Long Distance Foraging and Recruitment by a Stingless Bee, Melipona Mandacaia Brunno Kuhn-Neto, Felipe A.L

Long distance foraging and recruitment by a stingless bee, Melipona mandacaia Brunno Kuhn-Neto, Felipe A.L. Contrera, Marina S. Castro, James C. Nieh To cite this version: Brunno Kuhn-Neto, Felipe A.L. Contrera, Marina S. Castro, James C. Nieh. Long distance foraging and recruitment by a stingless bee, Melipona mandacaia. Apidologie, Springer Verlag, 2009, 40 (4), 10.1051/apido/2009007. hal-00892028 HAL Id: hal-00892028 https://hal.archives-ouvertes.fr/hal-00892028 Submitted on 1 Jan 2009 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 40 (2009) 472–480 Available online at: c INRA/DIB-AGIB/ EDP Sciences, 2009 www.apidologie.org DOI: 10.1051/apido/2009007 Original article Long distance foraging and recruitment by a stingless bee, Melipona mandacaia* Brunno Kuhn-Neto1,FelipeA.L.Contrera2,3,MarinaS.Castro1,4, James C. Nieh2 1 Universidade Estadual de Feira de Santana, Departamento de Ciências Biológicas, Feira de Santana, Bahia, Brazil 2 University of California San Diego, Division of Biological Sciences, Section of Ecology, Behavior, and Evolution, La Jolla, California, USA 3 Current address: Universidade Federal do Pará, Instituto de Ciências Biológicas, Belém, PA, Brazil 4 Empresa Baiana de Desenvolvimento Agrícola, Laboratório de Abelhas, Salvador, Bahia, Brazil Received 24 October 2008 – Revised 13 December 2008 – Accepted 16 December 2008 Abstract – Body size is hypothesized to play a major role in animal foraging, particularly in pollinators. In general, species with larger bodies forage over greater distances. Studies have found support for this body size-foraging range hypothesis across a wide variety of pollinator species, but have not investigated the possibility that this effect also applies within a pollinator species. We trained foragers of the stingless bee Melipona mandacaia to feeders in their native habitat under natural conditions, and found that larger foragers forage at and recruit to significantly greater distances than smaller foragers. The maximum foraging and recruitment distances are significantly greater (by 24% and 48% respectively) for larger as compared to smaller foragers. We also provide the first direct evidence that stingless bees can forage in their native habitat at distances up to 2.1 km and recruit over 1 km from their nest, recruiting more than 230% farther than previously reported for any stingless bee feeder experiments. Natural size variation among colonies within the same species may play a role in foraging range, and could thus influence plant gene flow and population structure. stingless bees / foraging range / body size / recruitment / size variation 1. INTRODUCTION the strong effect of body size (Araujo et al., 2004; Greenleaf et al., 2007; Pereboom and Bees are among the most important in- Biesmeijer, 2003; van Nieuwstadt and Iraheta, sect pollinators in a wide variety of ecosys- 1996). For example, Araujo et al. (2004) con- tems (Bawa, 1990), especially in neotropi- cluded that 75% of maximum stingless bees cal lowland rain forests (Bawa et al., 1985). flight distances could be attributed to worker Many bee species are long distance foragers body size. However, the foraging ranges of that can, depending upon seasonal food densi- most bee species are unknown (Greenleaf ties, forage over several kilometers (Dornhaus et al., 2007). et al., 2006), and thus influence plant gene Relatively few studies have directly mea- flow (Bawa et al., 1985). Researchers have sured foraging distances (quantifying how therefore examined predictors of foraging far individuals travel to forage on natu- ranges in different bee species, principally ral food sources), despite the importance of this data for parameterizing ecological mod- Corresponding author: J.C. Nieh, els, determining adequate sizes for refugia [email protected] supporting these keystone pollinators, and * Manuscript editor: Stan Schneider understanding the evolution of bee foraging Article published by EDP Sciences Long distance bee foraging 473 strategies. Foraging range can be measured in- dacaia, in its native habitat. We chose this directly through capture and release studies species because foragers can recruit nestmates that model the probability of a released for- to a specific distance and direction (Nieh et al., ager returning to the nest (Goulson and Stout, 2003a) and because this is one of relatively 2001; Roubik and Aluja, 1983). This probabil- few meliponine species whose recruitment ity should decrease when foragers are released communication has been studied in detail. For- in distant areas they are not familiar with. agers produce sounds inside the nest, and the Genetic analysis of bees captured at sites temporal characteristics of these sounds are around the nest can yield direct estimates of correlated with the quality of the food and its foraging distance (Darvill et al., 2004). To distance from the nest (Nieh et al., 2003b). date, no published studies have used genetic Foragers can also deposit odors to assist orien- analysis to determine meliponine foraging tation near the food source (Nieh et al., 2003c). ranges. Finally, bees can be trained to feeders, with the maximum foraging distance measured as the maximum training distance. Un- 2. MATERIALS AND METHODS like capture and release or genetic analysis, training provides a direct measure of the max- 2.1. Colonies and study site imum distances at which the recruitment communication is used. Feeder training studies can Melipona mandacaia Smith is endemic to therefore provide key information about the the Caatinga biome and occurs around the São recruitment communication systems that have Francisco and the Vaza Barris rivers in Brazil evolved in response to different environments (Neves and Castro, 2006). This species ranges from and to fill diverse ecological niches. the north of Minas Gerais, throughout the state of Bahia, and extends to the border of Pernambuco. We focused on stingless bees (Hy- It also occurs in Paraiba and Ceará (Silveira et al., menoptera, Apidae, Meliponini), the only 2002). native neotropical pollinators known to recruit We conducted our studies in the Caatinga habitat nestmates to specific locations (Nieh, 2004). (a semi-arid habit with deciduous plants) on a small Stingless bees are significant pollinators farm in João Dourado, Bahia, Brazil (41◦4115W, throughout the tropics (Roubik et al., 1986), 11◦1845S). The Caatinga habitat is a relatively and exhibit a wide span of foraging distances. arid and inhospitable ecosystem, with average an- Kerr (1959) states that small bees such as nual temperatures of 28 ◦C, a prolonged dry season Plebeia mosquito (3 to 4 mm in length) can of food dearth and a short wet season of relative be trained to a feeder up to 500 m away food abundance whose timing varies with region and recruit up to 300 m (Piracicaba, Brazil). and year (Ab’Saber, 1974; Andrade-Lima, 1981; Medium sized bees such as Trigona spinipes Rizzini, 1997). The flora is dominated by small de- (5 mm) can be trained to feeders up to 840 m ciduous trees and shrubs that frequently bear spines and recruit up to 630 m (Piracicaba, Brazil, or thorns, cacti, and bromeliads (Andrade-Lima, Kerr, 1959). Large bees such as M. fuliginosa 1981; Rizzini, 1997). In this habitat, M. mandacaia (13–15 mm) have a flight range of 2000 m is an important native pollinator for many endemic (estimated from mark and recapure studies, species of flowering plants (Melo et al., 2002). We Wille, 1975). Using a training feeder, Kerr used three colonies during the dry season in 2005 (1959) found that T. trinidadensis can recruit from May to October (average annual rainfall is 55±48 mm per month and 13±14 mm from May to nestmates via an odor trial to distances up to October, data from http://br.weather.com). A larger 800 m and could be trained to 980 m (even data set would have been preferable, but we were though training conditions were not optimal only able to obtain three colonies. This species is because the feeder was in a shaded area). To difficult to find and becoming increasingly rare. In- date, 980 m is the greatest published distance dividuals who find wild colonies frequently destroy to which any stingless bee has been trained. them for their honey and do not keep them for We therefore used feeder training to esti- meliponiculture. In addition, nest sites are rapidly mate maximum foraging distance and recruit- disappearing because M. mandacaia prefers to nest ment distance of the stingless bee, M. man- in trees also valued for fence construction (Neves 474 B. Kuhn-Neto et al. and Castro, 2006). Thus, opportunities to obtain and colony 2 trial, but did not affect trials with other study M. mandacaia in its natural habitat are in- colonies. We trained bees by placing the feeder in creasingly limited. All colonies had been at this lo- contact with the nest entrance, waiting until 10 bees cation for several years. Colony flight activity cor- fed, and then moving the feeder in 20 m steps. We responds strongly to the number of foragers per moved the feeder 20 m further away when all bees colony in M. bicolor (Hilário et al., 2000, 2003). visiting at the previous distance returned. If no bees Based upon their flight activity levels, all three M. from the previous distance returned, we moved the mandacaia colonies were of similar size. Through- feeder 20 m back towards the nest. If the total num- out all trials, natural food sources were limited prin- ber of foragers decreased by 50%, we did not move cipally to Mimosa tenuiflora (Mimosaceae) flowers.

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