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Pollination Biology of Two Columnar Cacti (Neobuxbaumia Mezcalaensis and Neobuxbaumia Macrocephala) in the Tehuacan Valley, Central Mexico1

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Pollination Biology of Two Columnar Cacti (Neobuxbaumia Mezcalaensis and Neobuxbaumia Macrocephala) in the Tehuacan Valley, Central Mexico1 American Journal of Botany 84(4): 452±455. 1997. POLLINATION BIOLOGY OF TWO COLUMNAR CACTI (NEOBUXBAUMIA MEZCALAENSIS AND NEOBUXBAUMIA MACROCEPHALA) IN THE TEHUACAN VALLEY, CENTRAL MEXICO1 ALFONSO VALIENTE-BANUET,2, 4 ALBERTO ROJAS-MARTIÂNEZ,2 MARIÂADELCORO ARIZMENDI,2 AND PATRICIA DAÂ VILA3 2Instituto de EcologõÂa, UNAM, A.P. 70±275, MeÂxico 04510 D.F.; and 3Instituto de BiologõÂa, UNAM, A.P. 70±233, MeÂxico 04510 D.F. We document the pollination biology and mating systems of Neobuxbaumia mezcalaensis and Neobuxbaumia macroce- phala, two Mexican giant columnar cacti. These two species form mixed forests in the western Tehuacan Valley, Mexico. The ¯owers of both N. mezcalaensis and N. macrocephala exhibit nocturnal anthesis, are self-incompatible, and are pollinated primarily by three species of nectar-feeding bats (Choeronycteris mexicana, Leptonycteris curasoae, and Leptonycteris nivalis). Neobuxbaumia mezcalaensis is androdioecious, a breeding system that appears to be uncommon among Cactaceae. Neobuxbaumia macrocephala is hermaphroditic. We hypothesize that columnar cacti show a geographical dichotomy in ¯oral biology specialization that probably can be related to predictability in pollinator abundance. Key words: androdioecy; Cactaceae; columnar cacti; mating systems; nectar-feeding bats; pollination biology; Neobux- baumia mezcalaensis; Neobuxbaumia macrocephala; Tehuacan Valley. Columnar cacti (Tribe Pachycereeae) are dominant ical deserts, in contrast, probably face more predictable plants in arid and semiarid zones in central Mexico where pollinator activity and therefore can depend on bat pol- they sometimes form succulent forests with densities as lination (Sosa and Soriano, 1992; Valiente-Banuet et al., high as 1200 individuals/ha (Valiente-Banuet and Ezcur- 1996). ra, 1991; Valiente-Banuet et al., 1996). Many columnar In south-central Mexico the giant columnar cacti Neo- cacti depend on animals for pollination (Grant and Grant, buxbaumia mezcalaensis (Bravo) Backeberg and Neo- 1979). Valiente-Banuet et al. (1996) showed that 54 out buxbaumia macrocephala (Weber) Dawson form mixed of 70 species of Mexican columnar cacti (60%) are bat forests in the western part of the Tehuacan Valley. Both pollinated (as de®ned by Faegri and van der Pijl, 1979) species are endemic to the TehuacaÂn Valley and the Bal- and have strong large white ¯owers with nocturnal an- sas River Basin. Although the dominance and endemism thesis, large nectar quantities, wide corolla entrance, and of N. mezcalaensis and N. macrocephala have been well strong scent. However, several studies have shown that documented, their ¯oral biology has not been studied. some columnar cacti, specially those inhabiting extra- The purpose of this paper is to document the ¯oral tropical deserts are also effectively pollinated by diurnal biology and mating systems of these two species, as a animals, such as birds and bees (Alcorn et al., 1959; project in which the geographical dichotomy of ¯oral bi- McGregor et al., 1959, 1962; Alcorn, McGregor, and Olin ology of columnar cacti is being tested by studying plants 1961, 1962; Fleming, 1993). The results of Sosa and So- growing in a tropical desert. riano (1992) and Valiente-Banuet et al. (1996) indicate that in the tropics, columnar cacti depend primarily on METHODS bats for pollination. We hypothesize that columnar cacti show a geographical dichotomy in specialization. Cacti Study siteÐResearch was conducted in the semiarid valley of Za- inhabiting temperate extratropical deserts probably face potitlaÂn de las Salinas (188 209 N, 978 289 W), a local basin of the unpredictable pollinator activity and hence tend to have TehuacaÂn Valley in the state of Puebla, Mexico. This region owes its nonspecialized ¯oral biology and a coterie of pollinators aridity to the rain shadow produced by the Sierra Madre Oriental that includes both bats and diurnal pollinators (Fleming, (Smith, 1965), and receives an average annual rainfall of 380 mm. An- nual mean temperature averages 218C with very rare frosts (GarcõÂa, 1993; Valiente-Banuet et al., 1996). Cacti inhabiting trop- 1973). The main vegetation type is arid tropical scrub (Rzedowski, 1978) in which giant columnar cacti constitute the most important phys- 1 Manuscript received 25 April 1996; revision accepted 3 October iognomic elements. The study was conducted during April and May 1996. 1994 and from March to May of 1995. 4 Author for correspondence. The authors thank Everardo Castillo and Carolina Chavez for ®eld Plant abundance and ¯owering intensityÐto determine the density assistance; Dr. Carlos MartõÂnez del RõÂo and Dr. Theodore Fleming for valuable suggestions made to the manuscript. Financial support was of N. mezcalaensis and N. macrocephala we conducted a 100 by 10 m provided by the DireccioÂn General de Asuntos del Personal AcadeÂmico transect during the ¯owering peak of columnar cacti in the valley (Val- (DGAPA IN 208195), and CONABIO project G017. The authors want iente-Banuet et al., 1996). For each individual cactus within this transect to dedicate this paper to the memory of Maricela Sosa and JesuÂs Ra- we recorded height and the number of ¯owers and fruits. We de®ned mõÂrez. ¯owering intensity as the frequency of potentially reproductive individ- 452 April 1997] VALIENTE-BANUET ET AL.ÐPOLLINATION BIOLOGY OF TWO COLUMNAR CACTI 453 uals ($ 2 m as stated by Valiente-Banuet and Ezcurra, 1991) with ¯ow- (each plant sample was obtained by a mixture of pollen obtained from ers. ten individual plants). Bat feces were also collected in order to obtain seeds and pollen. Floral biologyÐto describe ¯oral biology 20 hermaphroditic ¯owers were selected at random from a total of 30 individual plants per species. RESULTS Only one ¯ower per plant was measured (total length, i.e., length from the petals base to the nectaries, and width, i.e., corolla anthesis). In Neobuxbaumia mezcalaensis is an unbranched colum- order to infer ¯ower receptivity, we marked 30 buds in 30 individual nar cactus that attains a height of 14 m. It is the dominant plants. Every 2 h from ¯ower opening to ¯ower closing, we monitored species in the study area and occurs at densities of 1680 anther and stigma turgidity. adult plants/ha. Flowering occurs from April to late of The determination of sex of individual plants was assessed in 1994 June, just before the beginning of the rainy season and and in 1995 for 30 individual marked plants. Fruit production was also fruiting from May to June (Rojas-MartõÂnez, 1996). Re- determined for each year for the 30 marked plants. Sex ratio was cal- productive maturation seems to occur when plants are ø culated with data derived from transect counts described above. Pollen 2 m tall (none of the censused plants below this height viability in male and hermaphrodite ¯owers was tested in 1996 by ob- produced fruits). serving pollen tube growth in culture media, in a sample of 100 ran- The second species, Neobuxbaumia macrocephala, is domly chosen grains per sex, obtained from ®ve different ¯owers. Nectar volume was measured in ten ¯owers per species randomly a branched columnar cactus that attains a height of 10 m chosen among 30 individuals. Flowers were bagged before anthesis with and grows as a codominant with N. mezcalaensis. It oc- mosquito netting, and nectar accumulated during night and day was curs at densities of 200 individuals/ha. Flowering occurs measured with microcapillary tubes. from March to August and fruiting from April to August (Rojas-MartõÂnez, 1996). Breeding plants are always .2 Breeding systemÐto determine the breeding system and differential m tall (none of the censused plants below this height effectiveness of visitors in each species, 60 ¯ower buds from a total of produced fruits). 60 plants were marked and bagged with mosquito netting. Ten ¯owers Flowering peak occurred simultaneously in N. mezca- were assigned to each of the following treatments. (1) Nonmanipulated laensis and N. macrocephala in April 1994 (Rojas-Mar- self-pollination: ¯ower buds were bagged and monitored until they tõÂnez, 1996) when 50% of all the potential reproductive aborted or set fruit. (2) Nocturnal pollination: ¯ower buds were bagged individuals were ¯owering. before opening; when ¯owers opened, they were exposed to nocturnal ¯oral visitors by the removal of the bag from 2000 to 0500 (1 h before Floral biologyÐNeobuxbaumia mezcalaensis has an sunrise). At this time ¯owers were rebagged and monitored until abor- androdioecious breeding system with both male and her- tion or fruit production. (3) Diurnal pollination: ¯ower buds were maphrodite plants. Male ¯owers have a completely re- bagged; ¯owers were exposed to diurnal visitors by removing the bag duced gynoecium without mature ovules and do not pro- at 0600 until they closed at ø 1030. At this time ¯owers were rebagged duce fruits (N 10 males with an average of 30 ¯owers and monitored until abortion or fruit production. (4) Cross-pollination: 5 ¯ower buds were bagged; when ¯owers opened they were hand-polli- produced per plant, range 21±36). Sex expression re- nated, using fresh pollen obtained from another plant. (5) Self-pollina- mained constant for all the hermaphroditic individuals tion: ¯ower buds were bagged; when ¯owers opened they were hand- marked in 1994 and examined in 1995 (N5 30), while pollinated, using pollen obtained from the same ¯ower. (6) Unmani- only 50% of male individuals (N510) produced ¯owers pulated open-pollinated ¯owers: ¯owers were only marked and left until in 1995. This 50% of the male plants maintained their abortion or fruit production. male sex constant. Sex ratio in the population is 6.5 her- Due to the lower availability of ¯owers in N. macrocephala, only maphrodites/male. All pollen grains produced by both self-incompatibility was tested (treatments 1, 4, 5, and 6). hermaphroditic and male ¯owers produced pollen tubes. In the case of N. mezcalaensis hermaphroditic ¯owers were used in Thus, we concluded that the two types of ¯owers were all treatments, except for the cross-pollination treatment where pollen functionally viable. from male ¯owers was used.
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