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Pollination Biology in a Tropical High-Altitude Grassland in Brazil: Interactions at the Community Level Author(S): Leandro Frei

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Pollination Biology in a Tropical High-Altitude Grassland in Brazil: Interactions at the Community Level Author(S): Leandro Frei Pollination Biology in a Tropical High-Altitude Grassland in Brazil: Interactions at the Community Level Author(s): Leandro Freitas and Marlies Sazima Source: Annals of the Missouri Botanical Garden, Vol. 93, No. 3 (Oct., 2006), pp. 465-516 Published by: Missouri Botanical Garden Press Stable URL: http://www.jstor.org/stable/40035488 Accessed: 20-08-2014 17:23 UTC Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Missouri Botanical Garden Press is collaborating with JSTOR to digitize, preserve and extend access to Annals of the Missouri Botanical Garden. http://www.jstor.org This content downloaded from 143.106.1.143 on Wed, 20 Aug 2014 17:23:24 UTC All use subject to JSTOR Terms and Conditions POLLINATIONBIOLOGY IN A Leandro Freitas3 and Marlies Sazima4 TROPICAL HIGH-ALTITUDE GRASSLAND IN BRAZIL: INTERACTIONSAT THE COMMUNITYLEVEL1-2 Abstract Surveysof local assemblagesof plants and their pollinatorsare amongthe most useful ways to evaluate specializationin pollinationand to discuss the patternsof plant-pollinatorinteractions among ecosystems. The high-altitudegrasslands from southeasternBrazil constitutediminutive island-like formationssurrounded by montanerainforests. We registeredthe floral traits of 124 species from the Serra da Bocaina grasslands(about 60% of the animal-pollinatedspecies of this flora), and determinedthe pollinatorsof 106 of them. Asteraceae(40 species) and Melastomataceae(10 species) were prominent,while most families were representedby few species. The predominantfloral traits were: dish or short-tubularshape; nectar as a reward;and greenishor violaceouscolors. Pollinatorswere divided into eight functionalgroups (small bees, syrphids,other dipterans, etc.) and small bees, wasps, and large bees were the most importantpollinators. Butterflies, beetles, and hummingbirdswere poorlyrepresented, and no bats, hawkmoths,or odor-collectingbees were detected. Plants were grouped in nine pollinationsystems, amongwhich nectar-flowerspollinated by bees (28%), by wasps or wasps and flies (21%), or by several insect groups (19%) were the most representative.With regardto the degree of specialization,plant species were classified according to their number of pollinator groups. About 33% of the species were monophilousand 30% were oligophilous(i.e., pollinated by one or two functionalgroups, respectively).The remainingspecies were either polyphilous (17%)or holophilous(19%), a highly generalistsystem in which at least three groupsact as indistinctpollinators. The general trends of the floral traits and plant-pollinatorinteractions at the Bocaina grasslands resemble those of biogeographic- connected ecosystems, such as the Venezuelan arbustal, and the Braziliancampo rupestreand cerrado.However, in the Bocainagrasslands, the mean numberof pollinatortypes per plant was 2.09, one of the highest values obtainedfor worldwide floras.The originof the high-altitudegrasslands is linked to episodes of expansionand retractiondue to glacial events. Such a situationmay have favoredspecies able to quickly occupy new habitats,including those that do not depend on a few highly specialized pollinators. The prevalence of Asteraceae may also be linked to more generalized pollination systems. Alternatively,some floraltraits, such as spontaneousself-pollination and long-livedflowers, may be advantageousfor species with more specialized systems in these grasslandswith harsh climatic conditionsand low rates of pollinatorvisitation. Key words: Asteraceae,bees, biogeography,floral biology, generalization,pollination ecology, specialization,syndrome, wasps. 1 This paper is part of the first author'sdoctoral dissertation submitted to the Programade Pos-Graduacaoem Biologia Vegetal,Universidade Estadual de Campinas.We wouldlike to thankI. Alves-dos-Santos,A. A. A. Barbosa,P. E. Berry,D. R. Campbell,P. Feinsinger,R. A. Figueiredo,J. Semir,and S. Vogel for their commentson the early versionsof this manuscript; R. Goldenbergand two anonymousreviewers for their carefulrevision of the manuscript;A. Francoisfor the English revision; I. F. Bressan,E. Gross,R. Ramos,A. L. Ravetta,and I. San Martin-Gajardofor field and laboratoryassistance; A. AmaralJr., M. C. E. Amaral,N. M. Bacigalupo,V. Bittrich, M. Bovini, E. Cabral,L. CapellariJr., T. B. Cavalcanti,A. Chautems,N. Chukr,I. Cordeiro,I. P. Correa,J. H. A. Dutilh, G. L. Esteves, R. L. Esteves, A. D. Faria, M. A. Farinaccio,A. Fillietaz, A. Flores, M. Groppo,A. Guglieri, P. J. Guimaraes,R. M. Harley, N. Hind, S. L. Jung-Mendacoli,M. L. Kawasaki,L. S. Kinoshita,H. M. Longhi-Wagner,M. C. H. Mamede,M. C. M. Marques,A. B. Martins,V. F. Miranda,R. Monteiro,M. D. Moraes,J. N. Nakajima,R. C. Oliveira,E. R. Pansarin,J. R. Pirani,M. F. Salimena,P. T. Sano, J. Semir, G. J. Shepherd,R. Simao-Bianchini,A. 0. SimSes,R. B. Singer,J. P. Souza,V. C. Souza,J. R. Stehmann,J. Tamashiro,A. M. G. Tozzi,A. 0. S. Vieira, F. A. Vitta, M. G. L. Wanderley,K. Yamamotoand C. S. Zickel for plant identifications;I. Alves dos Santos,S. T. P. Amarante,K. S. Brown,J. M. F. de Camargo,S. A. Casari,B. W. Coelho,A. V. L. Freitas,E. Giannotti,A. X. Linhares,U. R. Martins,G. A. R. Melo, L. C. Passos, S. R. M. Pedro, I. Sazima, C. Schlindwein,0. T. Silveira, and D. Urbanfor animal identifications;J. B. Allen and R. C. Forzzafor the nomenclaturalverification of plant taxa; and IBAM A for allowingus to workin the PARNA Serrada Bocaina (throughM. A. B. Rondon).CNPq, CAPES,and FAEP-UNICAMPprovided financial support. 2 The editors of the Annals thank Sophia Balcombfor her editorialcontribution to this article. 3JardimBotanico do Rio de Janeiro,Rua Pacheco Leao 915, 22460-030, Rio de Janeiro-RJ,Brasil; [email protected]. 4 Departamentode Botanica, Caixa Postal 6109, UniversidadeEstadual de Campinas,13083-970, Campinas-SP,Brasil; [email protected]. Ann. Missouri Bot. Gard. 93: 465-516. Published on 24 October 2006. This content downloaded from 143.106.1.143 on Wed, 20 Aug 2014 17:23:24 UTC All use subject to JSTOR Terms and Conditions 466 Annals of the Missouri Botanical Garden Plant reproductiveprocesses are believed to help Brazilian high-altitude grasslands are interesting determinethe compositionand structureof commu- communities in which to study plant-pollinator nities (Heithaus,1974, 1979; Bawa, 1990; Oliveira& interactions. Gibbs, 2000). Among such processes, the plant- In pollinationbiology, the degree of specialization pollinatorinteractions form a dynamic,yet somewhat in plant-pollinatorrelationships has generateda de- cohesive, ecological subunit of a community,which bate in which the traditional view based on the can be studied in terms of species diversity and syndromeconcept (see Faegri & van der Pijl, 1979) distribution,resource utilization,and niche packing, has been counterbalancedby skepticism about the for instance (Moldenke & Lincoln, 1979). In the specializednature of pollinationsystems (Waser et al., Neotropics,pollination biology at the communitylevel 1996; Herrera, 1996; see also Johnson & Steiner, has been studied in forest areas (Bawa et al., 1985; 2000 and Fenster et al., 2004 for reviews of both Kress & Beach, 1994), savanna-like vegetation views). Surveysof entire local assemblagesof plants (Silberbauer-Gottsberger& Gottsberger,1988; Ra- and their pollinators provide the best evidence to mirez, 1989, 2004; Barbosa,1997; Oliveira& Gibbs, assess the degree of specialization in pollination 2000; see also Ramirez & Brito, 1992) and sub- (Waser et al., 1996), because particular plant- Andean vegetation (Arroyo et al., 1982). In the pollinatorinteractions may be examined on a broad Brazilian Atlantic Forest Domain, there are several ecological scale, reducingthe samplingbias inherent studies on pollinationbiology in forest areas on both to the comparisonof data originatingfrom small scale individualspecies and flowerassemblages (Sazima et studies, such as those concerning particular plant al., 1995, 1996, 1999; Buzato et al., 2000 and taxonomicgroups. This paper describes the commu- references therein). However, for the high-altitude nity-level interactionsbetween plants and pollinators grasslands or campos de altitude- a subtype of the of high-altitudegrasslands at the Serra da Bocaina, Atlantic Forest Domain- informationon plant-polli- southeasternBrazil. We studied the floral biology of nator interactions is limited to a few case studies plant species, recordingtheir sexual systems, flower (Martinelli,1997; Freitas & Sazima,2001, 2003a, b; shapes, dimensions,resources, colors, and pollinators. Freitas et al., 2006). Combiningthe data on floral features and functional The high-altitudegrasslands in southeasternBrazil groups of pollinatorsallowed us to characterizenine comprise an archipelago of mountaintopformations pollination systems in these grasslandsand to group (ca. 1500 m elevation or higher) along the main plant species in four categories that express the mountain ranges, with a North/South orientation. degree of specialization/generalizationof plant-polli- Their origin is connected to glaciationepisodes since nator interactionsin this community.In addition,we at least
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