horas de observaci on realizadas bisemanalmente durante un a no, P. royenii recibi o visitas de murci elagos, mariposas nocturnas, abejas y aves, pero el u nico visitante efectivo fue la abeja carpintera (Xylocopa mordax). Solo cuatro visitas de murci elagos fueron notadas, todas antes de la receptividad de los estigmas. La morfolog a oral de P. royenii fue signicativamente m as variable que las otras especies de Pilosocereus polinizadas por murci elagos. Proponemos que las visitas infrecuentes de murci elagos son una consecuencia de una disminuci on en la poblaci on de murci elagos y que la variabilidad oral es debido a una selecci on relajada de los murci elagos polinizadores o un estado de transici on de polinizaci on por murci elagos a polinizaci on por abejas. Key words: bat; cactus; Caribbean; carpenter bee; Pilosocereus royenii; pollination; Puerto Rico.

IN SPECIALIZED PLANTPOLLINATOR SYSTEMS, oral morphology may correspond directly with pollinator morphology (e.g., Johnson & Steiner 1997). The degree of specialization may be so high that both partners may depend on each other for reproduction (e.g., Fleming & Holland 1998). Most plantpollinator relationships, however, may not be particularly specic. Waser et al. (1996) challenged the commonness of specialized pollinator systems, arguing that many of these associations are not as strict as once thought. These relationships may be so unspecialized that a plant may receive effective services from whole assemblages of pollinators (e.g., Herrera 1987). Certainly, relationships between plants and pollinators are not only asymmetrical, but may also be dynamic so that we expect a full range of specialization in this interaction (e.g., Schemske & Horvitz 1984, Bascompte et al. 2003, Ashworth et al. 2004). Both pollinator specialization and nonspecialization can be seen in columnar cacti that show characteristics of the bat pollination syndrome. In Mexico, Venezuela, and Curac ao, regions with large resident populations of glossophagine bats, columnar cacti are pollinated almost exclusively by these animals (Petit 1995, Valiente1 Received

2 Corresponding

8 September 2005; revision accepted 5 December 2005. author; e-mail: bertriveram@yahoo.com

Banuet et al. 1996, 1997, Nassar et al. 1997, Ruiz et al. 1997). In extratropical regions where glossophagine bats are uncommon, columnar cacti are pollinated by bats, as well as by birds and bees (Fleming et al. 1996, 2001, Sahley 1996, Nassar et al. 1997). Columnar cacti are also common on Caribbean islands but we know little of their pollination biology. Because islands generally show a trend away from specialized pollinator relationships (Carlquist 1974, Olesen et al. 2002) and also show an increased frequency of autogamy (Spears 1987, Ackerman 1985), we expect that cacti on islands will not be completely dependent on bats for pollination. This should be particularly true for cacti on islands prone to hurricanes, which can cause cyclical breakdowns in plantanimal relationships, particularly for those involving vertebrates (Waide 1991, Walker et al. 1991, Zimmerman et al. 1996, Rathcke 2000, 2001). We tested these ideas on the Caribbean island of Puerto Rico, where columnar cacti are common in dry regions. Our model system was Pilosocereus royenii (L.) Byles and Rowley, a cactus with oral traits usually associated with bat pollination (von Helverson 1993). Its white, bell-shaped owers are malodorous, nocturnal, and produce copious amounts of nectar and pollen. We hypothesized that, whereas some oral traits should be similar to other bat-pollinated members of the genus (e.g., irregular owering phenology), P. royenii
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should have a more exible breeding system, a broader array of pollinators, and greater variation in oral morphology than its mainland counterparts.

METHODS
STUDY SPECIES.Pilosocereus royenii is known from Puerto Rico, Mona Island, the Virgin Islands, and the Lesser Antilles. Plants grow to 7 m in height (Little Jr. et al. 1967) and its solitary owers last one night (Fig. 1). Pilosocereus royenii produces a large red berry containing numerous, small black seeds (Little Jr. et al. 1967). Fruits remain on the plant until they are eaten or the fruit splits open, dropping seeds to the ground. SITE DESCRIPTION.Puerto Rico is subject to periodic tropical storms and hurricanes with an average return time of 21 yr (Saliva 1972, Scatena & Larsen 1991). Our study was conducted in the Gu anica state forest (17 57 N, 65 52 W), which is located in the municipality of Gu anica along the SW coast of Puerto Rico. The vegetation is subtropical dry forest encompassing over 4000 ha (Murphy & Lugo 1990). Pilosocereus royenii is the dominant cactus in this region. Our study site is located on the southern part of the forest at an estimated altitude of 90 m above sea level, predominantly over a limestone substrate (Conde-Costas & Gonz alez 1990).

MATING SYSTEM.Five different treatments were applied to a total of 65 owers to determine the sexual system of P. royenii. For each treatment, all owers were from different plants. Ten owers were bagged with bridal veil netting immediately after opening to exclude all visitors and assess the possibility of autogamy. Stigmas unfurl after 2200 h. To determine whether or not unfurled stigmas were receptive, we cross-pollinated ten owers at 1930 h, just after they opened. These were then bagged to prevent further pollinations. Since pollinations done prior to 2200 h were unsuccessful, all other hand manipulations were performed after 2300 h to assure receptiveness. To detect self-incompatibility, we self-pollinated 15 owers and cross-pollinated another 15. The owers were bagged with bridal veil netting upon opening, manipulated, and bagged again after each treatment to exclude visitors. All hand pollinations were made by rubbing a cluster of ve to ten anthers on the stigma of an experimental ower. Finally, 15 owers were exposed to natural pollinators as a control group. Fruit initiation was noted for each treatment. Because of fruit predation prior to full maturity by the common rat, Rattus rattus L., we collected fruits as soon as they showed any degree of maturation such as reddish coloration. The number of seeds per fruit was determined and compared among treatments. A t-test was performed to determine if there was a signicant difference between seed set from cross- and self- pollinations. FLORAL REWARDS.Nectar standing crop was measured between 2030 h and 2130 h using single owers from 14 different plants. Nectar was removed and measured using a capillary tube of known volume. Nectar sugar concentration, expressed as a percentage of sucrose equivalent units, was measured with a Leica Inc. (Allendale, NJ, USA) hand-held refractometer. Nectar production of 11 owers from different plants was measured every 2 h beginning at 1930 h and ended at 0530 h when the owers stopped yielding nectar (Fig. 2). The owers were bagged with bridal veil before opening and unbagged only for the removal of nectar. Nectar was removed from the owers and not replaced. Sugar concentration and nectar volume were measured as above. We performed a one-way ANOVA to determine any similarity between nectar volumes of the standing crop and the samples taken throughout anthesis. PHENOLOGY.Observations of the phenology of P. royenii began in October 2000 and ended 1 yr later. Forty-eight plants were marked haphazardly in a 1-ha plot. Buds, open owers, old owers, new fruit, ripe fruit, and dry fruit were counted every 2 weeks during the study period. The number of owers and fruit was graphed against total rainfall per month and a linear regression was performed between number of mature buds and/or owers, and rainfall to determine whether or not there was any correspondence between them. To avoid counting the same ower twice, rst as a bud and then as an open and/or old ower, only nearly mature buds were included in the analysis. We calculated fruit set by dividing the total number of fruit produced per plant from November 2000 to October 2001 by the total number of buds produced per plant from October 2000 to September 2001, and multiplying by 100. We then calculated

FIGURE 1. The ower of P. royenii indicating morphometric measurements. CD = corolla diameter, FL = corolla length, SL = stigma length.

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just before sunrise and the arrival of diurnal visitors. Any initiated fruit was considered a product of pollination by a nectar-feeding bat. Fruit initiation or ower abortion was noted for all visited owers. Nearly mature fruits were collected, and their seeds were counted. We then compared seed set (total number of seeds per fruit) of hand cross- and self-pollinations, unmanipulated owers (i.e., controls), and fruits produced by each visitor group. Seed set produced by the various visitors, hand-pollinations, and the control group was compared with a one-way ANOVA followed by post hoc pairwise Tukeys tests. FLORAL MORPHOLOGY AND VARIABILITY.We measured corolla length, corolla diameter (N = 23), and total stigma length (N = 19; Fig. 1). Floral traits of visited owers were correlated with seed set produced by pollinators to detect selection on any particular trait. Because diverse visitors pollinating the owers may have exerted different selective pressures on the oral traits, morphological variability in the above oral measurements was compared with that of Venezuelan Pilosocereus moritzianus (Otto) Byles and Rowley and P. lanuginosus (L.) Byles and Rowley, both of which are pollinated almost exclusively by glossophagine bats (Nassar et al. 1997). To compare the variability of the ower length, corolla diameter, and stigma length of P. royenii with that of P. moritzianus and P. lanuginosus, a ratio of the coefcients of variation was computed between P. royenii and P. mortzianus, and P. royenii and P. lanuginosus. The ratio was determined by dividing the greatest coefcient of variation by the least. The degrees of freedom were then determined by the numerators sample size. The F statistic (Sokal & Rohlf 1981) was then used to assess signicant differences between the variability of the oral measurements of these plants.

FIGURE 2. Nectar production presented as a function of time (mean SD). (A) Nectar volume in milliliters throughout the night (N = 11). (B) Sugar concentration (% sucrose) throughout the night (N = 11).

the average of the percent of fruit produced per ower per plant. Development from late bud to fruit takes approximately 1 mo, so the fruits counted in 1 mo are of the same cohort as the buds counted in the previous month. FLORAL VISITORS AND THEIR RELATIVE IMPORTANCE.Nocturnal and diurnal visitors were observed from a distance greater than or equal to 2 m. A night vision scope (Moonlight Inc., Lenexa, KS, USA) was used to observe nocturnal visitors, while diurnal visitors were viewed with or without binoculars. Observations took place once every 2 weeks from October 2000 through September 2001. Depending on spacing, 212 owers were observed continuously throughout the night from sundown, when they opened, until the next day when they closed. A total of 108 owers were observed during 217 h of nocturnal and diurnal observations. The time of ower opening and closing was recorded for every observation day. Visits were recorded in detail, including time and date of the observation. Duration of each visit was timed with a chronometer, and general behavior of the visitors was noted. Visited owers were bagged using bridal veil after a single visit. After 8 mo of observations we observed only four bat visits. Because our presence may have been interfering with bat visits and after determining that the other possible nocturnal visitors, such as rats and hawkmoths, were incapable of pollinating P. royenii, a total of 81 owers were left available overnight on three different nights (N = 20; N = 36; N = 25) for nectar-feeding bats. These were then bagged the next day

RESULTS
MATING SYSTEM.Pilosocereus royenii owers show some mechanical barriers to self-pollination. Flowers are protandrous and the stigmas extend beyond both the corolla and anthers. Pollinator exclusion experiments conrm the need for pollinator-mediated pollination. The owers of P. royenii that were bagged immediately after opening (N = 10) did not yield fruit. All self-pollinated (N = 15) and cross-pollinated (N = 15) owers initiated fruit. A cost of self-pollination appeared at the seed production level. Selfed owers produced 21 percent fewer seeds than cross-pollinated owers (self: mean = 2066; SD = 513; cross: mean = 2617; SD = 712), and the difference was signicant (t-test: t = 2.435, df = 28, P = 0.022). FLORAL REWARDS.The average standing crop nectar volume measured between 2030 h and 2130 h was 0.327 ml (N = 14; SD = 0.132). Nectar production throughout the night was measured from 11 different owers. The owers of P. royenii produced a maximum mean nectar volume of 0.346 ml (SD = 0.115) during the third removal at 2330 h. After the third removal, the volume yielded by owers continued decreasing until owers stopped producing nectar. The average nectar production per ower per night was 1.285 ml

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(SD = 0.389 ml/ower/night). We found signicant differences between the average nectar volume of the standing crop, early and late anthesis (one-way ANOVA: F = 3.551; df = 2, 35; P = 0.04). Tukeys test revealed that the source of signicant variation was the average nectar volume during late anthesis. Between 2030 h and 2130 h, the average standing crop sucrose concentration was 21.0 percent (N = 14; SD = 1.5%); average sugar concentration gradually diminished after that. Removals began at 1930 h and ended at 0530 h when the owers stopped yielding nectar (Fig. 2). The second removal at 2130 h yielded the maximum sucrose-equivalent concentration of 20.7 percent (N = 14; SD = 1.5). There were signicant differences between the mean sucrose concentration of the standing crop, late and early anthesis (one-way ANOVA: F = 13.571; df = 2, 35; P < 0.001). Tukeys test revealed that the main source of variation was late anthesis (P < 0.001). PHENOLOGY.Pilosocereus royenii (N = 48) owered throughout the year with all the individuals producing owers (Fig. 3). Four rainfall peaks, two small and two large, were recorded and four oral production peaks were observed. Overall, we observed little concordance between the number of owers and the amount of rain. Two owering peaks lagged behind rain peaks (November 2000 and February 2001), one owering peak coincided with a rain peak (May), and a fourth peak occurred between peaks (July 2001; Fig. 3). Linear regression did not show any relationship between rainfall and ower production (N = 13; df = 11, 1; F = 0.0237; P = 0.88). There were four small fruiting peaks. Three of these peaks corresponded with owering peaks while one lagged behind a owering event. Average control fruit set from November 2000 through October 2001 was 29.9 percent (N = 48 plants, 988 owers; SD = 31%). Fruit set of hand outcrossed pollinations, however, was 100 percent. Fruit set was clearly pollen-limited at this site.

FIGURE 3. Total rain fall; owering and fruiting phenology of P. royenii for 1 yr (N = 48 census plants).

FLORAL VISITORS AND RELATIVE IMPORTANCE.Out of the 108 observed owers, 45 were visited (45.6%). Nocturnal visitors to P. royenii included one species of nectar-feeding bat Monophyllus redmani Leach (Phyllostomidae), at least two species of hawkmoths (Sphingidae: Pseudosphinx tetrio L. and Manduca sp.), and the common rat, R. rattus L. (Muridae). Diurnal visitors included two species of bees, Apis mellifera L. (Apidae) and Xylocopa mordax L. (Apidae), and three species of birds, the Antillean Mango (Anthracothorax dominicus L., Trochilidae), the Bananaquit (Coereba aveola L., Emberizidae), and the Troupial (Icterus icterus L., Emberizidae). A total of four visits by M. redmani were recorded on two different nights during the study period. The bats arrived individually to a ower and probed for an average of 3 sec (SD = 0.82). On two occasions, the bats ignored owers of neighboring plants after probing a ower of a plant at less than 1 m distance. A fth bat was seen hovering in front of an open ower and leaving after less than 3 sec without probing it. All four visits occurred prior to stigma receptiveness, and all owers subsequently aborted. Moreover, none of the 81 owers left available overnight for the bats yielded fruit. Pseudosphinx tetrio was seen visiting a ower of P. royenii on one occasion. Eight individuals of Manduca sp. were also seen probing the owers. All visits occurred after 2230 h when stigmas were receptive. The hawkmoths probed for an average of 6.5 sec (SD = 2.0) by inserting their proboscis into the ower without coming in contact with the stigmas. All visits by these moths resulted in ower abortions. Honey bees, A. mellifera, were seen visiting owers on all observation days between 0625 h and 1000 h. The average number of individuals observed at a single ower was 8.9 (SD = 3.74). Visits lasted from 20 min to 2.5 h. Due to their small size, these bees were able to crawl into the owers without making contact with the stigma. All visits by A. mellifera that we monitored resulted in abortions. Moreover, all the owers that were occupied by these bees were avoided by other visitors. Six Antillean mango hummingbirds, A. dominicus, were observed visiting the owers. All visits occurred between 0800 h and 0822 h and lasted an average of 3.5 sec (SD = 0.55). The hummingbirds probed the owers without coming in contact with the stigma that resulted in unpollinated owers. Only two bananaquits, C. aveola, were observed visiting owers. These birds landed on the top of the corolla and probed into the ower to remove nectar and possibly pollen without making contact with the stigma. The visits lasted an average 5.5 sec (SD = 0.71) and resulted in abortions. We observed the carpenter bee, X. mordax, visit owers of P. royenii 15 times. These large bees visited the owers between 0634 h and 0720 h in search of pollen and probably collected nectar. The bees landed on the corolla and remained within the ower for an average of 8.9 min (SD = 2.5). Once within the ower they circled the corolla many times, buzzing on many occasions. Of the 15 visits, 14 yielded fruit, representing all successful natural pollinations observed during the study period. Mean seed production per bee visit was 1399.5 seeds (SD = 940.3) per fruit. There were signicant

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TABLE 1.

Comparison of variation in the oral morphology of P. moritzianus (Pm), P. lanuginosus (Pl), and P. royenii (Pr), including mean, standard deviation (in cm), sample size, coefcient of variation, and F values for each comparison. An asterisk ( ) indicates signicant difference among coefcients of variation (P < 0.05). The data of P. moritzianus, and P. lanuginosus are from Nassar et al. (1997). F:Pr/ Pm F:Pr/ Pl

P. mortizianus Flower length Corolla diameter Stigma length 4.30 0.06 N = 23 CV = 0.083 2.50 0.02 N = 23 CV = 0.009 4.70 0.04 N = 20 CV = 0.624

P. lanuginosus 4.20 0.15 N = 22 CV = 0.496 2.30 0.06 N = 22 CV = 0.079 4.00 0.16 N = 22 CV = 0.562

P. royenii 4.30 0.89 N = 23

9.43 1.58

CV = 0.785 2.95 0.53 31.33 3.6 N = 23 CV = 0.282 4.75 1.03 N = 19 CV = 1.061

1.007 1.89

FIGURE 4. Average number of seeds ( SD) per fruit after cross-pollination (N = 15), self-pollination (N = 15), visits by Xylocopa mordax (N = 15), and unmanipulated control owers (N = 15). Different letters indicate signicant differences at = 0.05 in a Tukeys test.

DISCUSSION
Based on studies of other cacti of the same genus (Sosa & Soriano 1996, Nassar et al., 1997, Ruiz et al. 1997), we hypothesized that P. royenii would be similar to its congeners in owering phenology, as well as most oral traits associated with bat pollination. We predicted differences in the breeding system and expected that the pollination system would be more generalized. Furthermore, if the pollination system was indeed generalized, then we expected that oral traits associated with pollinator attraction and pollination mechanics would be more variable than that of strictly bat-pollinated cacti. We found that average nectar volume produced by P. royenii (1.285 ml/ower/night; SD = 0.389 ml/ower/night) is similar to other bat-pollinated species and falls within the range typical of bat-pollinated columnar cacti (1.071.98 ml/ower/night; Fleming et al. 1996, Valiente-Banuet et al. 1996, Nassar et al. 1997). Although more dilute than most other bat-pollinated cacti (e.g., Fleming et al. 1996, Valiente-Banuet et al. 1996), the average sugar concentration lies within the range of the Venezuelan cacti (18 22%; Nassar et al. 1997). Pilosocereus royenii is also similar to its congeners in owering phenology (Sosa & Soriano 1996, Ruiz et al. 1997). Our P. royenii population owered throughout the year, but ower production was highly irregular uctuating about 30-fold throughout the year (Fig. 3). Moreover, fruit production was asynchronous with rainfall or ower production, corresponding three times and lagging after a fourth owering peak. We did not detect any relationship between either owering or fruiting phenology, and either rainfall or reproductive activity of the bats, which for M. redmani is from December through February (Homan & Jones 1975). This is consistent with a loose relationship with the bats whose increased energy demands during reproductive periods fail to increase visitation and increase in fruit production (Ruiz et al. 1997).

differences between the means of the seed set produced by X. mordax visits, outcrossed pollinations, self-pollinations, and the control group (one-way ANOVA; F = 9.282; df = 3, 56; P < 0.001; Fig. 4). Tukeys test revealed that the main sources of variation were the low seed set from X. mordax pollinations (P < 0.001) and control treatments (P < 0.001). The common rat, R. rattus, was observed on three different occasions removing whole owers from P. royenii. As with the rat, the Troupial, I. icterus, also destroyed the owers it visited. Although the owers were not removed, the birds tore apart the corollas, possibly to access the nectaries. FLORAL MORPHOLOGY AND VARIABILITY.Correlations between seed set produced by X. mordax visits and ower length, corolla width, and stigma lengths were nonsignicant. We compared measurements of oral morphology of P. royenii with those of two species of Venezuelan Pilosocereus using the coefcients of variation (CV) of these traits for P. moritzianus and P. lanuginosus reported by Nassar et al. (1997). For all three measurements compared, the CVs were highest in P. royenii. Between P. royenii and P. mortzianus, variation in ower length (F = 9.43; P < 0.05) and corolla diameter (F = 31.33; P < 0.05) were signicantly different, but between P. royenii and P. lanuginosus the variation was signicantly higher only for corolla diameter (F = 3.6; P < 0.05). Although the CV for stigma length was nearly twice as high in P. royenii, the variation was not signicant between any of the species of Pilosocereus (Table 1).

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Contrary to expectations, P. royenii also has a mating system similar to related species (Nassar et al. 1997). Pilosocereus royenii is pollinator dependent and shows a number of characteristics that enhance the probability of cross-pollination. Flowers are protandrous and receptive stigmas extend well beyond the anthers. Furthermore, few owers are produced at a time (13) when they are produced at all. Hand-pollinations indicate that cross-pollinations produce more seeds than self-pollinations, which suggests that P. royenii is either partially self-incompatible or that some inbreeding depression occurs. Pilosocereus royenii was severely pollen limited during the study period, more so than nearly all other bat-pollinated columnar cacti (Fleming et al. 1996, 2001, Nassar et al., 1997). Natural fruit set was approximately 30 percent over the entire period of our study whereas hand-pollinations yielded 100 percent fruit set. Less than 30 percent of the owers we monitored for pollinator activity were actually visited; thus, the low fruit set is likely the consequence of infrequent pollinator visits. Reproduction was also limited by either the efciency of pollinators or the quality of pollinations. Seed set was signicantly higher for fruits produced from experimental cross-pollinations than selfpollinations, and fruits from open-pollinated plants were statistically indistinguishable from those of hand self-pollinations. We may have deposited more pollen on the stigmas than the pollinators or most fruits were products of geitonogamous pollinations. Flowers of P. royenii show traits typical of the chiropterophilous pollination syndrome, and we expected that bats would play a signicant role (although not the only one) in pollination. Our local nectarivorous bats, M. redmani, however, played no role in pollination of P. royenii in the Gu anica forest. The four nonpollinating visits by M. redmani, and the absence of fruit initiation for any of the 81 owers left available for nocturnal pollination indicate that the bat was not a pollinator. This lack of pollination by M. redmani is not necessarily due to a poor morphological t between owers and bats (observed visits occurred prior to stigma receptiveness), but may reect small population densities of these bats in the forest. After sampling with 33 m of mist net twice a week for seven consecutive hours, over a period of 1.5 yr at three nearby caves known to have harbored M. redmani colonies, only eight individuals were captured (B. Rivera-Marchand, pers. obs.) suggesting that the population is indeed small. Small populations of M. redmani in the Gu anica forest may be temporary. Jones et al. (2001) found that the population densities of bats in some areas of Puerto Rico declined dramatically after Hurricane Georges in 1998, with M. redmani among the most strongly affected. Due to widespread vegetation damage on the island (including Gu anica) caused by this hurricane, the population of M. redmani in Gu anica likely suffered a similar fate as those studied by Jones et al. (2001). With its low reproductive rate (SilvaTaboada 1979), and only 23 yr since the hurricane the Gu anica population may have not yet recovered. Severe pollination limitation occurred in the bird-pollinated Pavonia bahamensis of the Bahamas after the passage of a strong hurricane, and this was associated with a sharp decline in pollinator populations (Rathcke 2000). Unlike in our plants, no other pollinators

were involved. Because we do not have reproductive data for P. royenii before the hurricane, we do not know whether the carpenter bee, X. mordax, compensates for the absence of pollinating bats. Pilosocereus spp. in Colombia are considered a secondary food source for nectar-feeding bats, which seemed to rely more on other cacti for nectar (Ruiz et al. 1997). In Gu anica, alternative chiropterophilous cacti, such as Stenocereus hystrix (Haw.) Buxb., are much less abundant than P. royenii, averaging less than one individual per hectare (B. Rivera-Marchand, pers. obs.). Pilosocereus royenii would seem to be a more attractive food source, but its irregular and low rate of ower production may make this species a poor choice for diet specialization. Because the pollen vectors of P. royenii are animals other than bats, this system is more like those populations of chiropterophilous cacti found outside the tropics (e.g., the Sonoran desert: Fleming et al. 1996, 2001, Per u: Sahley 1996) than like its tropical counterparts (Curac ao: Petit 1995, Mexico: Valiente-Banuet et al. 1996, Venezuela: Nassar et al. 1997). Perhaps as a result of the lack of association with a bat pollinator, the owers are signicantly more variable than its exclusively bat-pollinated congeners. The copious nectar and pollen produced by P. royenii attracted many animals. The cactus received visits from at least seven different species of animals belonging to ve different orders. The only effective pollinator, however, was the carpenter bee, X. mordax. Because of their large bodies and robust foraging behavior within the owers, these bees contacted both anthers and stigmas. Pollinations by X. mordax yielded seed set similar to those of controls. Thus, these bees most likely accounted for all pollinations of P. royenii in Gu anica during our study. All other visitors may be considered thieves of the oral rewards offered by the cactus. The worst of these were honey bees that occupied owers for up to an hour while foraging for pollen and possibly nectar, and actively deterred all other visitors, including carpenter bees. Such aggressiveness may be responsible, at least in part, for low fruit set in P. royenii. Without bats pollinating P. royenii in Gu anica, one would expect that either selection on some oral characteristics would be relaxed or that activities of the carpenter bees would impose some directional or disruptive selection on oral characteristics. Our data favor relaxed selection. At least for the traits we measured we found no relationship between variation in ower morphometrics and reproductive success of the carpenter bee-pollinated owers. The bees were not selecting certain phenotypes and/or their buzzing and rummaging behavior within the owers resulted in highly variable seed set (Fig. 4). The morphological relationship between the two clearly is not one of a lock and key or the perfect t. The owers of P. royenii have traits related to bat pollination. Nevertheless, bats were not effective pollinators during the study. Effective visits by X. mordax, a pollinator not predicted by the plants pollination syndrome, is an indication of generalized pollination (Waser et al. 1996). Although the shape, color, aroma, nectar volume and concentration of P. royeniis owers suggest the chiropterophilous syndrome (Faegri & van der Pijl 1976), the effective pollination by X. mordax contradicts this prediction. Even though the carpenter bee was the sole pollinator of this chiropterophilous cactus during our study, we do not characterize the pollination

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system of P. royenii as either specialized or generalized because it may be simply a species in transition. If Hurricane Georges caused a decrease in the M. redmani population and if the bat recovers to become an effective pollinator of P. royenii, then the system may once again be functionally chiropterophilous. Selection regimes may then change and variation in oral characteristics may shift as has been demonstrated in other natural systems (e.g., Price et al. 1984, Schemske & Horvitz 1989). Carpenter bees are considered important pollinators on islands (e.g., McMullen 1989, 1993). Because of their resourceful foraging and nesting behavior (Jackson & Woodbury 1976, Roubik 1989, Scott et al. 1993), they may be extremely resilient to disturbances and unpredictable food sources. With a lack of a patterned owering period and low availability of owers per day, the cactus benets from an asymmetrical relationship with Xylocopa whose populations would not be sensitive to reduced ower densities of a particular species. Thus, the pollination biology of P. royenii contradicts the hypothesis that Neotropical chiropterophilous cacti are strictly pollinated by bats. In addition, pollinating activity of carpenter bees may be affecting variation in oral characteristics. Our data and that of others suggest that the chiropterophilous pollination syndrome in columnar cacti appears to break down in extratropical regions and islands subjected to periodic, severe disturbances.

ACKNOWLEDGMENTS
This research was supported by Fondo Institucional para la Investigaci on (FIPI) from the University of Puerto Rico, R o Piedras Campus. The Departamento de Recursos Naturales y Ambientales de Puerto Rico (DRNA) provided the necessary permits. We are especially indebted to Jaffett Nassar for sharing valuable data and offering advice. We thank Elvia Mel endez-Ackerman, Catherine N. Duckett, and Armando Rodr guez-Dur an for their comments on the manuscript. For their help in the eld we would like to thank Jennifer Fern andez-Betancourt, Erik Rivera-Marchand, Mayela Alsina, Kristy Barksdale, Jos e Fumero, Luis F. Castillo, and Gretchen Rivera. Finally we thank Luzelvia D az for her artistic services.

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