Differential Insecticide Susceptibility of the Neotropical Stingless Bee
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Differential insecticide susceptibility of the Neotropical stingless bee Melipona quadrifasciata and the honey bee Apis mellifera Mário Sarto, Eugênio Oliveira, Raul Guedes, Lúcio Campos To cite this version: Mário Sarto, Eugênio Oliveira, Raul Guedes, Lúcio Campos. Differential insecticide susceptibility of the Neotropical stingless bee Melipona quadrifasciata and the honey bee Apis mellifera . Apidologie, Springer Verlag, 2014, 45 (5), pp.626-636. 10.1007/s13592-014-0281-6. hal-01234763 HAL Id: hal-01234763 https://hal.archives-ouvertes.fr/hal-01234763 Submitted on 27 Nov 2015 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 (2014) 45:626–636 Original article * INRA, DIB and Springer-Verlag France, 2014 DOI: 10.1007/s13592-014-0281-6 Differential insecticide susceptibility of the Neotropical stingless bee Melipona quadrifasciata and the honey bee Apis mellifera 1 1 1 Mário César L. Del SARTO , Eugênio E. OLIVEIRA , Raul Narciso C. GUEDES , 2 Lúcio Antônio O. CAMPOS 1Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil 2Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil Received 28 October 2013 – Revised 23 January 2014 – Accepted 18 February 2014 Abstract – The toxicity of three insecticides frequently used in Neotropical tomato cultivation (abamectin, deltamethrin, and methamidophos) was estimated on foragers of the Neotropical stingless bee Melipona quadrifasciata (Lep.) and the honey bee Apis mellifera (L.). Our results showed that the susceptibility varied significantly with the type of exposure (ingestion, topical, or contact), and there were significant differences between species. While M. quadrifasciata was usually more susceptible to insecticides (except for abamectin) in realistic exposures (via ingestion and contact) than A. mellifera, the former was less susceptible than A. mellifera to topically applied insecticides, a less realistic means of insecticide exposure. These findings challenge the common extrapolation of toxicity bioassays with A. mellifera to all (native) bee pollinators. Such equivocated extrapolation may compromise the significant services provided by native bees in Neotropical ecosystems. insecticide exposure / acute toxicity / buzz pollinators / wild bees 1. INTRODUCTION findings suggest that multifactor interactions between honey bee diet, parasites, diseases, and The reported decline of bee populations and pesticides potentiate the decline in managed the potential impairment of the sustainability of honey bee colonies (vanEngelsdorp and Meixner pollination services performed by these insects 2010; Cornman et al. 2012;Becheretal.2013; are the target of current worldwide concerns Pettis et al. 2013). (Potts et al. 2010; Cameron et al. 2011; The significant decline of managed honey Lautenbach et al. 2012). Habitat destruction, bee colonies that has been reported mainly in climate change, pathogens, and pesticides are the USA and Europe drew further attention to thought to be the main contributors to colony wild pollinator communities and their potential decline of the honey bee Apis mellifera (L.) importance for pollination services in certain (Biesmeijer et al. 2006; Potts et al. 2010; landscapes and crop systems (Winfree et al. vanEngelsdorp and Meixner 2010), and recent 2007; Garibaldi et al. 2013; Jha and Kremen 2013). Native pollinator bees can perform equal to or better than the honey bee as pollinators for Corresponding author: E.E. Oliveira, some crops (Maeta and Kitamura 1981; Freitas [email protected] and Paxton 1998), significantly contributing to Manuscript editor: Monique Gauthier crop production even when honey bees are Insecticide toxicity to pollinator bees 627 present (Winfree et al. 2007; Garibaldi et al. Nature and Natural Resources (IUCN 2013), 2013). The stingless bees of the genus Melipona reinforcing the importance of assessing insecti- have been recognized as important pollinators cide impacts on M. quadrifasciata. Insecticide of native plants in subtropical and tropical areas bioassays were also performed with the honey bee (Antonini et al. 2006) and have been recently because of its broadly recognized role as the recognized as promising agents for commercial bee pollinator model in ecotoxicology protocols pollination in crop systems, such as those of for assessing the toxic effect of pesticides on tomatoes (Del Sarto et al. 2005; Bispo dos pollinators (Felton et al. 1986). Santos et al. 2009), eggplants (Nunes-Silva et Insecticide toxicity assessments using dif- al. 2013), and sweet peppers (Cruz et al. 2005). ferent means of exposing the stingless bee M. However, considering that pesticide application quadrifasciata (in addition to honey bees) pro- is a common agricultural practice in tropical vide basic toxicological information to guide areas (e.g., 500 pesticide active ingredients are insecticide use and minimize their potential non- registered in Brazil (Silveira and Antoniosi- target impact on native pollinators. The findings Filho 2013)), and that over 150 pesticides are of this study also assist in assessing the validity of currently used and known to be toxic to honey the honey bee as an indicator of insecticidal bees (Devillers et al. 2003; Johnson et al. 2010; impact on native stingless bees. Mullin et al. 2010), it is likely that stingless bee species that provide pollination services may 2. MATERIAL AND METHODS also be the non-intended target of harmful insecticide effects. 2.1. Insects Despite the recognized ecological and agri- cultural importance of stingless bees in tropical All insects used in this investigation were obtained areas, the majority of studies assessing insecti- from seven colonies of the Neotropical stingless bee cide impacts on pollinators have focused on M. quadrifasciata or from seven colonies of the honey bees with few studies assessing the Africanized honey bee A. mellifera maintained under insecticide susceptibility of stingless bee species field conditions at the Experimental Apiary of the (Moraes et al. 2000; Valdovinos-Núñez et al. Federal University of Viçosa (UFV, Viçosa, MG, 2009; Lourenço et al. 2012; Tomé et al. 2012). Brazil, 20°45′ S, 42°52′ W). To ensure genetic Here, we compared the susceptibility between variability between the colonies and to obtain more foragers of the honey bee A. mellifera and of reliable toxicological estimates, sets of foragers from the Neotropical stingless bee Melipona different colonies of either bee species were considered quadrifasciata (Lepetelier) to three insecticides as replicates. (deltamethrin, methamidophos, and abamectin) that are commonly used against insect pest species 2.2. Insecticides in Brazilian tomato fields (MAPA 2013). Concern regarding the stingless bee M. quadrifasciata is The concentration–mortality bioassays followed due to its wide distribution in Brazil, especially directive numbers 213 and 214 of the Organization where field and protected tomato systems are for Economic Cooperation and Development (OECD cultivated (Del Sarto et al. 2005; Bispo dos Santos 1998a, b). The insecticides used are neurotoxic et al. 2009). Furthermore, M. quadrifasciata compounds registered and commonly used for pest belongs to the same genus as the bee species control in field and in protected tomato crop systems Melipona capixaba (Moure and Camargo), which in Brazil (MAPA 2013). Attempting to mimic a more is recognized as an endangered species not realistic insecticide exposure in the field, bees were only by the Brazilian Ministry of Environment orally exposed to the insecticide commercial formu- (Normative Instructions no. 3, May 27, 2003 lations (pyrethroid deltamethrin: Decis 25 EC, Bayer (Resende et al. 2008; Luz et al. 2011)) but also by CropScience, São Paulo, Brazil; organophosphate the International Union for the Conservation of methamidophos: Tamaron BR, Bayer CropScience, 628 M.C.L. Del Sarto et al. São Paulo, Brazil; avermectin abamectin: Vertimec drilled to allow the bees (group of seven) access to 18 EC, Syngenta Proteção de Cultivos LTDA, São the honey syrup diet. Insecticide solutions were Paulo, Brazil). For the assays in which the bees were mixed in the diet and never exceeded 10 % of the topically exposed or contact-exposed, technical grade total diet volume. The bees were fasted for 1 h prior insecticides (purity≥90 %) were used and directly to the experiments before allowed access to the obtained from the manufacturers (deltamethrin and insecticide-treated diet for the subsequent 5 h. The methamidophos: Bayer CropScience, São Paulo, food consumption during this 5-h period was calcu- Brazil; abamectin: Syngenta Proteção de Cultivos lated by subtracting the amount of food left in the LTDA, São Paulo, Brazil). Whenever suitable, the Eppendorf tube, which allowed us to estimate the insecticides were classified according to their dose of insecticide to which the insects were exposed. toxicity to bees as described by Felton et al. After this 5-h period, the bees were allowed access to (1986) in