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0 Desert Botanical Garden, 1201 N. Galvin Parkway, Phoenix, Arizona 85008 USA
Received for publication February 11, 1999. Accepted for publication September 7, 1999.
ABSTRACT
I studied the pollination biology of two closely related species of agave, Agave palmeri and A. chrysantha (Agavaceae), which exhibit several chiropterophilous (bat-pollinated) traits. Floral studies, floral visitor observations, and pollination studies were conducted over four summers at six different sites to examine floral traits and determine the relative importance of diurnal vs. nocturnal pollinators. Agave chrysantha appears to have developed minor shifts in several floral characters that enhance diurnal pollination. Although floral shifts towards diurnal pollination were fewer in A. palmeri, stigmas were diurnally receptive and copious floral rewards were available in the morning, indicating that some adaptations exist to allow for multiple pollinators. Differences in fruit and seed set between naturally day- and night-pollinated umbels for both species were either not significant or significantly higher in day-pollinated plants. Bats were not important pollinators of A. chrysantha, and the mutualistic relationship between A. palmeri and the lesser long-nosed bat was found to be asymmetric. "Bat-adapted" floral traits appear to be flexible enough to respond to the climatic and pollinator unpredictability experienced by agaves at the northern edge of their distribution. This variability may be a more important factor affecting evolution of floral characters than a particular pollinator.
Key Words: Agave chrysantha • Agave palmeri • century plant • fruit set • Leptonycteris curasoae • lesser long-nosed bat • pollination • seed set
Agaves, or century plants, are perennial, rosette-shaped leaf succulents native to the southwestern United States, Mexico, Central America, and the Canary Islands. Many paniculate agaves exhibit floral characteristics suggestive of chiropterophily, or bat pollination (Howell, 1972
; Faegri and van der Pijl, 1979
; Gentry, 1982
; Sutherland, 1987
; Kuban, 1989
). These characteristics include flowers with large floral tubes that are presented in clusters on tall candelabra-shaped inflorescences, copious quantities of nocturnally produced nectar and pollen, pale yellow to yellow flowers, often with reddish tinged tepals, and a floral scent similar to fermenting or rotting fruit. Members of the Group Ditepalae of the genus Agave (Agavaceae) (sensu Gentry, 1982
) possess many of these "bat flower" traits and are largely distributed within the migratory range of the nectarivorous lesser long-nosed bat, Leptonycteris curasoae yerbabuenae Martinez and Villa (Fleming, Nunez, and Sternberg, 1993
). Phenological data suggest that several species of columnar cacti and Ditepalae agaves provide a "nectar corridor" for nectarivorous, migratory bats from spring as they migrate north, through the fall when they return to southern roosts (Gentry, 1982
; Fleming, Nunez, and Sternberg, 1993
). While columnar cacti form the bulk of available food for the lesser long-nosed bat during spring and early summer, the Ditepalae agaves bloom significantly later in the year (mean peak flowering period is August) than other paniculate agaves and columnar cacti, and can provide a potentially important food source during southern migration when other Crassulacean acid metabolism (CAM) plants are no longer available (Fleming, Nunez, and Sternberg, 1993
).
Agave palmeri Engelm. (Agavaceae), one of the northernmost distributed members of the Ditepalae, is native to savanna grassland and oak woodland communities of northern Mexico and southern portions of Arizona and New Mexico. Portions of the range of A. palmeri are sympatric with that of the lesser long-nosed bat (Fig. 1). Several studies (Howell, 1974, 1979
; Howell and Hodgkin, 1976
) have shown the lesser long-nosed bat, currently listed as an endangered species in the United States (Schull, 1988
), has a mutualistic association with A. palmeri. Howell and Roth (1981)
found high seed set in A. palmeri populations where bats were present, low seed set where bats were not present, and declines in fruit and seed set in herbarium specimens over a 30-yr period (but see Cockrum and Petryszyn, 1991
). They suggested that A. palmeri was "strongly dependent" upon the lesser long-nosed bat for pollination, although sphinx moths, carpenter bees, and other solitary nectar-feeding bats were indicated as potential, occasional pollinators (Howell, 1979
; Howell and Roth, 1981
). Howell and Roth (1981)
concluded that reported declines in lesser long-nosed bat populations (Hayward and Cockrum, 1971
; Howell and Roth, 1981
) could severely limit sexual reproduction of A. palmeri and other paniculate agaves. On the other hand, low fruit set has been shown to be common in outcrossing, largely self-incompatible hermaphroditic plants such as agaves (Sutherland and Delph, 1984
). Sutherland (1982, 1987)
found that fruit set in paniculate agaves was primarily resource limited with fruit set averaging 20% and that "excess" or aborted flowers played an important role in pollen donation and male fitness.
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) with an adjacent and partially overlapping range to the north (Fig. 1). Agave chrysantha occupies a variety of habitats, including desertscrub, chaparral, juniper woodland, and the fringes of pinyon pine-oak woodland communities of central and south-central Arizona. It also displays characteristics of bat pollination, such as nocturnal pollen dehiscence and nectar production, and a floral odor suggestive of ripening fruit. However, it has vivid yellow to yellow-orange flowers more typical of insect- or bird-pollinated flowers, and a distribution that is largely north of the range of nectar and pollen-feeding bats (Baker and Cockrum, 1966
) (Fig. 1). Schaffer and Schaffer (1977)
noted that a population of A. palmeri on the north side of the Santa Catalina Mountains (probably A. chrysantha) with bright yellow flowers appeared to depend on large bees for pollination.
Floral characters, phenology, and distribution patterns suggest that bats have been an important influence in Agave evolution. However, chiropterophilous agave species that occupy habitats at the edges or outside the range of nectarivorous bats can be successfully pollinated by other animals. Sutherland (1987)
noted that A. mckelveyana Gentry has nocturnal anther dehiscence and nectar production, but is primarily pollinated by diurnal insects. Agave havardiana Trel. in southern Texas was pollinated by the greater long-nosed bat (L. nivalis Saussure) at higher elevations, but white-winged doves (Zenaida asiatica L.) and orioles (Icterus parisorum Bonaparte) were the most significant pollinators in desert habitats (Kuban, 1989
). A variety of animals other than bats are known to visit flowers of A. palmeri and A. chrysantha (Schaffer and Schaffer, 1977
; Howell, 1979
; Howell and Roth, 1981
), but the characteristics of these relationships are not well understood. Additionally, the nature of the mutualistic relationship between the lesser long-nosed bat and A. palmeri appears to be unresolved based on current data. This study investigates the floral traits of A. palmeri and previously unstudied A. chrysantha and the importance of various pollinators on fruit and seed set. Floral traits, pollinator observations, and pollinator exclusion experiments were conducted over four summers in four populations of A. palmeri and two populations of A. chrysantha to address the following questions: (1) How do the floral traits of A. palmeri and A. chrysantha affect pollination? (2) Does the timing of pollen presentation and nectar production suggest adaptation strictly for nocturnal visitors? (3) Who are the diurnal and nocturnal floral visitors of A. palmeri and A. chrysantha and what are their relative contributions to fruit and seed set? (4) Does A. palmeri depend primarily on the lesser long-nosed bat for pollination? (5) Is pollinator limitation an important factor in sexual reproduction of A. palmeri and A. chrysantha? (6) What animals pollinate A. chrysantha and what are the reproductive implications of chiropterophilous traits in a plant that is largely distributed outside of the range of nectarivorous bats?
METHODS
Study sites
Research was conducted at six study sites in central and southern Arizona (Fig. 1). The study of geographic variation in plant-pollinator relationships can be informative (Thompson, 1994
), therefore 2–4 populations of each species were studied along a north-south gradient. Agave chrysantha study sites were located at the northern edge of its distribution in the Sierra Ancha Mountains (Parker Mesa site: 33°45' N, 110°58' W; 1400 m elevation), and near the southern edge of its range in the Santa Catalina Mountains (Peppersauce site: 31°33' N, 110°43' W; 1432 m elevation). Study sites for A. palmeri were located throughout the northern portion of its distribution in Arizona in the foothills of the Santa Rita Mountains (Santa Rita site: 31°47' N, 110°42' W; 1520 m elevation), the foothills of the Mustang Mountains (Mustang site: 31°43' N, 110°30' W; 1500 m elevation), Coronado National Monument (Coronado site: 31°21' N, 110°13' W; 1508 m elevation), and Fort Huachuca Military Reservation (Fort Huachuca site: 31°30' N, 110°18' W; 1507 m elevation). The Coronado site was located ~4 km from a transient lesser long-nosed bat roost occupied in July–October (V. Dalton, University of Arizona, personal communication). Research was conducted on A. chrysantha at the Parker Mesa site during 14–20 July 1993 and at the Peppersauce site during 5–11 July 1994. Agave palmeri studies were conducted at the Santa Rita site 3–9 August 1993, the Mustang site 1–7 August 1994, the Coronado site 14–20 August 1995, and the Fort Huachuca site 20–26 July 1998.
Floral trait studies
To characterize the phenology of each species, the flowering seasons of 13 A. chrysantha and 14 A. palmeri populations were recorded in addition to the above study sites. Populations were visited 1–3 times per year from June to September, and it was noted whether plants were flowering or not. Flowering dates of the above populations were also obtained from herbarium specimens located at Arizona State University (ASU) and the Desert Botanical Garden (DES).
Flower traits were recorded during flowering at five sites. Twenty flowers on 1–3 plants per site were numbered prior to dehiscence. The length of exserted style and condition of filaments, tepals and stigma were recorded once daily until stigmas wilted.
Anther dehiscence was studied at all sites but the Fort Huachuca site. Twenty numbered predehiscent flowers were observed starting shortly before dusk and examined hourly to determine time of anther dehiscence.
To determine whether nectar was produced diurnally, 24-h nectar accumulation studies were carried out at Parker Mesa (A. chrysantha) and Santa Rita (A. palmeri) sites. Nectar was measured every 2 h in 20 numbered flowers on 1–2 replicates (separate plants). Nocturnal nectar accumulation was studied at Peppersauce (A. chrysantha) and Mustang sites (A. palmeri) where nectar was measured every 3 h from 1800 to 0600 in 20 numbered flowers on three replicates (separate plants). For both nectar accumulation studies, the same flowers were sampled each day during the dehiscent, postdehiscent, early pistillate, and pistillate floral stages. Sampled flowers were located on umbels in the middle section of the inflorescence and exclosed from pollinators with a 1.5-mm nylon mesh netting beginning at 1800 (Howell, 1979
). Nectar was removed with a tuberculin syringe and blunt needle and was not replaced after removal. Nectar accumulation was also measured at the Fort Huachuca site, but a different nectar collection method was employed. Nectar was measured in ten predehiscent, dehiscent, postdehiscent, and all pistillate stage flowers on 29 replicates (separate plants). The same flowers were sampled throughout each floral stage. Flowers were bagged at dusk, and nectar was allowed to accumulate until dawn, and then measured.
Standing nectar crop was measured at the Peppersauce (A. chrysantha) and Mustang (A. palmeri) sites at dusk and dawn on 20 numbered predehiscent, dehiscent, postdehiscent, and pistillate stage flowers on 1–2 replicates (separate plants). Nectar sugar concentration (percentage sucrose equivalents on a mass/mass basis) of standing nectar crop flowers was measured at dawn on dehiscent and early pistillate stage flowers in A. chrysantha and dehiscent, postdehiscent, and early pistillate stage flowers in A. palmeri with a hand-held refractometer.
Nectar statistical analyses were conducted using SYSTAT 6.0 for Windows (SPSS, 1996
). Nectar sugar percentage data were arcsine transformed prior to analysis (Zar, 1984
), but data are reported as percentages in this paper.
Floral visitor observations
To determine pollinator visitation rates and patterns, observations of pollinators were conducted over 3–4 d at all study sites, except the Santa Rita site where stormy weather limited observations to a single day. Flower visits were observed closely to determine whether or not stigma contact was made. Visitors were classified as pollinators if they appeared to transfer pollen to exserted (postdehiscent to pistillate) stigmas. Bat visits were generally <1 s, and it was difficult to determine by visual observation whether stigma contact was made. I assumed that bat visits that caused movement of the umbel (a lateral branch of the inflorescence with flowers borne in umbellate clusters) were a result of stigma contact with the bat's body. Night vision goggles (M973, Litton Co., Tempe, Arizona, USA) were used for nocturnal studies. Visitation rates of insects (primarily bees and moths) were determined by counting the number of insect visits to flowers on an umbel for 10 min every 2 h during the day (~0500–1900) and three times during the night (~2100, 2400, and 0400). Insects were observed from a ladder ~1.5 m from the study umbel. Birds and bats were observed 10–20 m from the inflorescence. Visitation rates of birds were measured by counting the number of visits to open flowers on an inflorescence for 1 h shortly after dawn, during mid-day, and 1 h prior to dusk. Bat visitation rates were determined by observing a clumped group of inflorescences for ~1 h after dusk, near midnight, and before dawn at the Santa Rita and Mustang sites. One inflorescence was observed from 2000 to 0430 on 16–17 August and 17–18 August at the Coronado site. Predominant flower stage(s) (predehiscent, dehiscent, postdehiscent, and pistillate) of each observed umbel was recorded. Identity of visitor, visitation behavior, and general environmental conditions were also noted. Bats were identified visually with night vision goggles using tail membrane characteristics; the lesser long-nosed bat has a very reduced tail membrane, which distinguishes it from the sympatric Mexican long-tongued bat (Choeronycteris mexicana Tschudi) (Hoffmeister, 1986
). Insects were collected while they visited flowers and stored for later identification.
Pollination experiments
To evaluate the relative importance of diurnal and nocturnal pollinators, the following pollinator exclusion experiments were performed on both Agave species. Experimental plants were centrally located within a population, if possible. Test umbels were chosen from the middle section of inflorescences, and 15 plants each were randomly assigned to one of the following treatments: (1) control umbels available to both diurnal and nocturnal visitors, (2) umbels available only to diurnal visitors (umbels bagged at sunset and unbagged at sunrise), (3) umbels available only to nocturnal visitors (umbels bagged at sunrise and unbagged at sunset), and (4) umbels bagged, but receptive stigmas were liberally hand-pollinated daily (from 0700 to 1100) with fresh pollen collected from different individuals within the population (Peppersauce and Mustang sites only) until they wilted. Umbels were bagged prior to stigma receptivity (generally after anther dehiscence), and bagging continued until all styles were wilted (4–5 d). Umbels of experimental and control plants were collected in October and November when fruits were partially dry but undehisced, number of mature fruits and aborted flower scars on each umbel were counted, and percentage fruit set was determined [number of fruits/(number of fruits + aborted flower scars)]. Mean seed set per fruit [number of black, fertilized seeds/(number of black, fertilized seeds + number of white, unfertilized ovules)] was determined for the Peppersauce, Mustang, and Coronado sites. Fruit and seed set data had non-normal distributions and heterogeneous variances and were analyzed with distribution-free multiple-comparison procedures (Edgington, 1995
) using the MRPP procedure (multiresponse permutation procedure) of BLOSSOM Statistical Software (Slauson, Cade, and Richards, 1994
). Probability values were adjusted using the Bonferroni procedure (Edgington, 1995
).
To determine whether differences existed in diurnal and nocturnal pistil receptivity of A. palmeri, anthers were removed from 30 predehiscent flowers from each of 13 plants at the Fort Huachuca site, and flowers were exclosed with nylon mesh netting. Once flowers became receptive (evening of day 4), five flowers per plant were hand-pollinated at dusk (1900–2000) and rebagged. Five additional flowers were hand-pollinated on each plant the next morning (day 5, 0600–0800). This procedure was repeated on the evening of day 5/morning of day 6 and the evening of day 6/morning of day 7. Donor pollen was gathered from several plants that were not in the experimental group. Fruits were collected in mid-October 1998, and fruit and seed set data were analyzed by one-way repeated-measures ANOVA using SYSTAT 6.0 for Windows (SPSS, 1996
). Fruit and seed set percentage data for receptivity experiments were arcsine transformed prior to analysis (Zar, 1984
), but are reported in this paper as percentages.
To determine whether A. chrysantha and A. palmeri were self-compatible, anthers from 15 predehiscent flowers were removed from ten plants each of both species at the Peppersauce and Mustang sites. Flowers were covered with nylon mesh netting, hand-pollinated on the evenings of days 4–6, and rebagged. Donor pollen was gathered from freshly dehiscent flowers from the same or an adjacent umbel. Fruits were gathered in October and November 1994, and mean fruit set was determined for each species.
The total number of fruits and aborted fruits was counted on control and experimental inflorescences at all study sites to determine mean fruit set of inflorescences for each population.
RESULTS
Floral trait studies
Although the flowering periods of the two taxa overlap partially, A. chrysantha had an earlier flowering period. At lower elevations (700–975 m) A. chrysantha began flowering in late May–early June. Peak flowering at mid-elevations (975–1650 m) where study sites were located occurred through June and July, and flowering continued at higher elevations (1700–2130 m) into early August. Agave palmeri began flowering in late June–early July at lower to mid-elevations (1000–1500 m) with peak flowering occurring from late July to August (1220–1828 m) and extending through September–early October.
Both agave species were protandrous, gradually changing from a staminate to pistillate state over a 5–6 d period. On day 1 of flowering (predehiscent stage), the tepals opened and the filaments and anthers were exserted above distal tips of tepals. Flowers remained in this condition until the evening of day 2 or early morning of day 3 (dehiscent stage) when anthers dehisced and pollen was presented. Stigmas were tightly closed at dehiscence, although styles had begun to elongate. Agave chrysantha styles were exserted 0–15 mm beyond tepals on the morning of day 3 (postdehiscent stage), whereas styles in A. palmeri were exserted 15–35 mm. On the morning of day 4 (early pistillate stage), the tripartite stigmas were usually closed, but were generally moist and open by evening. Thus, flowers became receptive ~48 h after anther dehiscence. Filaments began to wilt on day 4 with styles exserted 16–27 mm in A. chrysantha and 25–40 mm in A. palmeri. By the morning of day 5 (pistillate stage), stigmas were open and sticky, and filaments were completely wilted by the end of the day. Styles were exserted 21–30 mm and 25–48 mm in A. chrysantha and A. palmeri, respectively. Tepals were generally wilted by the morning of day 6 (late pistillate stage), and stigmas varied from being widely parted and moist to dry and slightly wilted. Styles of both taxa were thoroughly wilted by day 7. Floral scent differed between taxa. Agave chrysantha flowers had a mild odor, often coconut-like, while flowers of A. palmeri had a much stronger odor, which resembled fermenting or rotting fruit.
Time of pollen dehiscence differed significantly between taxa (Pearson chi-square, 
2 = 1374; df = 3, P < 0.001). Ninety-five percent (N = 360) of A. palmeri anthers dehisced shortly after sunset between 2000 and 2200 of day 2, while 96% (N = 340) of A. chrysantha anthers dehisced later, between 2400 of day 2 and 0200 of day 3. Occasionally, all six anthers in a flower did not dehisce on the same night, and the remaining undehisced anthers opened the following night. No matter what day anthers dehisced, all A. palmeri anthers dehisced between 2000 and 2400 and A. chrysantha anthers dehisced between 2400 and 0300.
Results of 24-h nectar accumulation experiments showed that nectar production was nocturnal in both species with no nectar produced from ~0600 to 2000. Flowers in nocturnal nectar accumulation studies produced the most nectar on days 1–3 (predehiscent, dehiscent, and postdehiscent stages), with nectar production declining thereafter (Fig. 2, Table 1). Daily nocturnal nectar accumulation was greater in A. palmeri (repeated-measures nested ANOVA, F1,4 = 21.051, P = 0.010) (Fig. 2), but the pattern among days was somewhat dissimilar between species (F3,12 = 5.834, P = 0.011). Thus, nectar accumulation among days was analyzed separately for each species. Nectar production significantly decreased between days 3 and 4 in A. chrysantha (postdehiscent/early pistillate) (Tukey's multiple-comparisons procedure with Bonferroni adjustment, P < 0.05) and between days 3–4 (postdehiscent/early pistillate) and days 4–5 (early pistillate/pistillate) in A. palmeri (Tukey's multiple-comparisons procedure with Bonferroni adjustment, P < 0.05) (Table 1).
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Mean nectar sugar concentrations of dawn samples of day 2 (dehiscent) and day 4 (pistillate) flowers were significantly higher in A. chrysantha than A. palmeri (t test with Bonferroni adjustment: dehiscent, t = 9.229, df = 36, P < 0.01; pistillate, t = 3.030, df = 38, P < 0.01) (Table 2). Nectar sugar concentrations significantly decreased between dehiscent (day 2) and pistillate (day 4) flowers of A. chrysantha (repeated-measures ANOVA, F1,18 = 29.862, P < 0.001). For A. palmeri, postdehiscent nectar sugar concentrations were significantly higher than dehiscent or pistillate concentrations (repeated-measures ANOVA, F2,17 = 42.639, P < 0.001).
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, carpenter bee (Xylocopa californica arizonensis Cresson) activity tended to peak later in the morning and continue through the afternoon. Peak visitation (2.4 visits/min) for hummingbirds at the Coronado site was during mid-day, but was generally during mid-morning and prior to dusk at other sites. Noctuid moths and sphinx moths were most active shortly after dusk, although sphinx moths were active near dawn as well. Moths differed in their foraging behavior. Sphinx moths hovered above flowers and probed for nectar, only occasionally landing on the umbel, while noctuid moths landed and crawled upon umbels. Visitation rate varied as a function of nectar production. Umbels with the highest visitation rates were predominately predehiscent/dehiscent (3.5–4.7 flower visits/min) and dehiscent/postdehiscent (3.5–3.9 flower visits/min), while rates were lowest in umbels containing predominately pistillate stage flowers (0.13–2.3 flower visits/min).
The proportion of stigma contacts in A. chrysantha (Parker Mesa and Peppersauce sites) was highest for pipevine swallowtail butterflies (Battus philenor L.) (0.25, N = 20 total visits scored), followed by carpenter bees (0.15, N = 13), houseflies (0.06, N = 16), bumble bees (0.04, N = 156), wasps (Polistes sp.) (0.01, N = 58), and honey bees (0.003, N = 1115). For A. palmeri (Santa Rita, Mustang, and Coronado sites), stigma contacts were most frequent for lesser long-nosed bats (1.00, N = 32), white-lined sphinx moths (0.18, N = 49), carpenter bees (0.07, N = 158), small unidentified bees (0.02, N = 111), bumble bees (0.01, N = 628), honey bees (0.002, N = 774), and broad-tailed hummingbirds (0.007, N = 1431). Of the total observed visits, diurnal insects only contacted stigmas ~1% of the time in both Agave species. Of the three diurnal insects (carpenter bee, bumble bee, and honey bee) that contacted stigmas of both A. chrysantha and A. palmeri, bumble bees had significantly higher stigma contact rates in A. palmeri (Fisher exact test, P = 0.017). Stigma contact rates for nocturnal insect visitors were 0% for A. chrysantha and 6% for A. palmeri, while 0 and 0.6% of bird visitations resulted in stigma contact in A. chrysantha and A. palmeri, respectively. All of the observed bat visits to A. palmeri resulted in stigma contact.
The small size of the majority of insect visitors allowed them to "rob" nectar by entering flowers above the tepals, avoiding the exserted, receptive stigmas. Honey bees were large exploiters of floral rewards, and probably performed little pollination due to their small size and foraging habits. Honey bees tend to gather pollen from a single inflorescence (McGregor et al., 1959
; Alcorn, McGregor, and Olin, 1961
), suggesting that if contact with receptive stigmas occurred, fertilization was unlikely as these species are largely self-incompatible (see Pollination studies section; Howell and Roth, 1981
). Stigma contact generally occurred when insects landed awkwardly on umbels and touched stigmas, or while foraging on freshly dehiscent anthers with erect filaments, they crawled over adjacent receptive stigmas. Native bumble bees and carpenter bees were fairly successful as pollinators as their intermediate size and awkward landing abilities often made it difficult for them to avoid exserted stigmas. Although larger than bees, hummingbirds and sphinx moths could generally hover and avoid stigmas unless foraging in the middle of moderate to large-sized umbels. Hummingbirds, despite their larger size, were more adept at avoiding stigmas than sphinx moths and were only slightly more effective than honeybees as pollinators. Although bat visitations rates were low, their large size and foraging behavior (dropping their head into or very near the umbel to lap nectar) resulted in regular contact with exserted stigmas.
Pollination studies
No significant differences were observed in mean fruit set between naturally day- and night-pollinated experimental umbels, except for A. chrysantha at the Peppersauce site where diurnally pollinated umbels had significantly higher fruit set than those which were nocturnally pollinated (Table 4). Although differences were nonsignificant at other sites, day-pollinated treatments had higher mean values than night-pollinated treatments at each site, including the A. palmeri population (Coronado site) where bats were seen. Day-pollinated umbels were generally pollinated as well as flowers open to both day and night visitors; control fruit set was only significantly higher than day-pollinated fruit set at the A. palmeri Coronado site. Among populations of the two species, control fruit set was quite similar (16.6–23.8%).
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No significant differences were noted between seed set of naturally night-, day-, or control-pollinated plants at the Peppersauce site (A. chrysantha) or the two A. palmeri sites (Mustang and Coronado) where seeds were counted (Table 4). Several fruits had <1% seed set. Hand-outcrossed umbels had significantly higher seed set than all naturally pollinated treatments of A. chrysantha and A. palmeri.
Fruit set in receptivity experiments of A. palmeri (Fort Huachuca site) was greatest in flowers that were hand-pollinated at the onset of receptivity (evening of day 4), and receptivity steadily decreased over the remaining floral stages (Fig. 4). Fruit set was significantly higher in flowers pollinated on the evening of day 4 than those pollinated the next morning (day 5) (one-way repeated-measures ANOVA, F1,12 = 6.720, P < 0.024). Flowers pollinated on the evening of day 5 also had significantly higher fruit set vs. those pollinated on the morning of day 6 (one-way repeated-measures ANOVA, F1,12 = 8.094, P < 0.015). However, there were no significant differences in fruit set between flowers pollinated in the morning or evening of day 5 or the morning or evening of day 6. Similar to fruit set results, seed set was significantly higher in flowers pollinated on the evening of day 4 than flowers pollinated the next morning on day 5 (one-way repeated-measures ANOVA, F1,12 = 12.995, P < 0.004) and in flowers pollinated on the evening of day 5 vs. those pollinated on the morning of day 6 (one-way repeated-measures ANOVA, F1,12 = 12.957, P < 0.004) (Fig. 5). Seed set was significantly different between flowers pollinated in the morning and evening of day 5 (day 5 a.m./day 5 p.m., one-way repeated-measures ANOVA, F1,12 = 4.541, P < 0.050).
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Floral traits and pollinators
Species diversity in Agave is highest in the mesic habitats of central Mexico (Gomez Pompa, 1963
) where the evolution of inflorescence and floral characters in paniculate agaves may have been significantly influenced by bat pollination (Howell, 1972
; Gentry, 1982
). However, many species have successfully radiated into more arid environments of northern Mexico and the southwestern United States, which are beyond or near the edges of the range of nectarivorous bats. Agave palmeri and A. chrysantha are two such species, representing the northernmost members of the Group Ditepalae, which is centered in the Sierra Madre Occidental. Kuban (1989)
has argued that floral adaptations that arose as a result of bat pollination pre-adapted many agaves to a multiple vertebrate pollinator syndrome, and that these floral characters have been so effective that only minor changes in the agave "bat pollination syndrome" have occurred. For example, keeping flowers open during the day may be the key adaptation for using diurnal pollinators, as in some columnar cacti (Fleming, Tuttle, and Horner, 1996
). Kuban (1989)
noted that A. havardiana, although retaining many chiropterophilous traits, had differences in floral characters (such as nectar sugar concentrations and pistil receptivity) between populations that suggested adaptation to different levels of bat and bird visitation. Agave chrysantha has also retained several typical chiroptophilous features such as nocturnal anther dehiscence, nocturnal nectar production, and peak stigma receptivity on the first night of receptivity. Although A. chrysantha produces less nectar per night than A. palmeri, volumes are still great enough to be attractive to bats. However, results of this study suggest A. chrysantha has evolved minor shifts in floral characteristics (such as pollen dehiscence closer to dawn, production of nectar later at night, a sweeter floral scent, and bright yellow flower color) that may promote a multiple or generalist pollinator syndrome. The high fruit and seed set of hand-outcrossed (pollinated from 0700 to 1100, Peppersauce site) and naturally day-pollinated treatments (Parker Mesa and Peppersauce sites) suggest that pistil receptivity is also relatively high diurnally. These floral changes may have evolved to attract more diurnal visitors as A. chrysantha expanded its range northward where bats were no longer reliable visitors.
Although the floral characteristics of A. palmeri have not shifted towards diurnal pollinator adaptations to the degree shown by A. chrysantha, several traits indicate that some adaptations exist to allow for multiple pollinators. Pollen dehiscence and nectar production occurred nocturnally in A. palmeri, but large amounts of pollen and nectar were available in the morning to attract diurnal pollinators (Table 1). This study found nectar accumulation to be 2–2.5 times greater at all sites than that reported by Howell (1979)
in the Chiracahua Mountains, but similar to values reported by Schaffer and Schaffer (1977)
in the Huachuca Mountains. Hand-pollination (conducted from 0700 to 1100 on days 4–6, Mustang site; Table 4) and daytime receptivity experiments (conducted from 0600 to 0800 on days 5–7, Fort Huachuca site; Figs. 4–5) demonstrated that significant diurnal fruit and seed production took place and that stigmas remained receptive throughout a 3-d period. These results are similar to the diurnal receptivity reported by Kuban (1989)
in A. havardiana and Fleming, Tuttle, and Horner (1996)
in saguaro cacti. Diurnal stigma receptivity was found to be higher in this study than in previous reports. Seed set the morning of day 5 was 40% and remained above 20% until the evening of day 6 (Fig 5), while Howell and Roth (1981)
found diurnal seed set was ~20–30% between 0600 and 1800 on day 5. Although pistil receptivity decreased over time (Figs. 4–5), no significant differences in fruit or seed set were observed between naturally day- and night-pollinated treatments (Table 4). Thus, despite the existence of several floral features that indicate bat pollination in A. palmeri, these characters are general enough to allow visitation by a large variety of animals that can affect pollination, including many diurnal animals.
Gregory (1963, 1964)
and Waser (1978)
have noted that plants with characteristics of a particular pollination syndrome may often depend on other animals for the majority of pollination. While both A. chrysantha and A. palmeri exhibit characteristics of chiropterophily, fruit and seed set results showed diurnal animals were important pollinators in both Agave species. At one of the A. chrysantha study sites (Peppersauce), diurnal pollinators were the primary pollinators. Although a large number of diurnal animals visiting Agave flowers were "thieves," pollination was achieved when animals accidentally made contact with receptive stigmas while foraging. Insect pollination (particularly by bumble bees and carpenter bees) occurred primarily by the "mess and soil" procedure, an imprecise method of pollination whereby insects become covered with pollen and eventually contact a stigma by "messing about" in simple flowers (Faegri and van der Pijl, 1979
). Although the relative effectiveness of this rather primitive method was observed to be low, the high density and visitation rates of diurnal insects (Table 3) contributed substantially to pollination. Prolonged viability of agave pollen may also improve the pollination success of diurnal insects. Although pollen viability was not tested in these field experiments, Kuban (1989)
reported that pollen may remain viable for 3 d after dehiscence. Pollen deposited on unreceptive stigmas by diurnal insects during the flurry of postdehiscence visitation may later contribute to pollination when stigmas become receptive.
Diurnal pollination appeared to be largely due to insects as hummingbirds were seldom observed touching stigmas and other bird visitors were rare (Table 3). Kuban (1989)
found many bird visitors to A. havardiana besides hummingbirds, while Martinez del Rio and Eguiarte (1987)
found several passerines commonly visiting at one A. salmiana Otto ex Salm site, and only one species at another site. It is possible that birds were wary of observers within 10 m of plants, but approach and avoidance behavior was only rarely observed in this study.
Nocturnal pollinators (moths or sphinx moths) were important pollinators in three of the four sites where bats were not observed. Night pollinators contributed little to fruit set (2.2%) in A. chrysantha at the Peppersauce site, and this rate approximated self-pollination rates of fruit set (1.5%) reported by Sutherland (1982)
and results of selfing experiments (1.2%) conducted at the site. Interestingly, sphinx moths were not observed at the Peppersauce site, while they were observed at the Parker Mesa site where nocturnal fruit set was 14.9%. Results of this study suggest that sphinx moths, along with large native bees (bumble bees and carpenter bees), are more important as pollinators of both A. chrysantha and A. palmeri than previously thought.
The nectarivorous Mexican long-tongued bat (Choeronycteris mexicana) is present from roughly May–September in southeastern Arizona where its range overlaps with A. palmeri and southern populations of A. chrysantha. Although it is known to use A. palmeri as a food source (Howell and Roth, 1981
) and may potentially use A. chrysantha as well, it was not observed at any of the study sites. Little is known about this rather solitary bat that roosts in very small groups, but it is a potentially important pollinator of agaves in localized areas.
Importance of the lesser long-nosed bat as a pollinator
Bats were not observed at any of the A. chrysantha study sites and were probably not present in southeastern Arizona during study periods. Lesser long-nosed bats do not normally arrive in southeastern Arizona until late July and were not known to be present in the region during early July when exclosure experiments were conducted. In fact, the arrival period of the lesser long-nosed bat to southern Arizona is well past the peak flowering period of A. chrysantha throughout most of its range, and many populations have completed flowering by the time of the bats' arrival. Because lesser long-nosed bats may forage 24–32 km from roosts when feeding on columnar cacti (Dalton, Dalton, and Schmidt, 1994
; Sahley, Horner, and Fleming, 1993
), some southern populations such as the Peppersauce site (16–32 km away from the closest known roosts) are presumably within the bats' foraging range. However, the majority of A. chrysantha populations are located well beyond this distance. The Parker Mesa site is located over 160 air km north of the closest known roost (Cockrum and Petryszyn, 1991
), making even sporadic bat visitation unlikely. Results of pollination experiments, combined with present knowledge about the distribution and phenology of A. chrysantha and the migratory patterns of the lesser long-nosed bat, suggest that bats are not currently important pollinators of A. chrysantha.
Fruit and seed set results of this study did not support the hypothesis that A. palmeri is strongly dependent upon the lesser long-nosed bat for pollination. Although A. palmeri is believed to be the primary food source of the lesser long-nosed bat during August–September in southeastern Arizona, the lesser long-nosed bat was not found to be the sole pollinator of A. palmeri. In no case did night pollinators contribute to higher fruit set than daytime pollinators or controls, even when bats were nocturnal visitors to flowers. Rather, both diurnal and nocturnal pollinators played an important role in the pollination of A. palmeri. Although a trend towards greater diurnal fruit set was observed in both species, high variability in fruit and seed set was present in all populations (Tables 4–5) and may be a factor in the lack of detectable significant differences between some treatments. Factors other than pollinator availability may also influence agave fruit and seed set, such as umbel position within the inflorescence (Sutherland, 1987
), spatial arrangement of inflorescences (Howell and Roth, 1981
), genetic factors, and resource availability (Sutherland, 1982
).
In addition to fruit and seed set results, bat migration and phenological data do not provide strong evidence for an obligate mutualism between A. palmeri and the lesser long-nosed bat. Several workers (Cockrum and Petryszyn, 1991
; Fleming, Nunez, and Sternberg, 1993
) have suggested that seasonal movements of lesser long-nosed bats may be quite variable, particularly in the northern portion of their range. Lesser long-nosed bats arrive at known roosts in southeastern Arizona anytime from late July to mid-August (B. Alberti, Coronado National Monument, personal communication), while A. palmeri growing in the vicinity of these roosts may begin flowering as early as late June–early July. Flowering is asynchronous in A. palmeri, and one-third–one-half of the total floral crop may have finished flowering before the arrival of bats. Early-flowering plants would be completely or nearly through flowering in a late bat-arrival year. Kuban (1989)
also noted unpredictable arrival of the greater long-nosed bat in relation to peak flowering of A. havardiana, a chiropterophilous agave that uses multiple pollinators presumably as a result of pollinator variability. Even when bats arrive during peak flowering, their numbers are often low. At the Fort Huachuca site, 87% of plants were flowering on 28 July 1998, but only a few hundred bats were present in nearby roosts (B. Alberti, Coronado National Monument, personal communication). The lack of synchrony in the flowering of A. palmeri and the arrival of lesser long-nosed bats does not indicate a tightly coevolved relationship, but suggests that A. palmeri employs a more generalist pollinator strategy, at least in northern populations.
Pollinator limitation
Fruit and seed set of hand-pollinated umbels greatly exceeded that of control umbels and indicated some pollinator limitation existed at the time of flowering of experimental umbels. Low numbers of bats, inefficient pollination by diurnal pollinators, and removal of pollen by bees may have all contributed to low pollination rates. Sutherland (1982)
also found that hand-pollinated single branches (umbels) of A. chrysantha had significantly higher fruit set than single branches that were naturally pollinated, but when all umbels (entire inflorescences) were hand-pollinated, there were no significant differences in fruit set between hand-, hand + natural, and naturally pollinated inflorescences (~20% fruit set). Sutherland concluded that paniculate agaves were primarily resource, rather than pollen, limited.
Although some pollen limitation was observed in outlying plants and some umbels of control plants in this study, percent fruit set of control umbels and entire inflorescences averaged ~20% (Tables 4–5), even at sites where bats were not observed. The "high" fruit set reported by Howell and Roth (1981)
in bat-pollinated populations of A. palmeri may have been a result of inadequate sample size or the normal variability that can occur among branches, while the "low" results may be more representative of normal fruit set. A few plants had zero fruit set despite hand-pollination, implying that genetic incompatibilities or meiotic problems may have existed. However, results of this study suggest that pollen limitation and genetic factors play a smaller role than resource limitation in the pollination biology of agaves, and in particular, bats were not critical for adequate sexual reproduction in the populations of A. palmeri and A. chrysantha examined. Nonetheless, on a per visit basis, lesser long-nosed bats appear to be effective pollinators because some stigma contact generally occurs when bats visit. Kuban (1989)
noted the greater long-nosed bat had higher pollinator effectiveness vs. other pollinators when visiting A. havardiana. As very effective pollinators, even low numbers of bats may enhance fruit and seed set to levels that can be supported by a particular plant's resource pool.
Mutualisms and agaves
In a review of mutualisms, Bronstein (1994)
noted that it is common for dependence within a mutualistic relationship to show some degree of asymmetry. While Valiente-Banuet et al. (1996)
and Nassar, Ramirez, and Linares (1997)
have shown that the relationship between nectar-feeding bats and columnar cacti is mutualistic and partially symmetrical in tropical zones (bats depend on cacti for food during part of the year while plants depend on bats for pollination), Fleming, Nunez, and Sternberg (1993)
and Fleming, Tuttle, and Horner (1996)
have illustrated an asymmetrical pattern in temperate zones (bats depend on cacti for food during part of the year, but plants do not require bats for pollination). Year-round residency of nectar feeding bats in tropical areas may have promoted tighter mutualistic relationships between some columnar cacti and bats, while the unpredictability of migrant nectarivorous bats in the Sonoran Desert may have favored the development of floral characters that enhance diurnal pollination (Fleming, Tuttle, and Horner, 1996
). This same scenario may be equally as valid for chiropterophilous agaves distributed in temperate regions.
It is noteworthy that several striking similarities in floral and reproductive biology exist between columnar cacti and agaves distributed at the edges of the range of nectarivorous bats. Nectar production curves of organ pipe [Stenocereus thurberi (Engelm.)Buxbaum] and cardon [Pachycereus pringlei (S. Watson) B. & R.] cacti are like that of A. palmeri, with nectar production peaking between 2000 and 2400 and gradually declining, while nectar production in saguaro [Carnegiea gigantea (Engelm.) B. & R.] peaks after 2400 and is more evenly distributed, similar to A. chrysantha (see Fleming, Tuttle, and Horner, 1996
). Flowers of cardon and organ pipe opened shortly after sunset and closed by 0900, but flowers of saguaro were more similar to agave flowers, opening later at night (2300–2400) and remaining available to diurnal pollinators until 1500–1700 the next day. Like agaves, diurnal visitors contributed to the majority of fruit set in two of the three cacti species: birds were responsible for most fruit set in organ pipe, birds and bees were the principle pollinators in saguaro, while bats accounted for most fruit set in cardon. The relatively low importance of bats as pollinators of columnar cacti in the northern Sonoran Desert appears comparable to Ditepalae agaves that are distributed near the northern edge of the bats' range.
The variable climatic conditions and low number of agave and cacti species in the southwestern United States and northern Mexico may have contributed to the variable and unpredictable migration behavior in northern populations of lesser long-nosed bats (Valiente-Banuet et al., 1996
), and this may also explain why columnar cacti in the southwestern United States are not specialized for a particular type of pollinator (e.g., Alcorn, McGregor, and Olin, 1961
; Fleming, Tuttle, and Horner, 1996
) as compared to the highly specialized flowers of columnar cacti of southern Mexico (Valiente-Banuet et al., 1996
) or Venezuela (Nassar, Ramirez, and Linares, 1997
). Climatic variability may also be a factor in lack of pollinator specialization in agaves that are at the northern edge of the distribution of the genus. Community composition and species associations in the southwestern United States and northern Mexico have been in flux throughout recent geological time, and the effectiveness of mutalistic relationships would also seem to be unstable over the long term (Howe, 1984
). Waser et al. (1996)
noted that pollinator specialization is less likely in plants that experience spatial variation in pollinator fauna and temporal variation in pollinator service, particularly in species with few reproductive episodes. Agave chrysantha and A. palmeri seem to fit the bill as generalist species; they are monocarpic (after a prolonged vegetative stage, plants flower once and die), generally nonsuckering, and experience pollinator unpredictablity and variability.
Both A. chrysantha and A. palmeri have diffuse interactions with a variety of organisms that may result in their pollination. A generalist pollinator strategy may be more adaptive in monocarpic species that occur in diverse habitats (A. chrysantha) or have large geographic ranges (A. palmeri), allowing plants to use a variety of pollinators that may vary both temporally and spatially. Reproductive characteristics of agave species at the northern edge of their distribution may be subject to more intense selection as a result of climatic and pollinator variability rather than selection for particular pollinators or dispersal agents. The conservation of "bat-adapted" traits may reflect the variable and relatively unpredictable suite of diurnal and nocturnal animals that inhabit the fluctuating climates at the edges of agave geographic ranges.
FOOTNOTES
1 The author thanks S. Buchmann, T. Burgess, V. Dalton, T. Fleming, L. Landrum, J. McAuliffe, D. Pinkava, P. Scott, and an anonymous reviewer for helpful guidance and comments on the manuscript; B. Johnson, S. Ahearn, D. Hansen, C. Christy, J. Rebman, M. Johnson, K. Mueller, and volunteers and staff of the Desert Botanical Garden for field and laboratory assistance; S. Buchmann for assistance in insect identifications; R. King, statistician at the Rocky Mountain Research Station, for advice and consultation; Wendy Hodgson for map drawings, B. Alberti of Coronado National Monument, and S. Stone of Ft. Huachuca Military Reservation for permission to conduct this work and their invaluable assistance; Yar Petrysyzn for assistance with bat observations and identifications at Coronado National Monument; and W. Hodgson, K. Rice, and C. Edminster for their advice, assistance, and encouragement. This research was supported in part by funds provided by the Desert Botanical Garden, a P.E.O. Scholarship grant, the Department of the Army, Fort Huachuca, and the Rocky Mountain Research Station, U. S. Department of Agriculture, Forest Service. 
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