Toxicological evaluation of different pesticides in <i>Tetragonisca angustula</i> Latreille (Hymenoptera, Apidae)

The stingless bee Tetragonisca angustula is an important pollinator of different agricultural and native crops. This study evaluated changes in the relative activity of esterases and critical electrolyte concentration in brain cells after exposure to pesticides malathion and thiamethoxam. Lethal concentration 50% showed greater toxicity of thiamethoxam in relation to malathion. Esterases EST-3 and EST-4 (carboxylesterase) were partially inhibited after contamination by contact and ingestion of malathion and contamination by contact with thiamethoxam, suggesting participation of these esterases in the metabolization of these compounds. The lowest critical electrolyte concentration (CEC) was found after contamination by malathion ingestion (0.15 M), indicating changes in gene expression. The alterations observed in the intensity of EST-3 and EST-4 and the chromatin structure indicate that pesticides can act in gene expression and be used as biomarkers of contaminant residues. Furthermore, knowing the susceptibility of T. angustula bees to pesticides, it would be possible to use this species for biomonitoring environmental quality in preserved areas and agroecosystems.

Keywords:
chromatin; esterases; isoenzymes; stingless bee

Authorship

Ana Lúcia Paz Barateiro Stuchi

Departamento de Zootecnia, Universidade Estadual de Maringá, Maringá, Paraná, Brazil. Universidade Estadual de MaringáBrazilMaringá, Paraná, BrazilDepartamento de Zootecnia, Universidade Estadual de Maringá, Maringá, Paraná, Brazil.

Daiani Rodrigues Moreira ^** Author for correspondence. E-mail: daianibiogeo@hotmail.com

Departamento de Biotecnologia, Genética e Biologia Celular, Universidade Estadual de Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil. Universidade Estadual de MaringáBrazilMaringá, Paraná, BrazilDepartamento de Biotecnologia, Genética e Biologia Celular, Universidade Estadual de Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil.

http://orcid.org/0000-0002-5279-6624

Adriana Aparecida Sinópolis Gigliolli

Douglas Galhardo

José Ricardo Penteado Falco

Vagner de Alencar Arnaut de Toledo

Maria Claudia Colla Ruvolo-Takasusuki

* Author for correspondence. E-mail: daianibiogeo@hotmail.com

SCIMAGO INSTITUTIONS RANKINGS

Tables

Tables (5)

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Table 1
Information on the commercial insecticides, manufacturers, active ingredients, and concentrations used in the bioassays.

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Table 2
Lethal concentrations 50% (LC50) of T. angustula bees exposed to malathion and thiamethoxam, both by contact and ingestion.

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Table 3
Inhibition of esterase activity in T. angustula after contact or ingestion of malathion or thiamethoxam. The minus symbol (-) indicates a lack of inhibition and the symbol (+) indicates partial inhibition.

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Table 4
Nuclear basophilia responses of the chromatin in brain of T. angustula workers after contamination by ingestion and contact with the insecticide malathion [stained with 0.025% toluidine blue (TB) added with MgCl2 in various concentrations (mol L^-1)].

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Table 5
Nuclear basophilia responses of the chromatin in brain of T. angustula workers after contamination by ingestion and contact with the insecticide thiamethoxam [stained with 0.025% toluidine blue (TB) added with MgCl₂ in various concentrations (mol L^-1)].

Table 1 Information on the commercial insecticides, manufacturers, active ingredients, and concentrations used in the bioassays.

Commercial insecticide	Company	Chemical group	Active ingredient (a.i.)	Crop	Concentrations
					Contact (g a.i. L^-1)	Ingestion (g a.i. L^-1)
Malathion EC 500	Cheminova	Organophosphate	Malathion	Tomato (borer)	3.1 × 10^-5	5 × 10^-3
					3.5 × 10^-5	7.5 × 10^-3
					3.7 × 10^-5	0.125
					5 × 10^-5	2.5 × 10^-2
					1.25 × 10^-3	3.7 × 10^-2
Actara 250 WG	Syngenta	Neonicotinoid	Thiamethoxam	Sugarcane	3 × 10^-4	3 × 10^-5
					4.2 × 10^-4	4.8 × 10^-5
					6 × 10^-4	6 × 10^-5
					1.2 × 10^-3	1.2 × 10^-4
					1.8 × 10^-3	1.8 × 10^-4

a.i.: active ingredient

Table 2 Lethal concentrations 50% (LC50) of T. angustula bees exposed to malathion and thiamethoxam, both by contact and ingestion.

Pesticide	Exposure route	LC₅₀ (g a.i. L^-1)	95% Confidence interval
Malathion	contact	6.67 × 10^-6	-----
Malathion	ingestion	1.66 × 10^-2	0.54467 - 2.18486
Thiamethoxam	contact	9.73 × 10^-4	0.06343 - 0.34581
Thiamethoxam	ingestion	1.27 × 10^-3	-0.00039 - 0.5357

a.i: active ingredient.

Table 3 Inhibition of esterase activity in T. angustula after contact or ingestion of malathion or thiamethoxam. The minus symbol (-) indicates a lack of inhibition and the symbol (+) indicates partial inhibition.

Contact exposure			Ingestion exposure
Concentration	Esterase		Concentration	Esterase
Malathion (g a.i. L^-1 )	EST-3	EST-4	Malathion (g a.i. L^-1 )	EST-3	EST-4
3.1 × 10^-5	-	+	5 × 10^-3	-	-
3.5 × 10^-5	-	-	7.5 × 10^-3	-	-
3.7 × 10^-5	+	+	0.125	+	+
5 × 10^-5	-	-	2.5 × 10^-2	-	+
1.25 × 10^-3	-	-	3.7 × 10^-2	-	-
Thiamethoxam (g a.i. L^-1 )			Thiamethoxam (g a.i. L^-1 )
3 × 10^-4	-	-	3 × 10^-5	-	-
4.2 × 10^-4	-	-	4.8 × 10^-5	-	-
6 × 10^-4	+	+	6 × 10^-5	-	-
1.2 × 10^-3	-	-	1.2 × 10^-4	-	-
1.8 × 10^-3	-	-	1.8 × 10^-4	-	-

a.i.: active ingredient.

Table 4 Nuclear basophilia responses of the chromatin in brain of T. angustula workers after contamination by ingestion and contact with the insecticide malathion [stained with 0.025% toluidine blue (TB) added with MgCl2 in various concentrations (mol L^-1)].

Stain	Control	Malathion (contact g a.i. L^-1)	Malathion (ingestion g a.i. L^-1)
Stain	Control	3.1 × 10^-5	7.5 × 10^-3	0.125
TB	Vi	Vi	Vi	Vi
TB + MgCl₂ 0.02 mol L^-1	Vi/Bl	Vi/Bl	Vi/Bl	Vi/Bl
TB + MgCl₂ 0.05 mol L^-1	Bl	Vi/Bl	Vi/Bl	Vi/Bl
TB + MgCl₂ 0.08 mol L^-1	Bl	Vi/Bl	Bl	Vi/Bl
TB + MgCl₂ 0.10 mol L^-1	Bl	Bl	Bl	Bl
TB + MgCl₂ 0.12 mol L^-1	Bl/Gr*	Bl/Gr*	Bl/Gr*	Bl/Gr*
TB + MgCl₂ 0.15 mol L^-1	Bl/Gr*	Bl/Gr*	Gr*	Bl/Gr*
TB + MgCl₂ 0.20 mol L^-1	Bl/Gr*	Gr*	Gr*	Gr*
TB + MgCl₂ 0.30 mol L^-1	Gr*	Gr*	Bl/Gr*	Gr*
CEC value (mol L^-1)	0.20 < CEC < 0.30	0.20	0.15	0.20

Abbreviations: a.i., active ingredient; Vi, violet; Bl, Blue; Gr, Green; *, modification to green coloring; Shading in cells, point of CEC.

Table 5 Nuclear basophilia responses of the chromatin in brain of T. angustula workers after contamination by ingestion and contact with the insecticide thiamethoxam [stained with 0.025% toluidine blue (TB) added with MgCl₂ in various concentrations (mol L^-1)].

Stain	Control	Thiamethoxam (contact g a.i. L^-1)		Thiamethoxam (ingestion g a.i. L^-1)
Stain	Control	4.2 × 10^-4	6 × 10^-4	4.8 × 10^-5	6 × 10^-5
TB	Vi	Vi	Vi	Vi	Vi
TB + MgCl₂ 0.02 mol L^-1	Vi/Bl	Vi	Vi	Vi	Vi
TB + MgCl₂ 0.05 mol L^-1	Bl	Vi/Bl	Vi/Bl	Vi/Bl	Vi/Bl
TB + MgCl₂ 0.08 mol L^-1	Bl	Vi/Bl	Vi/Bl	Vi/Bl	Vi/Bl
TB + MgCl₂ 0.10 mol L^-1	Bl	Bl	Bl	Bl	Bl
TB + MgCl₂ 0.12 mol L^-1	Bl/Gr*	Bl/Gr*	Bl	Bl	Bl
TB + MgCl₂ 0.15 mol L^-1	Bl/Gr*	Bl/Gr*	Bl/Gr*	Bl/Gr*	Bl
TB + MgCl₂ 0.20 mol L^-1	Bl/Gr*	Gr*	Gr*	Gr*	Bl/Gr*
TB + MgCl₂ 0.30 mol L^-1	Gr	Gr*	Gr*	Gr*	Gr*
CEC value (mol L^-1)	0.20<CEC<0.30	0.20	0.20	0.20	0.20

Abbreviations: a.i., active ingredient; Vi, violet; Bl, Blue; *, modification to green coloring; Shading in cells, point of CEC.

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Toxicological evaluation of different pesticides in <i>Tetragonisca angustula</i> Latreille (Hymenoptera, Apidae)

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[1] * Author for correspondence. E-mail: daianibiogeo@hotmail.com