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Pollination Ecology of Agave Macroacantha (Agavaceae) in a Mexican Tropical Desert.I

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Pollination Ecology of Agave Macroacantha (Agavaceae) in a Mexican Tropical Desert.I Copyright Notice This electronic reprint is provided by the author(s) to be consulted by fellow scientists. It is not to be used for any purpose other than private study, scholarship, or research. Further reproduction or distribution of this reprint is restricted by copyright laws. If in doubt about fair use of reprints for research purposes, the user should review the copyright notice contained in the original journal from which this electronic reprint was made. American Journal of Botany 87(7): 1004±1010. 2000. POLLINATION ECOLOGY OF AGAVE MACROACANTHA (AGAVACEAE) IN A MEXICAN TROPICAL DESERT.I. FLORAL BIOLOGY AND POLLINATION MECHANISMS1 SANTIAGO ARIZAGA,2 EXEQUIEL EZCURRA,3 EDWARD PETERS,2 FERNANDO RAMIÂREZ DE ARELLANO,2 AND ERNESTO VEGA2 2Instituto de EcologõÂa, Universidad Nacional AutoÂnoma de MeÂxico, Apartado Postal 27±3 (Xangari), 58190±Morelia, MichoacaÂn, Mexico; and 3Biodiversity Research Center of the Californias, San Diego Natural History Museum, P.O. Box 1390, San Diego, California 92112 USA In a study of sexual reproduction in long-lived semelparous plants, we observed Agave macroacantha in the tropical desert of TehuacaÂn-CuicatlaÂn, Mexico, describing duration of ¯owering, ¯ower phenology, and nectar production patterns. We also performed two manipulative experiments evaluating (a) the seed production ef®ciency of different crossing systems (sel®ng, cross-pollination, apomixis, and control), and (b) the effect of different pollinators (diurnal exposure to pollinators, nocturnal exposure, exclusion, and control) on the seeds produced. Flowering occurred from early May to late July and had a mean duration of 29 days in the individual rosettes. The ¯owers were protandrous; anthesis occurred in the afternoon of the third day after ¯oral opening, and the pistils matured in the afternoon of the ®fth day. The stigmas remained receptive from dusk to the following morning. Pollination was mostly allogamous. Nectar was produced principally during the night, from the ®rst stages of ¯oral aperture until the stigmas wilted and ¯owering ceased. The ¯owers were visited during the day by hymenoptera, butter¯ies, and hummingbirds and during the night by bats and moths. Only the nocturnal visitors, however, were successful pollinators. Agave macroacantha is extremely dependent on nocturnal pollinators for its repro- ductive success. Key words: Agave macroacantha; Agavaceae; nectar; nectar-feeding bats; pollination biology; rosette plants; tropical deserts. Species within the genus Agave are monocarpic, i.e., by random environmental events, which can reduce the the individual rosettes have only one reproductive event, ®tness of the individual rosette to zero. In a previous which leads to their death (GoÂmez-Pompa, 1963; Gentry, paper (Arizaga and Ezcurra, 1995) we showed how bul- 1982). When ¯owering starts, agaves develop a large ter- bils (i.e., small rosettes forming vegetatively on the mer- minal in¯orescence or ¯owering stalk (known botanically istems of the scape) are produced when pollinators fail as a ``scape,'' and called quiote in Mexico), as a result to arrive, and thus help to recover the individual ramet of the rapid elongation of the apical meristem after years from a demographic collapse by vegetatively propagating of vegetative growth of the basal rosette. The ¯owers the genet. The aim of this paper is to describe the polli- produce abundant nectar with which they attract their nat- nation mechanisms and to characterize the crossing sys- ural pollinators, which are hummingbirds, bats, or in- tems of Agave macroacantha Zucc. in a tropical desert sects, according to the different Agave species (Gentry, in southern Mexico. 1972, 1982; Schaffer and Schaffer, 1977; Freeman and Reid, 1985; MartõÂnez del RõÂo and Eguiarte, 1987; Eguiar- MATERIALS AND METHODS te and BuÂrquez, 1987; Slauson, 1994). The ¯oral biology of agaves is of interest from the Study areaÐOur ®eld observations for the studies of ¯oral biology point of view of ecological theory, as the rosettes are both and pollination mechanisms were done between May and September long lived and semelparous, and it has received substan- 1994 at the ®eld laboratory of UNAM's Institute of Ecology, located in tial attention during the last decades (e.g., Schaffer and ZapotitlaÂn Salinas (188209 N, 978289 W), 30 km south of the city of Schaffer, 1977; Howell and Hart, 1980; Howell and Roth, TehuacaÂn. Mean annual precipitation in the study site is ;400 mm 1981; Eguiate, 1983; Freeman and Reid, 1985; Eguiate (GarcõÂa, 1982) and the dominant vegetation type is a dry xerophytic and BuÂrquez, 1987; Slauson, 1994). One of the main de- scrub (Rzedowski, 1978) dominated by Neobuxbaumia tetetzo, a giant mographic risks in the life history of long-lived semel- columnar cactus (Zavala-Hurtado, 1982). The rainy season occurs in parous plants is the threat of reproductive failure induced summer, starting in late May and ending in late September. The site has a patchy population of Agave macroacantha (Agava- 1 Manuscript received 30 November 1998; revision accepted 30 Sep- ceae), a species that is endemic to the TehuacaÂn-CuicatlaÂn Valley (Gen- tember 1999. try, 1982). This species belongs to the subgenus Agave (Gentry, 1982), The authors thank Dr. Luis Eguiarte for discussion and review the a group characterized by open paniculate in¯orescences, with ¯owers manuscript; Mr. Everardo Castillo for ®eld assistance in ZapotitlaÂn Sa- in large umbellate clusters on long lateral peduncles. (The other sub- linas; the National Council for Science and Technology (CONACyT), the Support Program for Graduate Studies (PADEP) of UNAM, and the genus, Littaea, presents narrow spicate in¯orescences with ¯owers ar- U.S. Fish and Wildlife Service for ®nancial support. This research is ranged in clusters along the elongated scape). Agave macroacantha pro- part of the ®rst author's doctoral research at the Facultad de Ciencias, duces ¯owering stalks in April and May, and by September±November UNAM. the capsules are ripe and start to open. Although rarely consumed by 1004 July 2000] ARIZAGA ET AL.ÐFLORAL BIOLOGY OF AGAVE MACROACANTHA 1005 humans, the early ¯owering stalks suffer intense damage by foraging TABLE 1. Description and mean duration of the phenological stages of goats (Arizaga and Ezcurra, 1995). ¯ower development in Agave macroacantha (see also Fig. 1). The Due to the low density of the species, in March 1994, 16 budding ®rst number of each phenological stage de®nes the development rosettes were transplanted to the experimental site from other areas lo- phase of the protandrous ¯owers: (1) immature ¯owers, (2) ¯owers in male phase, (3) ¯owers in female phase, and (4) fruit develop- cated within a radius of 5 km that showed a similar vegetation. We used ment. in total 32 ¯owering individuals (16 transplanted and 16 native to the site), which were fenced to protect them from large herbivores. When Pheno- experimental treatments were applied to individual plants, the trans- logical Mean duration stage Description (hours 6 SE) planted individuals were randomized among treatments. The individuals used in the experiments were also used for observational procedures 1 Beginning of dehiscence of the corol- 9: 48 (61: 44) that did not require experimental manipulation. la. 2.1 Tepals become separated, stamens 19: 53 (64: 36) start to elongate. Floral biologyÐDuration of ¯oweringÐOn a random subset of nine 2.2 Anthers appear above the tepals. 19: 50 (66: 47) ¯owering individuals we monitored the time spent in each ¯owering 2.3 Stamen ®laments appear showing a 8: 58 (60: 49) stage, both at the level of the ¯owering ``branches'' (i.e., umbellate marked bent below the anthers. clusters at the end of the long lateral peduncles) and of the whole in- 2.4 Filaments elongate completely, style 19: 06 (60: 49) ¯orescence. For the branches, we registered the duration of the different appears above the tepals. ¯owering phases in the ®rst eight lateral umbellate clusters. In each 2.5 Anthers become dehiscent and release 10: 54 (60: 59) one, we considered that ¯owering started when the suture lines of at pollen. least one ¯oral bud split and concluded when the style of the last ¯ower 2.6 Anthers lose functionality, style elon- 19: 03 (60: 50) gates above the stamens. wilted. Flowers were classi®ed into three categories: (a) developing, 3.1 Style reaches maximum elongation, 26: 42 (60: 56) from ¯oral aperture to pollen release (anthesis), (b) staminate, from stigmal lobe spreading begins. pollen release to stamen decay, which coincides with dehiscence of the 3.2 Stigma fully open with maximum ex- 10: 05 (61: 36) stigma, and (c) pistilate, from stigmal lobes spreading to style wilting. udates. Total ¯owering duration in a single branch was computed from the 3.3 Style begins to wilt, stigma dries up. 4: 40 (61: 16) aperture of the ®rst ¯ower to the wilting of the stigma of the last ¯ower. 4 If ¯ower was fertilized, fruiting be- Ð Individual branches were observed twice each day, at 0700 and 1800. gins. In each observation, we registered the developmental stage of each Total Flowering time, from stage 1 to stage 147: 00 (68: 51) ¯ower. With these data, we could calculate for each branch the mean 3.3. time a ¯ower spent in each ¯owering stage. Once ¯owering in the ®rst eight branches concluded we continued monitoring the plants until ¯ow- ering in the last lateral branch concluded. Observations were made daily ¯owers with their stigmas covered by the plastic tubes throughout the at noon. In each observation we registered for the whole individual the ¯owering period. (4) Control. A fourth group of ¯owers was marked, presence of active ¯owers, the cumulative number of ¯owering branches but their stigmas were not covered. Pollination in these ¯owers was left produced, and the cumulative number of fruit capsules formed. to the natural agents in the ®eld. The plastic tubes allowed ¯owers of the four treatments to coexist in a ¯owering branch.
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