Abstract
In specialized plant-pollinator associations, partners may exhibit adaptive traits, which favor the maintenance of the interaction. The association between Calibrachoa elegans (Solanaceae) and its oligolectic bee pollinator, Hexantheda missionica (Colletidae), is mutualistic and forms a narrowly specialized pollination system. Flowers of C. elegans are pollinated exclusively by this bee species, and the bees restrict their pollen resources to this plant species. The pollen presentation schedules of C. elegans were evaluated at the population level to test the hypothesis that H. missionica females adjust their foraging behavior to the resource offering regime of C. elegans plants. For this, the number of new flowers and anthers opened per hour (as a proxy for pollen offering) was determined, and pollen advertisement was correlated with the frequency of flower visits during the day. Preferences of female bees for flowers of different stages were also investigated, and their efficiency as pollinators was evaluated. Pollen offering by C. elegans was found to be partitioned throughout the day through scattered flower openings. Females of H. missionica indeed adjusted their foraging activity to the most profitable periods of pollen availability. The females preferred new, pollen-rich flowers over old ones and gathered pollen and nectar selectively according to flower age. Such behaviors must optimize female bee foraging efficiency on flowers. Female bees set 93% of fruit after a single visit. These findings guarantee their importance as pollinators and the persistence of the specialized plant-pollinator association.
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References
ALMG (2009) Relatório Final: Comissão Especial das Serras da Calçada e da Moeda. Assembleia Legislativa do Estado de Minas Gerais. https://dspace.almg.gov.br/handle/11037/178. Accessed 10 March 2024
Alves-dos-Santos I, Wittmann D (2000) Legitimate pollination of the tristylous flowers of Eichhornia azurea (Pontederiaceae) by Ancyloscelis gigas bees (Anthophoridae, Apoidea). Plant Syst Evol 223(3–4):127–137. https://doi.org/10.1007/BF00985274
Araujo FF, Oliveira R, Mota T, Stehmann JR, Schlindwein C (2020) Solitary bee pollinators adjust pollen foraging to the unpredictable flower opening of a species of Petunia (Solanaceae). Biol J Linn Soc 129:273–287. https://doi.org/10.1093/biolinnean/blz193
Ayres M, Ayres Júnior M, Ayres DL (2007) Aplicações estatísticas Nas áreas das ciências bio-médicas, 5th edn. Instituto Mamirauá, Belém. Editor
Bond WJ (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Philos Trans R Soc Lond B Biol Sci 344(1307):83–90. https://doi.org/10.1098/rstb.1994.0055
Burger H, Dötterl S, Ayasse M (2010) Host-plant finding and recognition by visual and olfactory floral cues in an oligolectic bee. Funct Ecol 24:1234–1240. https://doi.org/10.1111/j.1365-2435.2010.01744.x
Cane HJ (2018) Co-dependency between a specialist Andrena bee and its death camas host, Toxicoscordion paniculatum. Arthropod-Plant Inte 12:657–662. https://doi.org/10.1007/s11829-018-9626-9
Cane HJ (2021) A brief review of monolecty in bees and benefits of a broadened definition. Apidologie 52:17–22. https://doi.org/10.1007/s13592-020-00785-y
Cane JH, Sipes S (2006) Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, pp 99–122
Carvalho AT, Schlindwein C (2011) Obligate association of an oligolectic bee and a seasonal aquatic herb in semi-arid north-eastern Brazil. Biol J Linn Soc 102(2):355–368. https://doi.org/10.1111/j.1095-8312.2010.01587.x
Carvalho AT, Dötterl S, Schlindwein C (2014) An aromatic volatile attracts oligolectic bee pollinators in an interdependent bee-plant relationship. J Chem Ecol 40:1126–1134. https://doi.org/10.1007/s10886-014-0510-5
Cerceau I, Siriani-Oliveira S, Dutra AL, Oliveira R, Schlindwein C (2019) The cost of fidelity: foraging oligolectic bees gather huge amounts of pollen in a highly specialized cactus-pollinator association. Biol J Linn Soc 128(1):30–43. https://doi.org/10.1093/biolinnean/blz083
CNCFlora (2012) Calibrachoa elegans in Lista Vermelha da Flora Brasileira, version 2012.2 Centro Nacional de Conservação da Flora. http://cncflora.jbrj.gov.br/portal/pt-br/profile/Calibrachoa%20elegans. Accessed 10 March 2024
Danforth BN, Minckley RL, Neff JL (2019) The solitary bees. Biology, evolution, conservation. Princeton University Press
Dobson HEM (1987) Role of flower and pollen aromas in host-plant recognition by solitary bees. Oecologia 72:618–623. https://doi.org/10.1007/BF00378991
Dötterl S, Füssel U, Jürgens A, Aas G (2005) 1,4-Dimethoxybenzene, a floral scent compound in willows that attracts an oligolectic bee. J Chem Ecol 31:2993–2998. https://doi.org/10.1007/s10886-005-9152-y
Dutra Al, Schlindwein C, Oliveira R (2020) Females of a solitary bee reject males to collect food for offspring. Behav Ecol 31(4):884–891. https://doi.org/10.1093/beheco/araa026
Gentry AH (1974) Flowering phenology and diversity in tropical Bignoniaceae. Biotropica 6(1):64–68. https://doi.org/10.2307/2989698
Gori DF (1989) Floral color change in Lupinus argenteus (Fabaceae): why should plants advertise the location of unrewarding flowers to pollinators? Evolution, 43:870–881. https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1558-5646.1989.tb05184.x
Hammer Ø, Harper DA, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:9. https://doc.rero.ch/record/15326/files/PAL_E2660.pdf Acessed 10 March 2024
Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am Nat 133(3):323–344. https://doi.org/10.1086/284922
Harder LD, Wilson WG (1994) Floral evolution and male reproductive success: optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evol Ecol 8:542–559. https://doi.org/10.1007/BF01238257
Hempel de Ibarra N, Langridge KV, Vorobyev M (2015) More than colour attraction: behavioural functions of flower patterns. Curr Opin Insect Sci 12:64–70. https://doi.org/10.1016/j.cois.2015.09.005
Lamont B (1985) The significance of flower colour change in eight co-occurring shrub species. Bot J Linn Soc 90:145–155. https://doi.org/10.1111/j.1095-8339.1985.tb02206.x
Lloyd DG, Yates JM (1982) Intrasexual selection and the segregation of pollen and stigmas in hermaphrodite plants, exemplified by Wahlenbergia Albomarginata. (Campanulaceae) Evol 36(5):903–913. https://doi.org/10.2307/2408071
Lunau K, Maier E (1995) Innate colour preferences of flower visitors. J Comp Physiol A 177:1–19. https://doi.org/10.1007/BF00243394
Lunau K, De Camargo MGG, Brito VLG (2024) Pollen, anther, stamen, and androecium mimicry. Plant Biol 66(3):349–368. https://doi.org/10.1111/plb.13628
Medeiros PCR, Schlindwein C (2003) Territórios De machos, acasalamento, distribuição e relação com plantas em Protomeliturga turnerae (Ducke, 1907) (Hymenoptera, Andrenidae). Rev Bras Entomol 47(4):589–596. https://doi.org/10.1590/S0085-56262003000400009
Melo BT, Mota T, Schlindwein C, Antonini Y, Oliveira R (2018) Floral colour change in Byrsonima Variabilis (Malpighiaceae) as a visual cue for pollen but not oil foraging by oil-collecting bees. Sci Nat 105:46. https://doi.org/10.1007/s00114-018-1572-y
Milet-Pinheiro P, Schlindwein C (2010) Mutual reproductive dependence of distylic Cordia leucocephala (Cordiaceae) and oligolectic Ceblurgus longipalpis (Halictidae, Rophitinae) in the Caatinga. Ann Bot 106:17–27. https://doi.org/10.1093/aob/mcq077
Milet-Pinheiro P, Ayasse M, Dobson HEM, Schlindwein C, Francke W, Dötterl S (2013) The Chemical basis of host-plant recognition in a specialized bee pollinator. J Chem Ecol 39:1347–1360. https://doi.org/10.1007/s10886-013-0363-3
Minckley RL, Wcislo WT, Yanega D, Buchmann SL (1994) Behavior and phenology of a specialist bee (Dieunomia) and sunflower (Helianthus) pollen availability. Ecology 75(5):1406–1419. https://doi.org/10.2307/1937464
Müller A (1996) Host-plant specialization in western palearctic anthidine bees (Hymenoptera: Apoidea: Megachilidae). Ecol Monogr 66(2):235–257. https://doi.org/10.2307/2963476
Nicholls E, Hempel de Ibarra N (2017) Assessment of pollen rewards by foraging bees. Funct Ecol 31:76–87. https://doi.org/10.1111/1365-2435.12778
Ogloblin A (1948) Descripción De Dos géneros nuevos de paracolletini argentinos (Colletidae, Apoidea, Hymenoptera). Notas Del Museo De La Plata: Zool 13:165–177
Oliveira R, Schlindwein C (2010) Experimental demonstration of alternative mating tactics of male Ptilothrix fructifera (Hymenoptera, Apidae). Anim Behav 80(2):241–247. https://doi.org/10.1016/j.anbehav.2010.04.024
Osche G (1979) Zur Evoution Optischer Signale Bei Blütenpflanzen. Biol Unserer Zeit 9(6):161–170. https://doi.org/10.1002/biuz.19790090604
Reck-Kortmann M, Silva-Arias GA, Stehmann JR, Greppi JA, Freitas LB (2015) Phylogenetic relationships of Petunia Patagonica (Solanaceae) revealed by molecular and biogeographical evidence. Phytotaxa 222(1):17–32. https://doi.org/10.11646/phytotaxa.222.1.2
Robertson C (1925) Heterotropic bees. Ecology 6(4):412–436. https://doi.org/10.2307/1929107
Rodrigues DM, Caballero-Villalobos L, Turchetto C, Jacques RA, Kuhlemeier C, Freitas LB (2018) Do we truly understand pollination syndromes in Petunia as much as we suppose? AoB Plants 10:ply057. https://doi.org/10.1093/aobpla/ply057
Schaal BA, Leverich WJ (1980) Pollination and banner markings in Lupinus texensis (Leguminosae). Southwest Naturalist 25:280–282. https://www.jstor.org/stable/3671260
Schlindwein C (2004) Are oligolectic bees always the most effective? In Freitas BM and Pereira JOP (eds.) Solitary bees. Conservation, rearing and management for pollination. Fortaleza. Impensa Universitária, pp 231–241
Schlindwein C, Martins CF (2000) Competition between the oligolectic bee Ptilothrix plumata (Anthophoridae) and the flower closing beetle Pristimerus Calcaratus (Curculionidae) for floral resources of Pavonia Cancelata (Malvaceae). Plant Syst Evol 224:183–194. https://doi.org/10.1007/BF00986342
Schlindwein C, Wittmann D (1997) Micro-foraging routes of Bicolletes pampeana (Colletidae) and bee-induced pollen presentation in Cajophora arechavaletae. Bot Acta 110:177–183. https://doi.org/10.1111/j.1438-8677.1997.tb00626.x
Silveira FAO et al (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403(1–2):129–152. https://doi.org/10.1007/s11104-015-2637-8
Siriani-Oliveira S, Oliveira R, Schlindwein C (2018) Pollination of Blumenbachia amana (Loasaceae): flower morphology and partitioned pollen presentation guarantee a private reward to a specialist pollinator. Biol J Linn Soc 124(3):479–491. https://doi.org/10.1093/biolinnean/bly061
Siriani-Oliveira S, Cerceau I, Schlindwein C (2020) Specialised protagonists in a plant–pollinator interaction: the pollination of Blumenbachia Insignis (Loasaceae). Plant Biol 22(2):167–176. https://doi.org/10.1111/plb.13072
Souza SS, Ramos RF, Dartora N, Pelegrin CMG, Pinheiro M (2022) Who are the pollinators of Petunia Interior (Solanaceae) and how are they attracted to flowers? Acta Bot Bras 36. https://doi.org/10.1590/0102-33062021abb0209
Stehmann JR, Semir J (2001) Biologia reprodutiva de Calibrachoa elegans (Miers) Stehmann & Semir (Solanaceae). Braz J Bot 24:43–49. https://doi.org/10.1590/S0100-84042001000100005
Stone GN, Gilbert F, Willmer P, Potts S, Semida F, Zalat S (1999) Windows of opportunity and the temporal structuring of foraging activity in a desert solitary bee. Ecol Entomol 24(2):208–221. https://doi.org/10.1046/j.1365-2311.1999.00181.x
Strickler K (1979) Specialization and foraging efficiency of solitary bees. Ecology 60(5):998–1009. https://doi.org/10.2307/1936868
Urban D, Graf V (2000) Albinapis gracilis gen. n. and sp. n. and Hexantheda enneomera sp. n. from Southern Brazil (Hymenoptera, Colletidae, Paracolletini). Rev Bras Zool 17:595–601. https://doi.org/10.1590/S0101-81752000000300005
Vázquez DP, Aizen MA (2004) Asymmetric specialization: a pervasive feature of plant–pollinator interactions. Ecology 85(5):1251–1257. https://doi.org/10.1890/03-3112
Viana PL, Lombardi JA (2007) Florística e caracterização dos campos rupestres sobre canga na Serra da Calçada, Minas Gerais. Brasil Rodriguésia 58(1):159–177. https://doi.org/10.1590/2175-7860200758112
Wcislo WT, Cane JH (1996) Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Annu Rev Entomol 41(1):257–286. https://doi.org/10.1146/annurev.en.41.010196.001353
Weiss MR (1991) Floral colour changes as cues for pollinators. Nature 354:227–229. https://www.nature.com/articles/354227a0
Westerkamp CH (1996) Pollen in bee-flower relations some considerations on melittophily. Bot Acta 109(4):325–332. https://doi.org/10.1111/j.1438-8677.1996.tb00580.x
Yang S, Chu G, Shi X, Wang S (2019) Elaborated pollen packaging and dispensing mechanism induced by petal architecture from a Papaveraceae species. PeerJ 7:e7066. https://doi.org/10.7717/peerj.7066
Acknowledgements
We thank João Renato Stehmann for critical comments on an earlier version of the manuscript; Elaine Cordeiro, Dario Dias, Rafael Cordeiro, and Satya Stewart for help with fieldwork; Rafael and Celso for kindly hosting for field studies; members of group Plebeia–Ecologia de Abelhas e da Polinização for support and discussion; we also thank the anonymous reviewers for constructive comments that improved the final version of the manuscript. Instituto Chico Mendes de Conservação da Biodiversidade-ICMBio for the license Nr 61658-1 to collect samples and work with the red list Calibrachoa elegans; Instituto Estadual de Florestas IEF for license Nr 033/2018; and Vale S.A. for the authorization to conduct the study on their property.
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We acknowledge financial support from the Conselho Nacional de Desenvolvimento Científico e Tecnológico–Brazil (CNPq) to CS (Universal 436095/2018-1; 403421/2023-3; PQ 314829/2021-0), from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) to RO (88882.316026/2019-0) and to LP (88887.336088/2019-00), and from Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) to ALCV.
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C.S., A.L.C.V., and R.O. conceived and designed the study; A.L.C.V. and L.C.P. collected data; A.L.C.V. and R.O. analyzed the data; R.O. and C.S. supervised the study; C.S. secured funding; A.L.C.V., R.O., and C.S. wrote the draft; A.L.C.V., L.C.P., R.O., and C.S. read and commented on subsequent drafts; all authors approved the final version.
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Vieira, A.L.C., Pataca, L.C., Oliveira, R. et al. Fields of flowers with few strikes: how oligolectic bees manage their foraging behavior on Calibrachoa elegans (Solanaceae). Sci Nat 111, 26 (2024). https://doi.org/10.1007/s00114-024-01912-w
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DOI: https://doi.org/10.1007/s00114-024-01912-w