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Factors Affecting the Distribution, Pollination Ecology, and Evolution of Agave chrysantha Peebles and A. palmeri Engelm. (Agavaceae)

Liz Slauson1

Abstract.-Taxonomy, biogeography and pollination ecology of two closely related taxa of the Madrean Archipelago, Agave chrysantha Peebles and A. palmeri Engelm. are reviewed. Several questions remain regarding the reported obligate mutualism between A. palmeri and an endangered species of bat, Leptonycteris curasorae, and the role bats and other animals may play in the pollination of A. chrysantha. Preliminary evidence suggests that diurnal visitors play an important role in pollination of A. chrysantha and A. palmeri, and bats appear to have a more faculative role in pollination than previously thought. The seasonal, variable and migratory nature of Leptonycteris seems unlikely to support a tight mutualistic relationship with agaves. Plasticity in pollinator species may be most adaptive in agaves with large geographic ranges (A. palmen) and variable habitats (A. chrysantha). "Bat-adapted" traits may be just as advantageous to insects and other animals in hot and arid climates where peak activity is near dawn and dusk.

INTRODUCTION morphology was often grossly altered due to the unnatural conditions of cultivation in green­ Agaves are perennial leaf succulents consist­ houses of Europe, and as a result, most taxa ing of a basal rosette where water and described during this era are unrecognizable by carbohydrates are stored. Plants are monocarpic; their written descriptions alone (Gentry 1982). Al­ they require 10-50 years to reach maturity, then though botanists became more familiar with the initiate an'inflorescence, flower and die. Although genus during the early 1900's, they rarely ob­ the genus Agave (Agavaceae) is an important served agaves in habitat and failed to realize the vegetation component in the biotic communities large degree of leaf variability that can exist both of the Madrean Archipelago, reproductive, eco­ within and between populations. Floral characters logical and speciation processes are poorly were largely ignored, and the concentration on understood. Taxonomic problems have long con­ vegetative differences resulted in a large degree of tributed to a large degree of confusion. During the taxonomic "splitting" at the species level (Gentry early to mid-nineteenth century, agaves from the 1982). Other factors contributed to a poor under­ New World were imported to Europe as ornamen­ standing of agaves as well, Few botanists have tal novelties. Early taxonomists in Europe collected specimens due to the presence of teeth, attempting to name these cultivated species gen­ spines, caustic juices, and the difficulty in process­ erally had no information regarding their origin, ing specimens. Consequently, few specimens of provided no preserved or type specimens, no il­ each taxon have been available for study, many of lustrations, and used vegetative rather than which were poorly prepared and lacked floral or reproductive characters to diagnose species. Leaf other taxonomically significant characteristics. Numerous populations exist in rugged and inac­ cessible terrain which has resulted in limited

1Desert Botanical Garden, 1201 N. Galvin Parkway, Phoenix, AZ distributional data. The long time span required 85008. by members of this genus to reach reproductive

194 maturity makes ex-situ reproductive biology stud­ flowers with red to brownish tepal apices of A. ies or rapid evaluation of offspring difficult palmen), 4} more congested umbels, 5} shorter (Gentry 1982). Thus, large gaps in knowledge ex­ panicles, 6} broader and shorter lanceolate leaves ist with respect to ecology, reproductive biology, with large teeth, and 7} undulate to repand leaf cytology and genetics. margins (Gentry 1982). Agave chrysantha has been Gentry's (1982) more recent and comprehen­ recognized as a subspecies of A. palmeri (Little sive monograph of Agave emphasized 1943) and as a distinct species (Gentry 1982). Gentry comparative morphology, particularly with re­ (1982) has suggested that A. chrysantha may be a gard to floral characters. Species comprehension geologically young species which has not yet was greatly enhanced by his understanding of reached a stabilized or isolated condition, possibly morphological variability of populations and eco­ originating "through introgression with A. palmeri types, reproductive biology, introgression, andA. parryi." Alternatively, A. chrysantha may hybridization and polyploidy. Both polyploidy represent the northern end of a cline of A. palmeri and hybridization are common in Agave (x = 30), that has developed by primary or secondary inter­ and appear to be important mechanisms in the gradation with A. palmeri. evolution of the genus (Pinkava and Baker 1985). The pollination ecology of the Ditepalae is of This trend towards reticulate evolution appears to interest as several recent studies have suggested be due to a lack of complete reproductive isola­ that bats of the genus Leptonycteris are obligate tion between taxa recognized at the species level pollinators of A. palmeri (Howell 1979, Schaffer (Gentry 1967, Burgess 1979, 1985). The climatic and Schaffer 1979, Howell and Roth 1981). Howell fluctuations in the southwestern U.S. during the and Roth (1981) proposed that reported declines glacial-interglacial cycle of the Pleistocene may in Leptonycteris popUlations could potentially se­ have resulted in repeated periods of range expan­ verely impact sexual reproduction in paniculate sion and genetic interchange between species, agaves. This hypothesis was based on a decline in followed by periods of range contraction and iso­ seed set of herbarium specimens over a 30 year lation in small, disjunct populations (Burgess period and low fruit and seed set (approximately 1985). This repeated contact may have been suffi­ 25% and 20% respectively) in A. palmeri popUla­ cient to prevent development of reproductive tions where bats were absent. Fruit and seed set barriers. were high (81% and 700/0) where bats were pre­ The genus Agave is generally thought to have sent. No data were presented documenting visitor evolved in the mesic habitats of central" Mexico or visitation rates. Sutherland (1982, 1987) has (Gomez Pompa 1963), however, many species documented that mean fruit set for paniculate have successfully radiated northward into the agaves is generally low (20-25%), however, fruit more arid environments of northern Mexico and and seed set may be highly variable between the southwestern United States. The Group branches. The high fruit set reported by Howell Ditepalae within the genus Agave is composed of and Roth in bat-pollinated popUlations may be a 13 taxa primarily centered in the Sierra Madre Oc­ result of inadequate sample size, while the "low" cidental of Mexico, but two closely related results may be more representative of normal fruit members of this group, A. chrysantha Peebles and set. Cockrum and Petryszyn (1991) have ques­ A. palmeri Engelm., extend into central and tioned reported declines in Leptonycteris southern Arizona respectively, representing the numbers based on the fact that few observers northernmost distribution of the group. Agave have understood the variability and seasonality of palmeri occupies grama grasslands and oak Leptonycteris movement in the northern part of woodlands of northern Mexico and southern por­ its range (resulting in reports of absent, declining tions of Arizona and New Mexico, whereas Agave and low popUlation numbers). Herbarium speci­ chrysantha is found in desertscrub, chaparral, ju­ mens cited by Howell and Roth were reviewed by niper woodland and the fringes of pine-oak Cockrum and Petryszyn who obtained different woodland communities of central and southern estimates of fruit and seed set. They also noted Arizona. Both species may be found on granitic, that specimens cited by Howell and Roth were volcanic and limestone mountain slopes. Agave from localities which were either near the edge or chrysantha appears to be the nearest relative of A. beyond the known range of Leptonycteris. palmeri based on floral and other morphological Gentry (1982) postulated that other members characteristics, and differs from A. palmeri by 1) of the Ditepalae may have mutualistic associa­ its smaller flower size, 2) shallower tube, 3) clear tions with nectar-feeding bats due to their similar yellow perianth (versus the pale greenish-yellow flower structure. He proposed that a "wave of

195 nectar flow" exists from spring to winter, pro­ tance. Nectar production in bat-pollinated species viding food for bats as they migrate south. such as A. palmeri is nocturnal with peak pro­ Starting in the south with the March bloom of A. duction from 2000-2200 hours (Howell 1979). colorata in Sonora, this "nectar flow" moves Pollen protein content of bat-pollina'ted agaves north to Arizona for the summer with the flow­ tends to be high (44% in A. palmerl) while nec­ ering of A. palmeri, then extends south through tar sugar concentration is relatively low the Sierra Madre Occidental via A. shrevei in (11-20%) (Howell 1972). Bee-pollinated species southern Sonora, to A. durangensis in Chihua­ generally exhibit the opposite trend. Pollen pro­ hua, and finally to A. wocomahiin Durango and tein content is generally low (8-16%) (Howell Zacatecas which bloom into December. Arita 1972), although nectar sugar concentrations are (1991) has shown that the ranges of L. curasoae more variable (18-68%) (Schaffer and Schaffer and L. nivaJis significantly coincide with those 1977). Nectar production amount and pattern, of A. angustifolia, A. salmiana, and A. nectar sugar concentration and pollen protein tequilana, although this relationship may be due percentage are unknown in A. chrysantha. to the fact that both bats and agaves occur in Factors other than pollinators may be im­ arid areas. portant with regard to fruit set and reproductive The distribution of the majority of Ditepalae fitness in agaves. Sutherland (1982) found no members also coincides with the range of Lep­ significant difference in percent fruit set per in­ tonycteris, although A. palmeri is the only florescence in A. chrysantha when pollinated member with documented Leptonycteris polli­ naturally, pollinated naturally plus hand polli­ nation (Howell 1972, Howell and Roth 1981). nated, or hand pollinated alone, suggesting that Southern populations of A. chrysantha are po­ fruit set in agaves is not pollen or pollinator lim­ tentially within the range of Leptonycteris, ited, but rather resource limited. Udovic (1981) however, Baker and Cockrum (1966) have sug­ obtained similar results in a study evaluating gested that Leptonycteris probably never the effect of pollinators on fruit production in extended very far north of the Santa Catalina the semelparous species Yucca whipplei Mountains. Schaffer and Schaffer (1977) noted (Agavaceae). However, in a comprehensive that a population of A. palnleri (? A. chrysantha) study of fruit set in eight species of yucca, Addi­ with bright yellow flowers on the north side of cott (1985) found that pollinator limitation was the Santa Catalina Mountains probably de­ the factor that most often controlled fruit set. pended on large bees for pollinatiqn. Anther Genetic load may be a more important general dehiscence and peak nectar production in A. factor in reproductive success than both pollen chrysantha occurs at night, and flowers have a and resource limitation. Weins (1984) and Weins "ripening fruit" odor, all of which may attract et al. (1987) have shown that preemergent repro­ bats or moths. However, flowers are yellow in ductive success in outcrossing species is not color and have pollen and nectar available dur­ linked to resource or pollen availablity, but ing the day to attract diurnal pollinators. rather to genetic load (any lethal mutation or Howell (1979) has suggested that bat-pollinated allelic combination) as a result of meiotic recom­ agaves are derived from insect-pollinated spe­ bination. In a recent review considering the cies, and that A. chrysantha is an intermediate roles of pollen limitation, resource limitation form between primitive insect-pollinated and and genetic load in fruit and seed set, Burd advanced bat-pollinated species. On the other (1994) found significant pollen limitation oc­ hand, insect pollination may be secondarily de­ curred in the majority of species evaluated, and rived in A. chrysantha from bat-pollinated this pollen limitation generally varied among Ditepalae (Le., A. palmerl). Sutherland (1987) times, sites or years. This suggests the pollina­ noted that A. mckelveyana, another paniculate tion environment can be quite stochastic, form of Aga ve, also has nocturnal anther dehis­ resulting in frequent pollination limitation and cence and nectar production, but is primarily limited female success at the level of individual pollinated by insects. He postulated that agave flowers, entire plants or populations. floral characters are conservative and retain bat­ adapted traits despite predominate pollination The purpose of this study was to investigate by insects. the pollination ecology of A. chrysantha and A. Nectar production, nectar sugar concentra­ palmeri, and to determine the importance of tion and pollen protein analysis may also various diurnal and nocturnal pollinators with provide important clues to pollinator impor- regard to fruit and seed set.

196 METHODOLOGY hours) for diurnal visitors and three times during the night (approximately 2100, 2400 and 0430 Study Sites hours) for nocturnal visitors. Insects were ob­ served from a ladder approximately 1.5 m from Research took place at four study sites in cen­ the study umbel. Predominate flower stage(s) tral and southern Arizona. Agave chrysantha (predehiscent, dehiscent, post-dehiscent and pis­ study sites were located at the northern edge of its tillate) of each observed umbel was recorded. distribution in the Sierra Ancha Mountains above Identity of visitor, visitation behavior and envi­ Parker Creek (Parker Mesa Site, Gila County, T5N ronmental conditions were also noted. Insects R13E Sec. 24, elevation 1400 m) and near the were captured and mounted for later identifica­ southern edge of its range in the Santa Catalina tion. Mountains above Peppersauce Canyon (pepper­ sauce Site, TION R16E Sec. 21, elevation, 1450 m). Study sites for A. palmeri were located in the foot­ Pollen and Nectar Studies hills of the Santa Rita Mountains (Santa Rita Site, Pima County, T19S R16E Sec. 10, elevation 1520 Predehiscent flowers were observed during m) and the foothills of the Mustang Mountains the night to determine time of dehiscence. Nectar (Mustang Site, Santa Cruz County, 31°43'13.6" N production was measured on three replicates each latitude, 110°30'52" W longitude, elevation 1500 of 20 predehiscent, dehiscent, postdehiscent and m). Research was conducted at the Parker Mesa pistillate flowers every three hours from 2100 to Site during July 1993 and at the Santa Rita Site 0600 (no nectar is produced during the day) with during August 1933. Studies were conducted at a tuberculin syringe and needle. Experimental the Peppersauce and Mustang Sites during July flowers were located on umbels positioned in the and August 1994 respectively. middle section of the inflorescence and exclosed from pollinators with a fine nylon netting (Howell 1979). Standing nectar crop was measured at dusk Flower and Pollinator Observations and dawn on two replicates each of 20 predehis­ cent, dehiscent, postdehiscent and pistillate Twenty flowers were chosen and labeled prior flowers. Nectar sugar concentration of standing to dehiscensce. Time of pollen dehiscence,..length nectar crop flowers was measured at dawn in the of exerted style and condition of filaments, tepals field with a hand-held refractometer. and stigma were noted each day until stigmas wilted. Observations of pollinators were conducted over 3-4 days at all study sites, except the Santa Pollination Studies Rita site where pollinators were only observed one day due to stormy weather. Pollinators were Plants with inflorescences that were centrally determined by field observations of floral visitors located within a population were chosen at each who appeared to transfer pollen to receptive stig­ site for pollination experiments. Test umbels were mas. Night vision goggles were used for chosen from the middle section of inflorescences, nocturnal studies. Birds and bats were surveyed and 15 plants each were randomly assigned to one separately from insects with the observer situated of the following treatments: 1) control umbels approximately 10 m away from the inflorescence. available to both diurnal and nocturnal visitors, 2) Visitation rates of birds were measured by record­ umbels available to only diurnal visitors (umbels ing the number of visits to open flowers on an bagged at sunset and unbagged at sunrise), 3) um­ inflorescence for one hour shortly after dawn, bels available to only nocturnal visitors (umbels during mid-day and approximately one hour bagged at sunrise and unbagged at sunset), and 4) prior to dusk. Bat visitation rates were deter­ umbels bagged, but liberally hand pollinated mined by scanning a clumped group of agaves for daily during stigma receptivity (3-4 days) with approximately one hour after dusk, near mid­ fresh pollen collected from different individuals night, and before dawn. Visitation rates of insects within the population (Peppersauce and Mustang (primarily bees and moths) were determined by sites only). Umbels were covered with nylon net scan sample: the number of insects active on an bags that excluded any animals greater than 1.5 umbel were counted for ten minutes every two mm in size. Umbels were bagged prior to stigma hours during the day (approximately 0500-1900 receptivity (generally after anther dehiscence),

197 and bagging continued until all styles were wilted tended to have all flower stages present during (4-5 days). Umbels of experimental and control the nlajority of time the umbel was blooming with plants from the Parker Mesa, Santa Rita and Pep­ a smaller numbers of flowers open in each stage. persauce populations have been collected thus far, Floral visitors included a diverse range of ani­ and percent fruit set was determined. Data were mals: honeybees (introduced), bumblebees, analyzed for each site by chi-square analysis. carpenter bees, hummingbirds, orioles, hawk­ moths, butterflies, wasps, moths, and a variety of small solitary bees. Bats were not observed at any RESULTS site despite over 15 total hours of periodic obser­ vations. Although visitors varied in composition and numbers between sites, honeybees (Apis mel­ Flower and Pollinator Observations li/era) were the dominant visitors and consumers of pollen and nectar at all sites (Table 1). Bumble­ Agave flowers are protandrous, gradually bees (Bombus sonorus) and carpenter bees changing from a male to female (pistillate) state (Xylocopa cali/ornica arizonensis) were generally over a 5-6 day period. On the first day of flower­ the next most common visitors. Although present ing (pre-dehiscent stage), the tepals open and the at the Peppersauce site, carpenter bees had low filaments and anthers are exerted. Flowers remain visitation rates as they tended to approach and in this condition until the evening of Day 2 (dehis­ then avoid the observed umbels, possibly both­ cent stage) when anthers dehisce. Time of ered by the observer. Small moths and dehiscence differs between taxa; anthers of A. pal­ hawkmoths were the predominate nocturnal visi­ meri open between 2000 and 2200, generally tors, however, diurnal visitor frequency was shortly after sunset, while A. chrysantha anthers greater than that of nocturnal visitors at all sites dehisce later, between 2400 and 0200 of Day 3. (Table 2). Peak visitation occurred at dawn and a Stigmas are tightly closed at dehiscence, although smaller burst of activity took place prior to dusk. styles are beginning to elongate. Agave chrysan­ Both honeybees and bumblebees foraged most ac­ tha styles are exerted 0-15 mm the morning of Day tively in the early morning, first actively 3 (post-dehiscent stage), while styles in A. palmeri gathering pollen, and once the majority of the are exerted 15-35 mm above the tepals. The morn­ day's crop was harvested, nectar was collected. ing of Day 4 (early pistillate stage), the tripartite Carpenter bee activity tended to peak later in the stigmas are usually closed, but are generally morning and continue through the afternoon. slightly moist and open by evening. Thus, flowers These results are similar to those obtained by become receptive approximately 48 hours after' Schaffer et al. (1979). Moths were most active dehiscence. Filaments are beginning to wilt at this shortly after dusk, however hawkmoths were ac­ time and styles are exerted 16-27 mm in A. tive near dawn as well. Some evidence of chrysantha and 25-40 mm in A. palmeri. By the aggression between foragers was observed. Hum­ morning of Day 5 (pistillate stage) stigmas are mingbirds seemed to be bothered by the presence open and sticky, and filaments are wilted by the of bumblebees at the Peppersauce site, and would end of the day. Styles are exerted from 21-30 mm pull away when bees approached. Carpenter bees and 25-48 mm in A. chrysantha and A. palmeri/ were quite aggressive at the Mustang site, often respectively. Tepals have generally wilted by the chasing each other away from umbels. Hawk­ morning of Day 6 (late pistillate stage), and stig­ moths and bumblebees were observed to knock mas may be widely parted and moist to dry and one another off flowers during their interactions slightly wilted. Styles are completely wilted by at dawn and dusk at the Santa Rita site. Day 7. Pollination was a very haphazard event, and Flower stage composition of umbels was only 36 potential pollination events were noted in noted to be different between A. chrysantha and over 30 hours of observation at all sites (bird and A. palmeri. Flowers on A. chrysantha umbels bat observation time excluded). The small size of tended to be predominately in only two stages the majority of visitors, allowed them to "rob" throughout the flowering period of the umbel, al­ nectar by entering flowers above the tepals and though larger umbels might exhibit more flower avoiding the exerted, receptive stigmas. Honey­ stages. For example, an umbel might be composed bees were large exploiters of floral rewards who mostly of buds and pre-dehiscent flowers, pro­ performed little pollination due to their small size gressing the next day to pre-dehiscent and and foraging habits. Honeybees tend to gather dehiscent stages, etc. However, A. palmeri umbels pollen from a single inflorescence (McGregor et al.

198 Table 1.-BebYIen-!ite variltion of maigr floral visitgrs of A. ch!Jl.santha and A. l1.almeri (visitslminlumbel}. A. chrysantha Parker Mesl Peln!erSauce Total min Total min Visitor Visits/min observed Visitor Visits/min observed Honeybee 0.34 480 Honeybee 1.38 690 Bumblebee 0.26 480 Moths 0.25 100 Hummingbird 0.13 360 Wasp 0.08 690 Moths 0.16 60 ' Carpenter bee 0.06 690 Hawkmoth 0.03 60 Bumblebee 0.04 690 Carpenter bee 0.02 480 Hummingbird 0.03 480 Scott's oriole 0.02 360 Housefly 0.02 690 Blk swallowtail 0.01 480 Sm blk bee 0.01 690 Bat 0.0 120 Hornet 0.01 690 Bat 0.0 120

A. palmeri Santa Rill Mustang Total min Total min Visitor Visits/min observed Visitor Visits/min observed Honeybee 2.4 90 Honeybee 1.42 300 Bumblebee 0.92 90 Carpenter bee 0.52 300 Hawkmoth 0.05 10 Wasp 0.32 300 Moths 0.05 10 Sm blk bee 0.31 300 Sm bees 0.05 90 Hummingbird 0.12 240 Bat 0.0 120 Moths 0.18 90 Small green bee 0.13 300 Hawkmoth 0.10 90 Sm bees 0.06 300 Other wasps 0.03 300 Brown wasp 0.02 300 Blkwasp 0.01 300 Bat 0.0 570

Table 2. -Between-site variation of diurnal and nocturnal visitors to A. chrysantha and A. palmeri (visits/min/umbel).

A. chrysantha

Parker Mesa PeRl2ersauce

Total min Total min Visitor Visits/min observed Visitor Visits/min observed

Diurnal 0.65 480 Diurnal 1.58 690 Nocturnal 0.20 60 Nocturnal 0.25 100 Birds 0.15 360 Birds 0.03 480 Bats 0.0 120 Bats 0.0 120

A.pa/merl

Santa Rita Mustang

Total min Total min Visitor Vlslta/mln observed Visitor Visits/min observed

Diurnal 3.46 90 Diurnal 3.09 300 Nocturnal 1.00 60 Nocturnal 0.30 90 Birds Birds 0.21 540 Bats 0.0 120 Bats 0.0 570

199 1959, Alcorn et al. 1961), so that if contact with receptive stigmas occurred, fertilization was not 0.7-r------~------__, likely (agaves are primarily self-incompatible). Larger animals such as hummingbirds and hawk­ o.e moths were observed to hoover and avoid 0.5 touching stigmas unless foraging in the middle of i a moderate to large-sized umbel. Stigma contact 0 4 generally occurred when insects landed awk­ 1• wardly on umbels and touched stigmas, or while I 0.3 foraging on freshly dehiscent anthers with erect filaments, crawled over adjacent receptive stig­ 0.2 mas. Bumblebees and carpenter bees were observed to most frequently come in contact with 0.1 receptive stigmas (Table 3), their intermediate size making it more difficult for them to avoid exerted stigmas while foraging. Day

Figure 1.-Dally nectar production of A. chrysantha and A. palmeri.

Pollen and Nectar Studies steady rate until 0300 when production slowly de­ clined. Agave palmeri nectar production rose Mean daily nectar production of flowers is rapidly from dusk until 2400 when it peaked, then presented for A. chrysantha (Peppersauce site) decreased steadily until dawn. This production and A. palmeri (Mustang site) in figure 1. Nectar curve was similar for all flower stages in both A. production curves were similar, although nectar chry.t;antha and A. palmeri except for pistillate amounts were greater in A. palmeri due to the flowers (evening of Day 5-morning of Day 6) larger size of flowers. Nectar production was ob­ which produced a small amount of nectar from served to decrease at a greater rate in A. palmeri dusk until 2100 with negligible production after­ after Day 3. As flowers moved from a male to wards. female stage, nectar production decreased. Hourly Standing nectar crop production versus total nectar production differed somewhat between hourly production and nectar sugar sugar concen­ taxa (fig. 2). Nectar production in A. chrysantha tration for Peppersauce and Mustang sites are began at dusk and nectar was produced at a fairly prest~nted in Table 4. Standing crop nectar

Table 3.-0bserved stigma contact by flora' vl.ltor. to A. chrysantha and A. palmeri. A. chryuntha fl[lnnMIH fIPPI[IIYCI Stigma Total min Stigma Total min Visitor contacts observed V'.'tor contacts observed Blk Swallowtail 5 480 Bumbleb.. 3 690 Bumblebee 4 480 Honeybee 690 Carpenter bee 2 480 Housefly 690 Wasp 1 480

A.palmerl Sloll Bill Mulling Stigma Total min Stigma Total min Visitor contacts ob.erved VI.'tor contacts observed Hawkmoth 90 Carpenter b.. 11 300 Bumblebee 5 300 Honefbee 2 300 5mb.. 2 300 Blk/Wh ite bee 300

200 amounts, although generally less than total daily 0.3 production, were similar to total daily values. Thus, the majority of nectar produced was avail­ 0.25 able for diurnal visitors at dawn. Variation in nectar production was greater in Days 4 and 5 as 0.2 flowers aged and production decreased. Mean nectar sugar concentrations were similar in both 0.15 taxa, and ranged from 13-21% in A. chrysantha and 13-25% in A. palmeri. 0.1 Visitation rate varied as a function of nectar production (Table 5). Umbels which were pre­ 0.05 dominately pre-dehiscent/ dehiscent and dehiscent/post-dehiscent had the highest visita­ tion rates while pistillate umbels had low 21 24 visitation rates. Hour

Figure 2.-Hourly nectar production of dehlscent to post dehlscent flowers in A. chrysantha and A. palmeri,

Table 4.-Standing nectar crop (ml), nectar sugar percentage and total daily nectar (ml) production of A. chrysantha (Peppersauce site) and A. palmeri (Mustang site). Data are mean values, numbers in parentheses are SE) A. chrysantha Standing~ NectiU Sygl[ % Totll DliI~ Nectar Dusk Dawn Total Day 1 0.093 0.254 0.35 17.6 0.47 (0.05) (0.07) .. (0.09) (1.77) (0.11 ) Day 2 0.104 0.184 0.228 0.247 (0.049) (0.081 ) (0.112) (0.124) Day 3 0.003 0.187 0.191 15.5 0.256 (0.007) (0.065) (0.064) (1.77) (0.124) Day 4 0.0 0.007 0.007 14.0 0.087 (0.022) (0.002) (N = 1) (0·.088) Day 5 0.0 0.0 0.0 0.001 (0.002)

A. palmeri Stlndlng~ ~Ictar Sugar % T2tal DII~ ~ Dusk Dawn Total Day 1 Day 2 0.141 0.390 0.532 17.0 0.623 (0.081) (0.121) (0.123) (4.1) (0.231 ) Day 3 0.061 0.471 0.532 19.22 0.677 (0.034) (0.146) (0.163) (3.04) (0.114) Day 4 0.083 0.282 0.366 15.87 0.341 (0.040) (0.177) (0.191) (3.16) (0.181) Day 5 0.008 0.005 0.013 14.50 0.002 (0.011) (0.016) (0.020) (N = 3) (0.007)

201 Pollination Studies 100 -,------,

90 -f------In preliminary studies at the Parker Mesa site, fruit set of A. chrysantha umbels exposed to only nocturnal pollinators was significantly lower 70 /------

(17.2%) than diurnally pollinated umbels (22.8%) 60 f------(0.001

Peppersauce site was also significantly lower 304------(2.2%) than day pollinated umbels (16%) (O.OOl

(significantly higher than day-pollinated plants, 10 0.001

Table S.-Mean dally nectar production (mO vs. diurnal visitation (visits/min) in A. chrysantha (Peppersauce site) and A. palmeri (Mustang Site). Table 6.-Effect of pollination treatment on fruit set % in A. clJrysantha and A. palmeri. (Data represents mean number A. chrysantha of fruits/number of fruits + number of aborted Flower Stage Nectar Amt Visits/Min fruits/umbel. Numbers in parentheses represent SE) A. chrysantha Pre-dehiscent 0.47 4.7 Parker Mesa . pepper,auce Dehiscent 0.24 3.96 % Fruit Set % Fruit Set Post-Dehiscent 0.25 3.56 Pistillate 0.09 2.34 Night pollinated 17.2 (18.6) 2.2 (3.49) Late pistillate 0.001 0.13 Day pollinated 22.8 (17.4) 15.7 (14.46) Control 24.1 (15) 18.8 (16.62) A. palmerl* Hand Pollinated 51.0 (36.42) Flower Stage Nectar Aim Visits/Min A. palmeri Pre:.cfehiscent/dehis. 0.623 4.5 Santa R.ita Dehiscent 0.623 3.5 % Fruit Set Post-dehiscent 0.677 Pistillate 0.341 1.27 Night pollinated 10.3 (16.24) Late pistillate 0.002 0.75 Day pClllinated 14.3 (18.67) Control 16.6 (14.03)

*Flower stage listed was the predominate stage, although flowers were present in previous and latter stages.

202 DISCUSSION rather primitive method of pollination can be achieved by a variety of animals which mayor may not include bats. The arrangement of floral stages within um­ Results of this study suggest that several dif­ ferences exist between A. chrysantha and A. bels appears to impact pollination as well. Pollination was most frequently observed when palmeri with regard to their reproductive biology. Time of pollen dehiscence, flower stage composi­ insects, attracted to flowers with freshly dehisced tion of umbels and peak nectar production were pollen or large amounts of nectar, would rather consistently different between taxa. When differ­ haphazardly touch adjacent flowers with recep­ ences in floral color and phenology tive stigmas. Consequently, as flowers aged and (yellow-flowered A. chrysantha blooms from late floral rewards decreased, visitation rates de­ May-early August, A. palmeri flowers from late creased and pollination events were less likely. June-early September and flowers are cream-col­ Umbel size and position on the inflorescence may ored with reddish tepal apices) are also taken into also effect fruit set. Umbels located in the middle account, separation at the species level appears of the inflorescence were the largest in size, and appropriate despite the lack of complete repro­ had the highest fruit set. The higher number of ductive isolation. flowers and floral stages at anyone time in large Pollinator observations suggest that diurnal umbels presumably increases pollination success. insects appear to play an important role in polli­ Flowering of individual agaves within a popula­ nation of A. chrysantha and A. palmeri, despite tion is asynchronous, so that umbels positioned several characteristics of chiropterophily. Gregory in the middle of the inflorescence of an early or (1963, 1964) and Waser (1978) have noted that late blooming plant may have a better chance of plants with characteristics of a particular pollina­ receiving pollen from another individual than tion syndrome may often depend on other those umbels on the bottom or top of an inflo­ animals for the majority of pollination. Although rescence. a large number of animals visiting flowers were Diurnal pollinators appear to contribute sig­ "thieves," pollination was predominately nificantly to pollination ~d subsequent fruit set achieved by diurnal insects (particularly native in A. chrysantha and A. palmeri. Control and day bumblebees and carpenter bees) by "accidently" pollinated umbel fruit set percentages were near making contact with receptive stigmas while for­ 20% and are similar to results of natural fruit set aging. The "mess and soil" pattern of ""pollination (Sutherland 1982). Outcrossing, hermaphroditic (Faegri and van der Pijl 1979) appears to be the plants commonly have low frUIt set (Sutherland primary method by which pollen is transferred to and 'Delph 1984), and observed pollination rates stigmas in the populations observed, and this of 20% suggest adequate pollination occurred. The similarity of fruit set in control and day-polli­ nated umbels imply that nocturnal pollinators are not critical for sufficient fruit set. Night pollina­ 90,------% tors contributed little to fruit set (2.2 ) in the Peppersauce population, and approximate re­ ported self pollination fruit set rates (1.580/0) 70 +---.-----.------.day pollination : o control (Sutherland 1982). Although the presence of bats 60 +------may increase fruit set of nocturnally pollinated 1: flowers, their presence does not appear to be vital ! 50 +------~ -----.------i for adequate fruit set to occur. Further studies are s= 240+------needed to deterqrine whether populations polli­ :Ii nated by bats have significantly higher fruit and 30+------·-·--- seed set than populations where bats are not pre­

20 t------sent. If agaves are resource limited as Sutherland (~982) suggests, then mean fruit set in any popula­ 10 hon would not be expected to be significantly higher than 20-25%. Hand pollination was very santa Rita Fruit Set % Santa Rita Fruit Abort effective in increasing fruit set above control and treatJnent percentages, indicating some pollinator Figure 4.-Percent fruit set of A. palmeri as determined by pollination limitation existed. Further studies are required to treatment evaluate the percent seed set per fruit.

203 Data from this study indicates that pollinator Cock),um, E.L. and Y. Petrysan. 1991. The long-nosed bat, populations vary between sites and years. An in­ Leptonycteris: an endangered species in the South­ termediate or facultative pollination syndrome west? Occasional Papers of the Museum of Texas Tech may be more adaptive in species that occur in di­ llniversity142:1-32. verse habitats (A. chrysantha) or have large Dodd, R.J. and Y.B. Linhart. 1994. Reproductive conse­ geographic ranges (A. palmeri), allowing plants to quences of interactions between Yucca glauca (Agavaceae) and Tegeticula yuccasella (Lepidoptera) in utilize a variety of pollinators that may vary both Colorado. AmericanJournal ofBotany81 (7): 815-825. temporally and spatially. Bats often do not arrive Faegri, K. and L. van der Pijl. 1979. The Principles of to known roosts in southeastern Arizona until Pc.llination Ecology. Pergammon Press Ltd., Oxford, mid-August (S. Schmidt, pers. comm.), however, England. A. palmeri in the vicinity begins flowering in late Gentry, H.S. 1967. Putative hybrids in Agave. Jounal of June-early July. The variable, seasonal and some­ Heredity58: 32-36. what unreliable movements of Leptonycteris Gentry, H.S.1982. Agaves of Continental North America. (Cockrum and Petryszyn 1991, pers. comm., V. University of Arizona Press, Tucson, AZ.670pp. Dalton) seem unlikely to support a tight mutualis­ GomE!Z Pompa, A. 1963. El genero Agave. Cact. Suculent. tic system. Recent studies have shown that the Mex.8:3-28. long-accepted example of obligate mutualism be­ Gregory, D.P. 1963. Hawkmoth pollination in the genus tween Yucca and the yucca moth (Tegeticula) Oenothera . Alis05: 357-384. appears to be faculative as well (Dodd and Lin­ Gregory, D.P. 1964. Hawkmoth pollination in the genus hart 1994). Fruit set results of this study suggest Oenothera. Alis05: 385-419. that a more faculative relationship exists with A. Howell, D. 1972. Physiological adaptations in the syn­ palmeri, and the "bat-adapted" traits that A. drome of chiropterophily with emphasis on the bat chrysantha and A. palmeri exhibit may be just as Leptonycteris Lydekker. Ph.D. Thesis. University of advantageous to insects and other animals in hot Arizona. 217 pp. and arid climates where peak activity is near Howell, D.J. 1979. Flock foraging in nectar-feeding bats: advantages to the bats and to thehost plants. American dawn and dusk. Mlturalist114(1): 23-49. Howdl, D.J. and B.s. Roth. 1981. Sexual reproduction in agaves: the benefits of bats; thecost of semelparous advertising. Ecology62(1): 1-7. Johnson,R.A.and D.W. Wichern. 1992. Applied Multivari­ ate Statistics, 3rd ed. Prentice-Hall Inc., Englewood LITERATURE CITED Cliffs, New Jersey. 642 pp. Little, A. 1943. Revisions of status of southwestestern de­ Addicott, J.F. 1985. Competition in mutual systems. Pp. serttreesandshrubs.InL.Benson,Amer.J.Bot.30:235. 217-246 in: Boucher, D.H. (ed.),TheBiologyofMutual­ McGregor,S.E., Alcorn,SM. Curtz, E.B. and G.D. Butler, Jr. isms. Croom Helm, London. 1959. Bee visitors to saguaro flowers. Journal of Eco­ Alcorn, S.M., McGregor, S.E., Butler, G.D., and E.B. Kurtz. nomicEntomology52: 1002-1004. 1961. Pollination of saguaro cactus by doves, nectar Pinkava, D.J. and M.A. Baker. 1985. Chromosome and feeding bats, and honeybees. Science 133: 1594-95. hybridization studies of agaves. Desert Plants 7(2): 93- Arita, H.T. 1991. Spatial segregation in long-nosed bats, 85. Leptonycteris nivalis and Leptonycteris curasoae, in Schaffer, W.M. and M.V. Schaffer. 1977. The reproductive Mexico.JMamm.72(4): 706-714. biology of Agavaceae: I. Pollen and nectar production Baker, R.J. and E.L. Cockrum. 1966. Geographic and eco­ in four Arizona agaves. Southwestern Naturalist22(2): logical range of the long-nosed bat Leptonycteris. J 157-168. Mamm.47: 329-331. Schaffer, W.M. and M.V. Schaffer. 1979. The adaptive sig­ Burd, M. 1994. Bateman's principle and plant reproduc­ nificance of variations in reproductive habit in the tion: the role of pollen limitation in fruit and seed set. Agavaceae II: Pollinator foraging behavior and selec­ Bot. Rev. 60(1): 83-111. tion for increased reproductive expenditure. Ecology Burgess, T.L. 1979. Agave-complex of the Guadalupe 60(5): 1051-1069. Mountains National Park; putative hybridization be­ Schaffer, W.M., Jenson, D.B., Hobbs, D.E., Gurevitch, L tween members of different subgenera. Pp. 79-89 in: Todd, J.R. and M.V. Schaffer. 1979. Competition, forag­ Genoways, H.H. and R.J. Baker (eds.), Biologicallnves­ ing energetics and the cost of sociality in three species of tigtions in the Guadalupe Mountains National Park bees . Ecology60(5): 976-987, Texas. National Park Service Proceedings and Transac­ Sutherland, S.D. 1982. The pollination biology of panicu­ tionsSeriesNo.4, Washington, D.C. late agaves: documenting the importance of male Burgess, T.L. 1985. Agave adaptation to aridity. Desert fitness in plants. Ph. D. dissertation. University of Ari­ Plants7(2): 39-50. zona.53pp.

204 Sutherland, S.D. 1987. Why hermaphroditic plants pro­ Waser, N.M. 1978. Competition for hummingbird polli­ duce many more flowers than fruits: experimental nation and sequential flowering in two Colorado tests with Agave mckelveyana. Evolution. 41(4): 750- wildflowers. Ecology59: 934-944. 759. Weins, D. 1984. Ovule survivorship, broodsize, life his­ Sutherland, S.D. and L.F.Delph.1984. On the importance tory, breeding systems and reproductive success in of male fitness in plants: Patterns of fruit set. Ecology plants. Oecologia64:47-53. 65: 1093-1104. Weins, D., C.L. Calvin, C.A. Wilson, C.I. Davern, D. Frank Udovic, D.1981. Determinants of fruit set in Yucca whip­ and S.R.Seavey.1987.Reproductive success, spontane­ plei: reproductive expenditure vs. pollinator ous embryo abortion, and genetic load in florwering availablity. Oecologia48: 389-399. plants.Oecologia71:501-509.

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