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Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides.

Tomé HV, Martins GF, Lima MA, Campos LA, Guedes RN - PLoS ONE (2012)

Bottom Line: No sublethal effect on body mass or developmental time was observed in the surviving insects, but the pesticide treatment negatively affected the development of mushroom bodies in the brain and impaired the walking behavior of newly emerged adult workers.Therefore, stingless bee larvae are particularly susceptible to imidacloprid, as it caused both high mortality and sublethal effects that impaired brain development and compromised mobility at the young adult stage.These findings demonstrate the lethal effects of imidacloprid on native stingless bees and provide evidence of novel serious sublethal effects that may compromise colony survival.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.

ABSTRACT
Declines in pollinator colonies represent a worldwide concern. The widespread use of agricultural pesticides is recognized as a potential cause of these declines. Previous studies have examined the effects of neonicotinoid insecticides such as imidacloprid on pollinator colonies, but these investigations have mainly focused on adult honey bees. Native stingless bees (Hymenoptera: Apidae: Meliponinae) are key pollinators in neotropical areas and are threatened with extinction due to deforestation and pesticide use. Few studies have directly investigated the effects of pesticides on these pollinators. Furthermore, the existing impact studies did not address the issue of larval ingestion of contaminated pollen and nectar, which could potentially have dire consequences for the colony. Here, we assessed the effects of imidacloprid ingestion by stingless bee larvae on their survival, development, neuromorphology and adult walking behavior. Increasing doses of imidacloprid were added to the diet provided to individual worker larvae of the stingless bee Melipona quadrifasciata anthidioides throughout their development. Survival rates above 50% were only observed at insecticide doses lower than 0.0056 µg active ingredient (a.i.)/bee. No sublethal effect on body mass or developmental time was observed in the surviving insects, but the pesticide treatment negatively affected the development of mushroom bodies in the brain and impaired the walking behavior of newly emerged adult workers. Therefore, stingless bee larvae are particularly susceptible to imidacloprid, as it caused both high mortality and sublethal effects that impaired brain development and compromised mobility at the young adult stage. These findings demonstrate the lethal effects of imidacloprid on native stingless bees and provide evidence of novel serious sublethal effects that may compromise colony survival. The ecological and economic importance of neotropical stingless bees as pollinators, their susceptibility to insecticides and the vulnerability of their larvae to insecticide exposure emphasize the importance of studying these species.

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Serial histological sections of the brain of a stingless bee worker (Melipona quadrifasciata anthidioides). The edges of the mushroom bodies are delineated with white lines. The sections are ordered such that A, D and H represent the beginning, middle and end of the structure, respectively. MC, median calyx; LC, lateral calyx; VL, vertical lobe; MB, mushroom bodies; Oce, oceli; Ant, antennal lobe; OL, optic lobe; CB, central body. Bar: 500 µm.
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pone-0038406-g001: Serial histological sections of the brain of a stingless bee worker (Melipona quadrifasciata anthidioides). The edges of the mushroom bodies are delineated with white lines. The sections are ordered such that A, D and H represent the beginning, middle and end of the structure, respectively. MC, median calyx; LC, lateral calyx; VL, vertical lobe; MB, mushroom bodies; Oce, oceli; Ant, antennal lobe; OL, optic lobe; CB, central body. Bar: 500 µm.

Mentions: Five brains were used for each combination of imidacloprid dose and age (one, four and eight days after emergence). Each brain was serially sectioned into 7 µm-thick slices with a glass knife on an automatic microtome. The sections were stained with hematoxylin and eosin and subsequently photographed using a digital camera (Canon Power Shot A640, Lake Success, NY, USA) coupled to a light microscope (Axioskop 40, Zeiss, Göttingen, Germany). One of the first six sections in which the mushroom bodies were apparent was randomly selected for area measurement (µm2). The same measurement was performed at each of six section intervals with the software Image-Pro Plus™ (MediaCybernetics, Bethesda, MD, USA). The volume of the mushroom bodies was determined by measuring the medial lobe, vertical lobe, peduncle and lateral and medial calyxes (Fig. 1), applying the Cavalieri method [55]. The volume estimated with this method differs by less than 5% from the volume estimated using all of the sections through this structure [37], [56], [57].


Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides.

Tomé HV, Martins GF, Lima MA, Campos LA, Guedes RN - PLoS ONE (2012)

Serial histological sections of the brain of a stingless bee worker (Melipona quadrifasciata anthidioides). The edges of the mushroom bodies are delineated with white lines. The sections are ordered such that A, D and H represent the beginning, middle and end of the structure, respectively. MC, median calyx; LC, lateral calyx; VL, vertical lobe; MB, mushroom bodies; Oce, oceli; Ant, antennal lobe; OL, optic lobe; CB, central body. Bar: 500 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3366975&req=5

pone-0038406-g001: Serial histological sections of the brain of a stingless bee worker (Melipona quadrifasciata anthidioides). The edges of the mushroom bodies are delineated with white lines. The sections are ordered such that A, D and H represent the beginning, middle and end of the structure, respectively. MC, median calyx; LC, lateral calyx; VL, vertical lobe; MB, mushroom bodies; Oce, oceli; Ant, antennal lobe; OL, optic lobe; CB, central body. Bar: 500 µm.
Mentions: Five brains were used for each combination of imidacloprid dose and age (one, four and eight days after emergence). Each brain was serially sectioned into 7 µm-thick slices with a glass knife on an automatic microtome. The sections were stained with hematoxylin and eosin and subsequently photographed using a digital camera (Canon Power Shot A640, Lake Success, NY, USA) coupled to a light microscope (Axioskop 40, Zeiss, Göttingen, Germany). One of the first six sections in which the mushroom bodies were apparent was randomly selected for area measurement (µm2). The same measurement was performed at each of six section intervals with the software Image-Pro Plus™ (MediaCybernetics, Bethesda, MD, USA). The volume of the mushroom bodies was determined by measuring the medial lobe, vertical lobe, peduncle and lateral and medial calyxes (Fig. 1), applying the Cavalieri method [55]. The volume estimated with this method differs by less than 5% from the volume estimated using all of the sections through this structure [37], [56], [57].

Bottom Line: No sublethal effect on body mass or developmental time was observed in the surviving insects, but the pesticide treatment negatively affected the development of mushroom bodies in the brain and impaired the walking behavior of newly emerged adult workers.Therefore, stingless bee larvae are particularly susceptible to imidacloprid, as it caused both high mortality and sublethal effects that impaired brain development and compromised mobility at the young adult stage.These findings demonstrate the lethal effects of imidacloprid on native stingless bees and provide evidence of novel serious sublethal effects that may compromise colony survival.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.

ABSTRACT
Declines in pollinator colonies represent a worldwide concern. The widespread use of agricultural pesticides is recognized as a potential cause of these declines. Previous studies have examined the effects of neonicotinoid insecticides such as imidacloprid on pollinator colonies, but these investigations have mainly focused on adult honey bees. Native stingless bees (Hymenoptera: Apidae: Meliponinae) are key pollinators in neotropical areas and are threatened with extinction due to deforestation and pesticide use. Few studies have directly investigated the effects of pesticides on these pollinators. Furthermore, the existing impact studies did not address the issue of larval ingestion of contaminated pollen and nectar, which could potentially have dire consequences for the colony. Here, we assessed the effects of imidacloprid ingestion by stingless bee larvae on their survival, development, neuromorphology and adult walking behavior. Increasing doses of imidacloprid were added to the diet provided to individual worker larvae of the stingless bee Melipona quadrifasciata anthidioides throughout their development. Survival rates above 50% were only observed at insecticide doses lower than 0.0056 µg active ingredient (a.i.)/bee. No sublethal effect on body mass or developmental time was observed in the surviving insects, but the pesticide treatment negatively affected the development of mushroom bodies in the brain and impaired the walking behavior of newly emerged adult workers. Therefore, stingless bee larvae are particularly susceptible to imidacloprid, as it caused both high mortality and sublethal effects that impaired brain development and compromised mobility at the young adult stage. These findings demonstrate the lethal effects of imidacloprid on native stingless bees and provide evidence of novel serious sublethal effects that may compromise colony survival. The ecological and economic importance of neotropical stingless bees as pollinators, their susceptibility to insecticides and the vulnerability of their larvae to insecticide exposure emphasize the importance of studying these species.

Show MeSH
Related in: MedlinePlus