Toxicity of Organophosphorus Pesticides to the Stingless Bees
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Toxicity of organophosphorus pesticides to the stingless bees Scaptotrigona bipunctata and Tetragonisca fiebrigi Andressa Linhares Dorneles, Annelise de Souza Rosa, Betina Blochtein To cite this version: Andressa Linhares Dorneles, Annelise de Souza Rosa, Betina Blochtein. Toxicity of organophosphorus pesticides to the stingless bees Scaptotrigona bipunctata and Tetragonisca fiebrigi. Apidologie, 2017, 48 (5), pp.612-620. 10.1007/s13592-017-0502-x. hal-02973427 HAL Id: hal-02973427 https://hal.archives-ouvertes.fr/hal-02973427 Submitted on 21 Oct 2020 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 (2017) 48:612–620 Original article * INRA, DIB and Springer-Verlag France, 2017 DOI: 10.1007/s13592-017-0502-x Toxicity of organophosphorus pesticides to the stingless bees Scaptotrigona bipunctata and Tetragonisca fiebrigi 1 2 1 Andressa Linhares DORNELES , Annelise de SOUZA ROSA , Betina BLOCHTEIN 1Departamento de Biodiversidade e Ecologia, Faculdade de Biociências, Pontifícia Universidade Católica do Rio Grande do Sul, Av. Ipiranga, 6681, Porto Alegre, RS 90619-900, Brazil 2Laboratório de Ecotoxicologia e Conservação de Abelhas, Instituto de Biociências, Universidade Estadual Paulista Júlio de Mesquita Filho, Av. 24-A, 1515, Bela Vista, Rio Claro, São Paulo 13506-900, Brazil Received 25 October 2016 – Revised 31 January 2017 – Accepted 24 February 2017 Abstract – This study estimated the toxicity of the insecticides chlorpyrifos and phosmet to the stingless bees Scaptotrigona bipunctata and Tetragonisca fiebrigi . The results showed significant differences in susceptibility between the tested species, indicating that S. bipunctata are more tolerant to chlorpyrifos than T. fiebrigi in both assays. In contrast, the two tested stingless bee species showed no significant differences in susceptibility to phosmet. Our findings indicated that the insecticides chlorpyrifos and phosmet are potentially dangerous to S. bipunctata and T. fiebrigi both topically and by ingestion. It is essential to propose measures to minimize the impact of these products on pollinators. This study is the first evaluation of the lethal effects of the insecticides chlorpyrifos and phosmet to S. bipunctata and T. fiebrigi , and it provides important support for future studies on pesticide toxicity in stingless bees. acute oral toxicity / acute topical toxicity / chlorpyrifos / phosmet / pollinators 1. INTRODUCTION Factors such as habitat fragmentation, loss of native vegetation and climate change are ongoing Pollination is an environmental service essen- contributors to reductions in bee populations tial for the maintenance of natural ecosystems and (Freitas et al. 2009). However, the unsustainable agriculture (Costanza et al. 1997; Ricketts et al. use of agricultural ecosystems and the excessive 2008). Approximately 85% of angiosperm species use of pesticides are considered the leading causes are pollinated by animals (Ollerton et al. 2011). of bee diversity losses (Wiest et al. 2011; Nicholls Bees are considered the most efficient pollinators and Altieri 2013; Sanchez-Bayo and Goka 2014). (Potts et al. 2010) and are responsible for pollinat- Within this context, pesticide applications on ing approximately 70% of cultured plant species crops that produce bee-attracting flowers should (Ricketts et al. 2008). be considered in studies of hazards to pollinator The current decline in diversity and abundance species. In Brazil, bee pollination services are of pollinators has raised concerns (Dively and critically important to several crops, including Kamel 2012) regarding the future sustainability apples, coffee, cotton, oranges and soybeans of pollination services (Biesmeijer et al. 2006). (Imperatriz-Fonseca 2004). Cultivating these crops involves applying a wide range of pesticides for disease and pest control Corresponding author: A. Dorneles, (Rocha 2012). Of particular importance in this con- [email protected] text are organophosphate pesticides such as chlorpyr- Manuscript editor: Monique Gauthier ifos and phosmet. These insecticides have a broad Insecticide toxicity to stingless bees 613 action spectrum and are highly toxic and damaging to do Rio Grande do Sul (PUCRS) (Porto Alegre, RS, the environment, including to non-target insect spe- Brazil, 30° 3′ S, 51° 10 W). cies (Cutler et al. 2014). Chlorpyrifos and phosmet Sixty bees from each species were used for each are neurotoxic insecticides that act by inhibiting ace- exposure (dose/concentration) and its respective tylcholinesterase, an enzyme essential to the transmis- controls. For tests on S. bipunctata , each treatment sion of nerve impulses (Silva et al. 2015). consisted of five replicates with 12 bees in each Due to its global importance as a pollinator, Apis replicate. For tests on T. fiebrigi ,eachtreatment mellifera L. is the species most often used as a consisted of three replicates with 20 bees in each model organism in studies of non-target insect tox- replicate. To maintain equivalent confinement con- icity (Brittain and Potts 2011). However, it is well ditions, the distribution of the number of bees in known that different bee species are differentially each box was determined by considering the size susceptible to insecticides (Alston et al. 2007). and behaviour of the individuals of the two species. Therefore, evaluation of pesticide toxicity in other To ensure genetic variability and obtain more reli- bee taxa should be considered. The stingless bees able toxicological estimates, each replicate consisted (Meliponini) have biological characteristics condu- of bees from different colonies. cive for use in managed pollination (Venturieri et al. For the oral exposure tests, bees were collected 2011) and are gradually being recognized as alter- near the entrance to each colony and transferred to natives for commercial pollination operations in wooden cages (9.5 × 11.5 × 2.5 cm). For the tropical and subtropical regions (Slaa et al. 2006). topical tests, the bees were transferred to Petri Nevertheless, there has been little research into their dishes (150 × 15 mm) lined with filter paper. susceptibility to pesticides (Santos et al. 2016). To minimize the stress of confinement, before Scaptotrigona bipunctata (Lepeletier) and testing, the bees were allowed to adapt for 24 h, Tetragonisca fiebrigi (Schwarz) are among the most during which time they were fed a sucrose solu- commonly kept Meliponini species in three Brazil- tion containing no insecticide. During the adapta- ian biomes (Pampas, Atlantic Rainforest and tion and experimental periods, the bees were Pantanal). S. bipunctata , popularly known as the maintained in a chamber of biochemical oxygen tubuna, is found in Bolivia, Brazil, Paraguay and demand (BOD) at 28 ± 2°C and 70 ± 2% RH. Peru, where it forms large nests with massive honey The insecticides used were commercially avail- output capacity. T. fiebrigi , known as the jataí, is able products: chlorpyrifos (Lorsban® 480BR, Dow found in parts of Argentina, Bolivia, Brazil and AgroSciences, 48% active ingredient (a.i.)) and Paraguay, is easily managed and is highly regarded phosmet (Imidan® 500wp, Cross Link, 50% a.i.) as an excellent honey producer (Venturieri et al. (MAPA 2015). 2011; Camargo and Pedro 2013). The susceptibility of bee foragers to each insec- In view of the widespread use of organophos- ticide was tested via two routes of exposure: oral phate insecticides on bee-attractive crops in Brazil and topical. Both trials were conducted in accor- and the consequent risk to non-target organisms, dance with the international guidelines for pesticide as well as the large geographic range of toxicity testing in honeybees (OECD 1998a, b). To S. bipunctata and T. fiebrigi , the present study determine the appropriate concentrations for the sought to determine the median lethal concentra- formal test, preliminary bioassays were performed tion (LC50) for oral exposure and the median with ten serial dilutions of the stock solution at a lethal dose (LD50) for topical exposure of factor of 10 (1 μg a.i./μL of distilled water) follow- S. bipunctata and T. fiebrigi of foragers to the ing Medrzycki et al. (2013). Second, a series of five insecticides chlorpyrifos and phosmet. concentrations (with a factor not exceeding 2) was established to cover the mortality range of 1 to 2. MATERIAL AND METHODS 100% in relation to the slope of the toxicity curve (OECD 1998a, b). To ascertain the median lethal The bees used in this study were obtained from concentration (LC50) for oral assays and median S. bipunctata and T. fiebrigi colonies kept at the lethal dose (LD50) for topical assays, mortality rates Meliponary of the Pontifícia Universidade Católica were recorded after 48 h of exposure to each 614 A.L. Dorneles et al. insecticide. Bees that remained immobile for more were determined with the Btwo-parameter log- than 10 s were considered dead. logistic function^ of the Bdrc^ package in the Analysis of Dose-Response Curves (Ritz and 2.1. Acute oral toxicity Streibig 2005), compiled in