Oil-collecting bee–flower interaction network: do bee size and anther type influence the use of pollen sources? Laíce S. Rabelo, Alice M. G. F. Vilhena, Esther M. A. F. Bastos, Cândida M. L. Aguiar, Solange Cristina Augusto To cite this version: Laíce S. Rabelo, Alice M. G. F. Vilhena, Esther M. A. F. Bastos, Cândida M. L. Aguiar, Solange Cristina Augusto. Oil-collecting bee–flower interaction network: do bee size and anther type influence the use of pollen sources?. Apidologie, Springer Verlag, 2015, 46 (4), pp.465-477. 10.1007/s13592- 014-0336-8. hal-01284464 HAL Id: hal-01284464 https://hal.archives-ouvertes.fr/hal-01284464 Submitted on 7 Mar 2016 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2015) 46:465–477 Original article * INRA, DIB and Springer-Verlag France, 2014 DOI: 10.1007/s13592-014-0336-8 Oil-collecting bee–flower interaction network: do bee size and anther type influence the use of pollen sources? 1 1 2 Laíce S. RABELO , AliceM.G.F.VILHENA , Esther M. A. F. BASTOS , 3 1 Cândida M. L. AGUIAR , Solange Cristina AUGUSTO 1Instituto de Biologia, Universidade Federal de Uberlândia, Rua Ceará, Campus Umuarama, s/n. Caixa Postal 593, Uberlândia, Minas Gerais CEP 38400-902, Brazil 2Diretoria de Pesquisa e Desenvolvimento, Laboratório de Recursos Vegetais e Opoterápicos, Fundação Ezequiel Dias, Belo Horizonte, Brazil 3Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, Feira de Santana, Brazil Received 26 June 2014 – Revised 7 November 2014 – Accepted 24 November 2014 Abstract – Pollination is an ecosystem service sustained by a differentiated use of resources among sympatric species. The bee size can influence the similarity in the use of resources, and poricidal anthers limit the access to pollen. Therefore, we evaluated the influence of body size and the anther type of pollen sources in Centridini–flower interaction network. We expected that the low niche overlap, promoted by these morphological parameters, would result in the formation of subgroups and lead to greater network resilience. We studied 15 bee species (n =73 females) and identified their pollen sources. The bee size and anther type influenced the formation of subgroups in the community, and the larger bees used a higher proportion of flowers with poricidal anthers. Only the anther type influenced the robustness of the network. We conclude that the parameters analyzed influence both the use of resources by oil-collecting bees and their food niche breadth. pollen analysis / robustness / ecosystem services / solitary bees / trophic niche 1. INTRODUCTION (Cortopassi-Laurino et al. 2003; Nogueira-Ferreira and Augusto 2007). In plants, the presence of Organisms interact with each other in search of poricidal anthers limits the access of bees to pollen, resources and the ecosystem services, such as pol- because the release of the grains results from the lination, depend on the maintenance of these inter- energy produced by the vibration of anthers at the actions. The maintenance of pollination services is proper frequency (Buchmann 1978). Bees are able associated with the differentiated use of resources to vibrate at different frequencies according to their among sympatric species due to morphological and body size (Buchmann 1978;HarderandBarclay behavioral differences (Begon et al. 2006). In bee– 1994). Larger bees present a lower buzzing fre- plant systems, the body size influences the foraging quency during pollen collection in poricidal anthers distance of bees (Greenleaf et al. 2007)andthe than smaller species, which is likely to lead to lower similarity in the use of resources, which seems to energy consumption (Burkart et al. 2011). be greater between species with similar body size The recognition of the influence of these char- acteristics in the community structure can be per- formed using analyses of pollen and interaction network. The first tool allows identifying food Corresponding author: S. Augusto, sources used by bees (Jones and Jones 2001). [email protected] The second tool is used for the construction of a Manuscript editor: Klaus Hartfelder visual model of the community structure and the 466 L.S. Rabelo et al. identification of network properties, such as ro- their food niche breadth. We verified whether bustness and niche overlap (Jordano et al. 2003; there were subgroups in the community, consid- Memmott et al. 2004; Lewinsohn et al. 2006; ering the anther type of flowers and body size of Dormann and Gruber 2012). The robustness rep- bees. We also calculated the robustness of the resents the tolerance of the networks to species community to the systematic removal of bee spe- extinctions (Memmott et al. 2004) and can be cies in descending order of body size and accord- affected by generalization of the species or num- ing to the anther type. ber of links (Memmott et al. 2004; Staniczenko et al. 2010), connectance of the network (Dunne 2. MATERIAL AND METHODS et al. 2002), and habitat loss (Evans et al. 2013). The niche overlap represents the resource shar- 2.1. Study area ing among different species in a community (Begon et al. 2006). In bee–plant systems, char- The study was conducted at the Experimental acteristics such as the tongue length (Goulson and Station of Água Limpa (19° 05′ 48″ S/48° 21′ 05″ W), Darvill 2004), level of specialization of bees and belonging to the Federal University of Uberlândia, lo- flower abundance (Aguiar et al. 2013), and tem- cated in Uberlândia, Minas Gerais State, Brazil. The poral aspects of resource availability (Carvalho station comprises 1,040,000 m2 of woody savanna and et al. 2013; Santos et al. 2013) can influence the 1,947,200 m2 of pastures, crops, and orchards (Neto niche overlap among the species. 2008). The climate is characterized by two distinct Centridini bees are important pollinators of seasons, one hot and wet (from October to March) and cultivated species (Freitas and Paxton 1998; other cold and dry (from April to September) (Rosa Vilhena et al. 2012;Yamamotoetal.2012; et al. 1991). Oliveira et al. 2013). The bees of this group are specialized in collecting floral oils, especially 2.2. Sampling of Centridini bees from Malpighiaceae species, which can be used as bait plants (Alves-dos-Santos et al. 2007; The Centridini bees were collected during their visits Ribeiro et al. 2008; Vilhena et al. 2012; Oliveira to flower of West Indian cherry or acerola (Malpighia et al. 2013). Centridini bees present variation in emarginata DC) crop. Among the cultivated species in the body size among the species, i.e., bees of the study area, there were approximately 11,000 m2 of medium–large body length (≥1.2 cm) and small West Indian cherry trees. This species is self- bees (≤1.2 cm) (sensu Frankie et al. 1983), and incompatible and dependent upon pollination made can vibrate at different frequencies according to mainly by Centridini bee species (Freitas et al. 1999; their body size (Buchmann 1978). Vilhena et al. 2012; Oliveira et al. 2013). In a long-term Thus, the chief goal of this study was to eval- study about West Indian cherry pollination, Vilhena uate if the parameters, body size of the Centridini et al. (2012) collected 23 species of Centridini bees species and the anther type presented by their collecting mainly oil as floral resource. pollen sources, influence in the structure of this Most of species of Centridini bees are active during bee–plant community. We expect that these pa- the wet season, the flowering period of M. emarginata rameters influence the use of pollen sources to and other Malpighiaceae species (Gaglinone 2003; reduce the niche overlap. The lower niche overlap Vilhena et al. 2012). To identify the pollen sources used would result in the formation of subgroups and, by them and calculate the niche breadth, we collected therefore, lead to a greater resilience of the net- females with pollen loads on their scopa while they work to the removal of species and to the mainte- were visiting West Indian cherry flowers. The females nance of the pollination services. The presence of were collected in October/November and January/ subgroups in the community may hinder the cas- February (one sample/month) from 2004 to 2011, total- cade effect of extinction in plant–pollinator net- ing 24 sampling days and 120 h of observation. The works (Bosch et al. 2009). bees were sampled between 9:00 A.M. and 14:00 P.M. To evaluate these possible effects, we identified One researcher carried out the collections walking along the pollen sources used by Centridini bees and the inter-rows. Each shrub that presented inflorescences Oil-collecting bee–flower interaction network 467 was observed for about 5 min. Because individuals of After the identification of the plants used as this tribe visit West Indian cherry trees preferably to pollen sources by Centridini bees, we performed collect oil (Vilhena and Augusto 2007), and there is a quantitative analysis dividing the coverslip into four variation in the frequency of visits of these pollinators quadrants. There were counted approximately 100 over the years (Vilhena et al. 2012), we needed to realize pollen grains in each quadrant, and among those a long-term study (2004–2011) to obtained samples of with fewer than 100 grains, we counted all grains, pollen loads from most species of floral visitors.