Differential insecticide susceptibility of the Neotropical stingless bee Melipona quadrifasciata and the honey bee Apis mellifera Mário Sarto, Eugênio Oliveira, Raul Guedes, Lúcio Campos
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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 the following categories: highly toxic an insecticide-free diet, and mortality was recorded
(median lethal dose (LD50) values <1.0 μg a.i./bee), after 24 h. The bees were considered dead if unable moderately toxic (1.1
papers (Whatman no. 1), which were left to dry for fell within the highly toxic range of insecticide 30 min. These filter papers were used to cover the toxicity suggested by Felton et al. (1986). bottom of Petri dishes (9.0-cm diameter) that had Deltamethrin and abamectin were also highly toxic their inner walls coated with Teflon® PTFE (DuPont, to foragers of A. mellifera¸ unlike methamidophos Wilmington, DE, USA) to prevent the bees from (LD50=3.7 μg a.i./bee; Table I). For M. escaping. Each Petri dish received a group of 10 adult quadrifasciata, the scale of insecticide toxicity was forager bees from different colonies of the same abamectin>methamidophos>deltamethrin; for A. species. Insect mortality was recorded after 24 h of mellifera, the scale was abamectin>deltamethrin> exposure, and the bees were considered dead if methamidophos. unable to walk when prodded with a fine hair brush. An insecticide-free honey syrup diet was provided ad 3.2. Susceptibility to topically applied libitum to the bees during the exposure. The insecticides bioassays were performed at 28±2 °C and 65±5 % relative humidity (r.h.). Our results showed that M. quadrifasciata and A. mellifera were very tolerant to topically 2.4. Statistical analysis applied deltamethrin and methamidophos (LD50 values ≥100 μg a.i./bee; Table II); therefore, The concentration–mortality data were subjected to these compounds are virtually non-toxic to probit analysis (PROC PROBIT; SAS Institute 2008). these bee species. Topically applied abamectin The differential insecticide susceptibility between M. was also virtually non-toxic to M. quadrifasciata quadrifasciata and A. mellifera was calculated for each (LD50=136.7 μg a.i./bee) but was moderately insecticide based on the estimated LD50 (or median toxic to A. mellifera (LD50=7.8 μg a.i./bee). The lethal concentration (LC50)) for each insecticide and bee scale of insecticide toxicity for M. quadrifasciata species and dividing the LD50 (or LC50) value obtained was deltamethrin>abamectin>methamidophos; for M. quadrifasciata by the LD50 (or LC50) value for A. mellifera, the scale was abamectin> obtained for A. mellifera (Robertson and Preisler 1992). deltamethrin>methamidophos. The 95 % confidence limits of these toxicity rate estimates were considered to be significantly different 3.3. Contact susceptibility to dry insecticide (P<0.05) if they did not include the value 1 (Robertson residues and Preisler 1992). M. quadrifasciata was as susceptible as A. 3. RESULTS mellifera to dried deltamethrin residues (Table III). Both bee species were moderately Insecticide susceptibility was assessed in for- susceptible to this compound (LC50 values ager bees of M. quadrifasciata and A. mellifera approximately 6 μg a.i./mL). In contrast, M. (the model pollinator species). The insecticide quadrifasciata was 4-fold more susceptible to susceptibility varied significantly with the type of abamectin than A. mellifera (Table III), but both exposure (ingestion, topical, or contact), and there bee species were tolerant to methamidophos were significant differences between species for (LC50 values ≥96 μg a.i./mL; Table III), which some means of insecticide exposure. was slightly toxic to M. quadrifasciata and virtually non-toxic to A. mellifera (LC50 values 3.1. Susceptibility to ingested insecticides ≥400 μg a.i./mL; Table III). The LC50 values for deltamethrin and abamectin fell within the Based on the LD50 obtained in the concen- moderately toxic range (1.1
2 a b c Insecticides/species Number of samples Slope±S.E. LD50 (95 % FL) LD95 (95 % FL) χ P values TR (95 % CL ) (μg a.i./bee) (μg a.i./bee)
Abamectin M. quadrifasciata 443 4.7±0.50 0.015 (0.013–0.016) 0.033 (0.028–0.042) 1.7 0.80 − A. mellifera 443 6.1±0.99 0.011 (0.010–0.012) 0.020 (0.012–0.026) 0.1 0.99 0.73 (0.64–0.86) Deltamethrin M. quadrifasciata 284 2,7±0.35 0.082 (0.065–0.097) 0.320 (0.240–0.480) 3.5 0.33 − A. mellifera 299 1.8±0.44 0.850 (0.400–1.170) 7.000 (4.200–27.980) 4.0 0.12 10.4 (7.25–15.15) Methamidophos M. quadrifasciata 348 3.7±0.47 0.066 (0.050–0.093) 0.066 (0.050–0.093) 0.3 0.99 − ...DlSroe al. et Sarto Del M.C.L. A. mellifera 343 9.6±2.37 3.700 (3.300–3.900) 5.500 (4.800–7.600) 0.6 0.91 56.1 (49.60–60.90) a Probability values b Toxicity ratio (LC50 to A. mellifera/LC50 to M. quadrifasciata) c If the 95 % CL of TR includes the 1.0, the TRs are not significantly different Table II. Relative toxicity of topically applied insecticides (technical grade) to M. quadrifasciata and A. mellifera.
2 a b c Insecticides/species Number of samples Slope±S.E. LD50 (95 % FL) LD95 (95 % FL) χ P values TR (95 % CL ) (μg a.i./bee) (μg a.i./bee)
Abamectin M. quadrifasciata 224 3.0±0.39 134.6 (109.7–168.9) 471.6 (336.1–799.6) 3.8 0.28 − A. mellifera 264 6.7±1.54 7.8 (6.5–8.9) 13.8 (11.5–20.8) 4.7 0.32 0.06 (0.04–0.08) Deltamethrin M. quadrifasciata 288 3.0±0.38 129.2 (105.0–154.7) 460.6 (347.9–707.9) 5.3 0.38 − A. mellifera 267 3.3±0.47 112.2 (90.8–134.8) 359.6 (272.9–564.6) 2.1 0.71 0.87 (0.66–1.14) netcd oiiyt olntrbees pollinator to toxicity Insecticide Methamidophos M. quadrifasciata 224 2.0±0.44 296.6 (215.7–428.8) 1916.0 (1006.0–6895.0) 0.9 0.62 − A. mellifera 208 2.5±0.48 408.5 (295.6–603.6) 1537.0 (1077.0–5454.0) 0.1 0.93 1.62 (0.69–2.14) a Probability values b Toxicity ratio (LC50 to A. mellifera/LC50 to M. quadrifasciata) c If the 95 % CL of TR includes the 1.0, the TRs are not significantly different 631 632 Table III. Relative toxicity of contact-exposed insecticides (technical grade) to M. quadrifasciata and A. mellifera.
2 a b c Insecticides/species Number of samples Slope±S.E. LC50 (95 % FL) LC95 (95 % FL) χ P values TR (95 % CL ) (μg a.i./mL) (μg a.i./mL)
Abamectin M. quadrifasciata 480 2.8±0.42 3.8 (3.2–4.9) 14.7 (9.7–31.1) 1.3 0.52 − A. mellifera 480 2.3±0.34 15.4 (12.1–19.0) 83.0 (55.7–166.1) 1.2 0.56 4.0 (3.0–5.5) Deltamethrin M. quadrifasciata 420 2.3±0.25 5.6 (4.4–6.9) 29.9 (21.9–46.7) 6.8 0.34 − A. mellifera 420 4.1±0.81 6.6 (5.0–7.9) 66.6 (13.1–26.0) 2.3 0.32 1.2 (0.9–1.6) Methamidophos M. quadrifasciata 480 3.9±0.73 96.1 (81.2–113.6) 251.1 (186.9–456.0) 0.2 1.00 − ...DlSroe al. et Sarto Del M.C.L. A. mellifera 480 3.0±0.47 442.6 (336.1–582.0) 1537.0 (1014.0–3257.0) 3.3 0.35 4.6 (3.4–6.3) a Probability values b Toxicity ratio (LC50 to A. mellifera/LC50 to M. quadrifasciata) c If the 95 % CL of TR includes the 1.0, the TRs are not significant different Insecticide toxicity to pollinator bees 633
4. DISCUSSION contact between bee foragers and contaminated plant surfaces, the harvesting of contaminated The present study assessed the insecticide pollen and nectar, or the ingestion of contami- susceptibility of the Neotropical stingless bees nated sap from plants originating from M. quadrifasciata and the honey bee A. insecticide-coated seeds (Johnson et al. 2010; mellifera. The insecticides exhibited low overall Gill et al. 2012; Mullin et al. 2010). In our toxicity when topically applied to adult forager study, we assessed insecticide toxicity in polli- bees, while the ingested insecticides were nator bees and explored distinct means of usually very harmful to both bee species. exposure (ingestion, topical, and contact expo- Furthermore, contact exposure to dry residues sure) by using highly controlled conditions and of deltamethrin and abamectin was moderately rigorous experimental design bioassays that harmful, while methamidophos was virtually enabled comparative toxicity assessments be- non-toxic to both bee species. Our results tween Neotropical stingless bees and A. revealed that M. quadrifasciata is usually more mellifera. The results obtained here revealed susceptible to insecticides in realistic exposures that ingested insecticides are very harmful for via ingestion and contact than A. mellifera, with both bee species but are 10-fold more effective the exception of abamectin. In contrast, M. in killing native species than the honey bee. quadrifasciata is usually less susceptible to This is in accordance with previous studies that topically applied insecticides, which is a less have shown that other native bees are more realistic means of insecticide exposure. The susceptible to insecticides (Cresswell et al. findings reinforce the importance of testing 2012; Lourenço et al. 2012; Hardstone and ingestion and contact exposure rather than only Scott 2010). However, the insecticide abamectin topical exposure and challenge the notion that provided contrasting results, showing that the the honey bee is a suitable pollinator model (or native stingless bee is more tolerant than the bioindicator) for insecticide toxicity and risk honey bee for ingested and topically applied assessment. abamectin. Insecticide application is very common in Different insecticide susceptibility may result agroecosystems, which may harm many insect from insecticide- or insect-related differences. species that assist in pollination (Freitas et al. For instance, insecticide formulations usually 2009; Johnson et al. 2010; Krupke et al. 2012). enhance the insecticidal activity of the active Studies with pyrethroids, fipronil, and espe- ingredient (i.e., the insecticide), and the cially neonicotinoids have provided accumu- Africanized honey bees used in our study, lated evidence that insecticides can cause which prevails in Brazil, may respond differ- potential problems for colonies of A. mellifera ently to insecticide exposure than the European (Cresswell et al. 2012; Gill et al. 2012; Tirado honey bee, which prevails in most of the USA et al. 2013). However, the risk posed by and Europe. Indeed, the DL50 values for topical insecticides on other pollinator species has insecticide applications on A. mellifera from our been largely unexplored, although suspicions study are higher than those reported by the US that these native pollinators are seriously Environmental Protection Agency (abamectin threatened by insecticide applications have 0.41 μg a.i./bee, deltamethrin <0.7 μg a.i./bee, begun to arise (Morandin et al. 2005;Thompson methamidophos <1.4 μg a.i./bee, EPA 2014). et al. 2007;Osborne2012; Biddinger et al. 2013; These differences are likely the result of Decourtye et al. 2013). methodological differences among the studies, Bee exposure to insecticide may take place such as the solvent used (acetone in ours and 2- through a variety of means. Although pesticide propanol in the EPA database) and period of exposure may occur with compounds applied to exposure (24 h in our study and 48 h in the EPA control Varroa parasitic mites in beehives, database). Regarding species-related differ- pesticide exposure usually results from the ences, the differential insecticide susceptibility 634 M.C.L. Del Sarto et al. between A. mellifera and M. quadrifasciata ACKNOWLEDGMENTS observed here may result from differences in the life histories of both bee species. Life This work was supported by grants from the histories of different bee species vary con- Arthur Bernardes Foundation (FUNARBE), Minas siderably, and life story traits (e.g., sociality, Gerais State Foundation for Research Aid (FAPEMIG), body size, target-site sensitivity, and capacity the National Council of Scientific and Technological for detoxification by enhanced metabolism) Development (CNPq), and the CAPES Foundation. have been linked to differential sensitivity to pesticides (Liu et al. 2005; Hardstone and Scott 2010; Brittain and Potts 2011; Decourtye et Différence de susceptibilité aux insecticides entre l’abeille al. 2013). sans aiguillon néotropicale Melipona quadrifasciata et The overall higher insecticide susceptibility l’abeille domestique Apis mellifera of the native species compared with the honey Exposition à un insecticide / toxicité aigüe / pollinisateur / bee emphasizes the limited value of the extrap- abeille sauvage olation of the results of the toxicity bioassays that compare the latter species to native polli- Unterschiedliche Empfindlichkeit gegenüber Insektiziden nator species. 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