Plant Syst Evol (2011) 293:147–159 DOI 10.1007/s00606-011-0432-4 ORIGINAL ARTICLE Pollen partitioning of three species of Convolvulaceae among oligolectic bees in the Caatinga of Brazil Raquel Andre´a Pick • Clemens Schlindwein Received: 29 October 2009 / Accepted: 20 February 2011 / Published online: 20 March 2011 Ó Springer-Verlag 2011 Abstract During the rainy season many species of Keywords Ipomoea Á Emphorini Á Merremia Á Convolvulaceae bloom simultaneously in the Caatinga of Oligolectic bees Á Resource partitioning Á Pollen flow northeast Brazil. In a Caatinga nature reserve we studied pollination and breeding systems of three sympatric species of Convolvulaceae, Ipomoea bahiensis, I. nil, and Merre- Introduction mia aegyptia, focusing on pollen partitioning among flower visitors and pollen flow. The study showed that only oli- When flowers of different species with similar floral traits golectic bees collected pollen and that these species had occur and set flower at the same place and time, they may different preferences among the three species of Convol- attract the same pollinators and compete for their polli- vulaceae: pollen of Ipomoea bahiensis, the only self- nation service (Armbruster and Herzig 1984; Caruso incompatible species, was collected mainly by Melitoma 1999; Levin and Anderson 1970). In bee-pollinated segmentaria, M. osmioides, and Melitomella murihirta; flowers, the relationships of plant species to bees are often pollen of I. nil by Lithurgus huberi; and that of Merremia based on pollen, the main food resource for bee larvae. In aegyptia by Ancyloscelis apiformis and an undescribed some cases such pollen-driven associations involve species of this genus. Introduced honey bees visited only mainly oligolectic bee species. These are pollen special- flowers of Merremia aegyptia, where they were extraor- ists which permanently restrict their pollen-host plants to dinarily frequent flower visitors. However, they discarded closely related taxa of the same family (Robertson 1925; the pollen grains, which led to almost 50% pollen loss. No Westrich 1989). Pollen specializations range from very polylectic bee species compete for pollen with the oligo- rare associations of a bee species to only one plant spe- lectic species. Partitioning of pollen diminishes competi- cies (monolectic bee species) up to multiple species in tion for floral resources in this specialized plant–pollinator several genera of the same plant family (broadly oligo- association. lectic bee species) (Cane and Sipes 2006; Robertson 1925). An example of an association between several oligo- lectic bee species with several plant species within one R. A. Pick family is found in the Convolvulaceae, a large family Programa de Po´s-Graduac¸a˜o em Cieˆncias Biolo´gicas (Zoologia), (about 2,000 species) of vines, herbs, shrubs, and occa- Universidade Federal da Paraı´ba—UFPB, sionally trees, occurring mainly in tropical regions (Souza Joa˜o Pessoa, PB 58059-900, Brazil and Lorenzi 2005). The huge genus Ipomoea is estimated e-mail: [email protected] to comprise a total of 600–700 species worldwide and up to C. Schlindwein (&) 500 species in the New World (Austin and Hua´man 1996). Departamento de Botaˆnica, Laborato´rio Plebeia—Ecologia de Other than a few sphingophilous and ornithophilous Abelhas e da Polinizac¸a˜o, Universidade Federal de Pernambuco, species, the genus shows almost exclusively melittophilous Av. Prof. Moraes Rego, s/n, Cidade Universita´ria, Recife, PE 50670-901, Brazil flowers. Numerous oligolectic species, especially of the e-mail: [email protected] Neotropical tribe Emphorini (Apidae), were shown to be 123 148 R. A. Pick, C. Schlindwein the main flower visitors of Ipomoea species. These are Morphology and flower biology medium-sized ground-nesting solitary bees of the genera Melitoma, Ancyloscelis, and Ptilothrix (Alves-dos-Santos At the nature reserve, 17 species of Convolvulaceae occur, 1999; Austin 1978; Ducke 1908, 1910; Kiill and Ranga belonging to the genera Jacquemontia (2), Cuscuta (1), 2000a, b; Linsley and MacSwain 1957; Linsley et al. 1980; Evolvulus (3), Ipomoea (9), Merremia (1), and Operculina Maimoni-Rodella and Rodella 1992; Maiomani-Rodella (1) (R. Teixeira, unpublished data). In this study, we et al. 1982; Michener et al. 1994; Pinheiro and Schlindw- selected the three most abundant species of Convolvula- ein 1998; Schlindwein 1998). ceae at the study site, all climbers: Ipomoea bahiensis, In the Caatinga, a widespread tropical dry forest in endemic to eastern Brazil, and very common in northeast northeastern Brazil which is characterized by a severe Brazil and Minas Gerais; I. nil, with a pantropical distri- annual drought, Convolvulaceae is, with a total of 103 bution; and Merremia aegyptia, which occurs from south- species, including 21 endemic species, the second most ern Mexico to northern Argentina (Sima˜o-Bianchini 2002). species-rich family (Giulietti et al. 2006; Sima˜o-Bianchini The species show a cornucopia flowering pattern (Gentry 2002) and a characteristic element of flowering Caatinga. 1974), and produce numerous flowers per day and plant The species, however, set flower only during the short during the rainy season. rainy season. In general, several species of the family For each species, we collected 15 flowers from different flower during the same period and time of day at a given plants to describe floral morphology and measure the place in Caatinga. The seasonal pattern of flowering of length of the nectar chamber (from the base of the nectary the Caatinga plants is accompanied by the seasonal disk to the insertion point of the filaments to the flower activity of most bee species, many occurring only during tube), stamens, styles, flower tube, floral diameter, and the rainy season (Aguiar and Martins 1997; Aguiar and diameter of flower tube. A digital calliper was used for Zanella 2005; Zanella and Martins 2003). This might measuring. Time of flower opening, stigmatic receptivity, increase competition for floral resources of flower-visiting anther dehiscence, and duration of flower longevity were bees and lead to resource partitioning among sympatric determined in 30 previously bagged and marked flowers. species. Stigma receptivity was determined following Kearns and In a Caatinga nature reserve of Rio Grande do Norte, Inouye (1993). northeast Brazil, we studied the pollination of three We made pollen reference slides of the Convolvulaceae co-occurring melittophilous species of Convolvulaceae, species and measured the diameter of 300 grains per spe- Ipomoea bahiensis Willd. ex Roem. & Schult., I. nil (L.) cies (including spine length) under a light microscope Roth, and Merremia aegyptia (L.) Urban and asked: How (4009 magnification). The total number of pollen grains are plant–pollinator associations characterized? Which per flower was determined in 10 flowers of different plant flower visitors are effective pollinators? How is pollen individuals per species. The anthers were opened on a Petri partitioned among the bee species? dish, and the pollen grains were stained with basic fuchsin and counted under a stereo microscope (Wild) with a manual counter. Ovules from 20 flowers were counted, and Materials and methods the pollen-to-ovule ratio was determined. To determine pollen viability, grains from ten flowers of Study area different plant individuals per species were removed from the anthers, fixed with FAA (formaldehyde 38% 5 parts— The study was conducted at the Estac¸a˜o Ecolo´gica de Se- glacial acetic acid 5 parts—ethanol 70% 90 parts), and rido´ nature reserve (ESEC-Serido´/IBAMA) situated in the transferred to microscope slides containing carmine acetate municipality of Serra Negra do Norte in the State of Rio (1.2%). Three hundred grains were counted per sample, Grande do Norte, Brazil (06°350–06°400S and 37°200– distinguishing between stained (viable) and unstained 37°390W) at altitude of approximately 170 m. Climate is (nonviable) pollen grains (Kearns and Inouye 1993). tropical hot (mean annual temperature 28°C) with a rainy Plant vouchers are housed at the Herbarium UFP Ger- season from January to June (mean annual rainfall aldo Mariz at the Federal University of Pernambuco— 497 mm). In rainy years, annual precipitation exceeds UFPE, Recife. 1,000 mm and in dry years remains below 300 mm (Ibama 1989; Barcellos and Paupitz 1992). The reserve covers Breeding system 1,166.38 ha of arboreal Caatinga vegetation (Duque 1973). Trees and shrubs maintain their leaves only during the To determine the breeding system of Ipomoea bahiensis, rainy season, and the herbaceous layer is dominated by I. nil, and Merremia aegyptia we conducted a controlled therophytes. pollination experiment (spontaneous self-pollination, hand 123 Pollen partitioning of three species of Convolvulaceae 149 self-pollination, hand cross-pollination) in 30 previously Pollen flow bagged flowers of different plant individuals per species and treatment. The hand cross-pollinated flowers were In 10 flowers per species of different individuals, we quan- emasculated before anthesis, and the flowers were polli- tified the pollen grains remaining in the flower at the end of nated with pollen from donors at least 300 m distant from anthesis, differentiating the number of grains adhering to the focal plants, using pollen grains from three anthers of anthers and petals. Moreover, we counted the number of different plant individuals. Another 40 control flowers per conspecific pollen grains deposited on the stigma surface. species were marked and kept open, accessible